Ecological stages of Maldivian reefs after the coral ... - Springer Link

1 downloads 0 Views 1MB Size Report
Aug 6, 2009 - Paolo Colantoni Æ Carla Morri Æ Carlo Nike Bianchi. Received: 24 ... mature stage represents a balance between biotic (coral growth) and ...
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 widespread 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 biogeomorphological descriptors (living hard corals; rubble and sand; coralline 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: [email protected] 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 erosion 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 predominance 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 Nin˜o, 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 recruitment (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

123

2

Facies (2010) 56:1–11

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 arborescent 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 contribution to reef surface complexity, with an approach requiring the interaction between geomorphology and biology (Andre´foue¨t 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. Table 1 Sites and atolls visited by the Albatros Scientific Cruises in 2006–2007 with indicated the two types of locations (outer and inner reefs), latitude, and longitude

1 2

Study area Some pioneering studies (Stoddart et al. 1966; SpencerDavies 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 Maldives are situated on the central part of the Chagos-Maldives-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 Maldives 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,

Site

Atoll

Location

Latitude

Longitude

Maadhoo Faru

South Male´

Outer reef

3°530 0400 N

73°280 0600 E

Outer reef

0

00

3°39 13 N

73°300 1100 E

0

00

Fufalhi Faru

Felidhoo

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

Fushidiggaru Falhu

South Male´ South Male´

Outer reef

0

00

3°59 33 N

73°310 2900 E

Outer reef

0

00

4°05 34 N

73°230 0800 E

Outer reef

0

00

4°26 01 N

72°580 0000 E

0

00

5 6 7

Boldhuffaru Thoddoo E

Thoddoo

8 9

Thoddoo NE Sexy Finolhu

Thoddoo South Male´

Outer reef Inner reef

4°26 33 N 3°570 1900 N

72°570 5600 E 73°270 3000 E

10

Biology Faru

Felidhoo

Inner reef

3°360 1800 N

73°230 4300 E

Inner reef

0

00

3°36 24 N

72°550 0000 E

Inner reef

0

00

3°58 02 N

72°540 2400 E

Inner reef

0

00

4°05 29 N

73°250 3700 E

Inner reef

0

00

4°24 19 N

73°220 0200 E

Inner reef

4°110 1400 N

72°470 1600 E

Inner reef

0

72°490 2600 E

11 12

Rasheed Finolhu Mushimasmingili

Ari Ari

14

Rasfari

South Male´ North Male´

15

Bodufoludhoo Kuda Giri

Ari

13

16

123

Materials and methods

Ali Kuda Faru

Velidhoo-dhiggaa Kuda Giri

Ari

00

4°09 09 N

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° 2°N

7 8

225°

14 73°E

North Malé Atoll

Rasdhoo Atoll 15 16 6

13

Ari Atoll 12

5

9 4

South Malé Atoll

1

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 Male´, South Male´, 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 estimates 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)

123

4 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)

123

Facies (2010) 56:1–11

Facies (2010) 56:1–11

5

Fig. 3 Depth profiles of outer reef sites. The variability among transects within each site is represented by the grey area. Numbers refer to sites as in Table 1

Distance (m) 0

10

20

30

40

50

60

0

10

20

30

40

50

60

0

1

2

3

4

5

6

7

8

10

20

0

Depth (m)

10

20

0

10

20

0

10

20

Fig. 4 Depth profiles of inner reef sites. The variability among transects within each site is represented by the grey area. Numbers refer to sites as in Table 1

Distance (m) 0

10

20

30

40

50

60

0

10

20

30

40

50

60

0

9

10

11

12

13

14

15

16

10

20

0

Depth (m)

10

20

0

10

20

0

10

20

123

6

RI ¼ 1  Lo =Lr where Lo is the projected length and Lr is the measured length of the transect line. The index ranges between 0 (minimum reef complexity) and 1 (maximum reef complexity). Mann–Whitney U test was used to test the null hypotheses of no differences for either reef dip or roughness values among reefscapes and depth zones. In order to evaluate the ecological stage of reefscapes and depth zones, ternary diagrams representing the three dominant categories of coral reef descriptors (living hard corals; rubble and sand; coralline algae on rock) were plotted. Ternary diagrams were similarly used by Perry et al. (2008) to individuate carbonate production states. Differences in percentage amount of each descriptor among depth zones within each reefscape were assessed through PERMANOVA, a non-parametric multivariate one-way analysis of variance based on permutations (Anderson 2001a). Data were analyzed using Bray–Curtis

123

dissimilarities and 4,999 random permutations, and considering ‘‘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 characterized by moderate wave energy, B by low wave energy, and C by high wave energy (Fig. 6). Euclidean distance

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-Gonza´lez et al. (2006) to describe spatially discrete elements of morphological and biological structure of a coral reef, as defined by clusters. Within each reefscape, 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 position, as sheltered, exposed, or very exposed, and subjected to low, moderate, or high wave energy (Grigg 1998). Nonparametric 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:

Facies (2010) 56:1–11

120 100 80 60 40 20 0 1

2

5

14

7

11

10

A

12

15

16

6

4

8

B

13

9

3

C

Fig. 5 The three reefscapes (A, B, and C) resulting from cluster analysis of horizontal projections of the mean profiles. Numbers refer to sites as in Table 1

3 2

N 1 0

L

M

A

H

L

M

B

H

L

M

H

C

Fig. 6 Number of sites (N) for each reefscape affected by low (L), moderate (M), and high (H) wave energy

Facies (2010) 56:1–11

7

Fig. 7 The two depth zones (reef flat and reef slope) resulting from cluster analysis of horizontal projections of the mean profiles within each of the three reefscapes (A, B, and C). Numbers refer to depth in meters

Reef flat

4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Reef slope

A 120 100 80

60

40

20

0

2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Reef flat

Reef slope B 120 100 80

60

40

20

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Reef flat

Reef slope C

0

120 100 80

60

40

20

0

Analyzing the mean profiles of the sites included in the three reefscapes separately made it possible to identify two different depth zones (Fig. 7): the first between 2–4 and 6– 7 m depth, henceforth called ‘‘reef flat’’; the second between 6–7 and 18 m, henceforth called ‘‘reef slope’’. A minor discontinuity in the reef profiles was recognized in all the three reefscapes around 13 m depth. In reefscapes A and C, the difference in dip angle between flat and slope was significant (U-test, P \ 0.01 in both cases), whereas no difference (U-test, P [ 0.05) was found in reefscape B (Fig. 8a). Overall reef dip angle was different between reefscapes A and B (U-test, P \ 0.001) and between A and C (U-test, P \ 0.05), but not between B and C (U-test, P [ 0.05). Roughness index increased significantly (U-test, P \ 0.01) passing from flat to slope in all reefscapes (Fig. 8b). Again, there was difference in roughness between reefscapes A and B (U-test, P \ 0.01) and between A and C (U-test, P \ 0.05), but no between B and C (U-test, P [ 0.05). Ecological stages Significant differences in percentage amount of geomorphological and biological descriptors between flat and slope were found in all the three reefscapes (PERMANOVA, 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 distributed 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

a

50 40

**

ns

**

B

C

30 20 10 0

A

***

ns

*

b

0.6

0.4

RI

Depth zones

Dip angle (°)

Euclidean distance

**

**

**

0.2

0.0

B

A

**

C ns

* Reef flat

Reef slope

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,

123

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 representing the dominant geomorphological and biological descriptors (living hard coral, rubble and sand, 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

Hard coral

Hard coral

A

Rubble and sand

B

Coralline algae

Rubble and sand Reef flat

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

123

Hard coral

C

Coralline Rubble algae and sand

Coralline algae

Reef slope

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 distinction between outer and inner reefs: waves are able to propagate through large and deep passes in the atoll rim,

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 similar 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 contribute 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 reefscapes 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 premortality 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 prebleaching 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 Male´) organized 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 photographs. Thanks are also due to an anonymous referee whose comments greatly improved the paper.

References Allison WR (1995) Changes in the Maldivian reef system. Coast Manage Trop Asia 4:6–8 Anderson MJ (2001a) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46 Anderson MJ (2001b) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639

123

10 Andre´foue¨t S, Guzman HM (2005) Coral reef distribution, status and geomorphology–biodiversity relationship in Kuna Yala (San Blas) archipelago, Caribbean Panama. Coral Reefs 24:31–42 Arias-Gonza´lez JE, Done TJ, Page CA, Cheal AJ, Kininmonth S, Garza-Pe´rez JR (2006) Towards a reefscape ecology: relating biomass and trophic structure of fish assemblages to habitat at Davies Reef, Australia. Mar Ecol Prog Ser 320:29–41 Barton AD, Casey KS (2005) Climatological context for large-scale coral bleaching. Coral Reefs 24:536–554 Bianchi CN, Colantoni P, Geister J, Morri C (1997) Reef geomorphology, sediments and ecological zonation at Felidu Atoll, Maldive Islands (Indian Ocean). Proc 8th Int Coral Reef Symp 1:431–436 Bianchi CN, Pronzato R, Cattaneo-Vietti R, Benedetti Cecchi L, Morri C, Pansini M, Chemello R, Milazzo M, Fraschetti S, Terlizzi A, Peirano A, Salvati E, Benzoni F, Calcinai B, Cerrano C, Bavestrello G (2004) Hard bottoms. Biol Mar Mediterr 11:185–215 Bianchi CN, Morri C, Pichon M, Benzoni F, Colantoni P, Baldelli G, Sandrini M (2006a) Dynamics and pattern of coral recolonization following the 1998 bleaching event in the reefs of the Maldives. Proc 10th Int Coral Reef Symp 1:30–37 Bianchi CN, Pichon M, Morri C, Colantoni P, Benzoni F, Baldelli G, Sandrini M (2006b) Le suivi du blanchissement des coraux aux Maldives: lec¸ons a` tirer et nouvelles hypothe`ses. Oce´anis: Serie de Documents Oce´anographiques 29:325–354 Bianchi CN, Morri C, Colantoni P, Sandrini M (2009) Italian research in the Maldives. Reef Encount 37:17 Burt J, Bartholomew A, Usseglio P (2008) Recovery of corals a decade after a bleaching event in Dubai, United Arab Emirates. Mar Biol 154:27–36 Ciarapica G, Passeri L (1993) An overview of the Maldivian coral reefs in Felidu and North Male´ atolls (Indian Ocean): platform drowning by ecological crises. Facies 28:33–66 Clua E, Legendre P, Vigliola L, Magron F, Kulbicki M, Sarramegna S, Labrosse P, Galzin R (2006) Medium scale approach (MSA) for improved assessment of coral reef fish habitat. J Exp Mar Biol Ecol 333:219–230 Colantoni P (2007) L’immersione scientifica. Tecniche di indagine subacquea. Editrice La Mandragora, Imola Colantoni P, Baldelli G, Bianchi CN, Capaccioni B, Morri C, Sandrini M, Tassi F (2003) A cave flooded by marine water with hydrogen sulphide highlights the recent evolution of the Maldives (Indian Ocean): preliminary notes. Le Grotte d’Italia, s.V. 4:29–37 Done TJ (1983) Coral zonation: its nature and significance. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 107–147 Dullo WC (2005) Coral growth and reef growth: a brief review. Facies 51:33–48 Gischler E (2006) Sedimentation on Rasdhoo and Ari Atolls, Maldives, Indian Ocean. Facies 52:341–360 Gischler E, Kikinger R (2006) Effects of the tsunami of 26 December 2004 on Rasdhoo and Northern Ari Atolls, Maldives. Atoll Res Bull 561:61–74 Gischler E, Hudson JH, Pisera A (2008) Late Quaternary reef growth and sea level in the Maldives (Indian Ocean). Mar Geol 250:104–113 Goreau TF (1959) The ecology of Jamaican coral reefs. I. species composition and zonation. Ecology 40:67–90 Goreau TJ, McClanahan TR, Hayes RL, Strong A (2000) Conservation of coral reefs after the 1998 global bleaching event. Conserv Biol 14:5–15 Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci USA 103:8425–8429

123

Facies (2010) 56:1–11 Grigg RW (1998) Holocene coral reef accretion in Hawaii: a function of wave exposure and sea level history. Coral Reefs 17:263–272 Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279 Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866 Holmes KE, Edinger EN, Hariyadi HR, Limmon GV, Risk MJ (2000) Bioerosion of live massive corals and branching coral rubble on Indonesian coral reefs. Mar Pollut Bull 40:606–617 Hopley D, Smithers SG, Parnell KE (2007) The geomorphology of the Great Barrier Reef: development, diversity, and change. Cambridge University Press, Cambridge Kench PS, Brander RW, Parnell KE, McLean RF (2006) Wave energy gradients across a Maldivian Atoll: implications for island geomorphology. Geomorphology 81:1–17 Lasagna R, Gattorna I, Albertelli G, Morri C, Bianchi CN (2006) Substrate heterogeneity and relation with coral recruitment in coral reefs of the Maldives (Indian Ocean). Biol Mar Mediterr 13:88–89 Lasagna R, Albertelli G, Giovannetti E, Grondona M, Milani A, Morri C, Bianchi CN (2008) Status of Maldivian reefs eight years after the 1998 coral mass mortality. Chem Ecol 24:67–72 Loch K, Loch W, Schuhmacher H, See WR (2002) Coral recruitment and regeneration on a Maldivian reef 21 months after the coral bleaching event of 1998. PSZN Mar Ecol 23:219–236 Loch K, Loch W, Schuhmacher H, See WR (2004) Coral recruitment, regeneration on a Maldivian reef four years after the coral bleaching event of 1998. Part 2: 2001–2002. PSZN Mar Ecol 25:145–154 Madin JS, Black KP, Connolly SR (2006) Scaling water motion on coral reefs: from regional to organismal scales. Coral Reefs 25:635–644 McClanahan TR (2000) Bleaching damage and recovery potential of Maldivian coral reefs. Mar Pollut Bull 40:587–597 McClanahan TR, Ateweberhan M, Graham NAJ, Wilson SK, Ruiz Sebastia´n C, Guillaume MMM, Bruggemann JH (2007) Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Mar Ecol Prog Ser 337:1–13 Morri C, Bianchi CN, Aliani S (1995) Coral reefs at Gangehi (North Ari Atoll, Maldive Islands). Publ Serv Ge´ol Luxemb 29:3–12 Perry CT, Hepburn LJ (2008) Syn-depositional alteration of coral reef framework through bioerosion, encrustation and cementation: taphonomic signatures of reef accretion and reef depositional events. Earth Sci Rev 86:106–144 Perry CT, Spencer T, Kench PS (2008) Carbonate budgets and reef production states: a geomorphic perspective on the ecological phase-shift concept. Coral Reefs 27:853–866 Pichon M (1974) Dynamics of benthic communities in the coral reefs of Tule´ar (Madagascar): succession and transformation of the biotopes through tract evolution. Proc 2nd Int Coral Reef Symp 2:55–68 Pichon M, Benzoni F (2007) Taxonomic re-appraisal of zooxanthellate scleractinian corals in the Maldive Archipelago. Zootaxa 1441:21–33 Price RG, Clark S (2000) The Maldives. In: Sheppard CRC (ed) Seas at the millennium: an environmental evaluation. Elsevier Press, Amsterdam, pp 199–219 Rasser MW, Riegl B (2002) Holocene coral reef rubble and its binding agents. Coral Reefs 21:57–72 Riedl R (1971) Water movement–animals. In: Kinne O (ed) Marine ecology. Wiley, New York, pp 1123–1156 Riegl B, Piller WE (2000) 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, pp 71–88

Facies (2010) 56:1–11 Risk MJ, Sluka R (2000) The Maldives: a nation of atolls. In: McClanahan TR, Sheppard CRC, Obura D (eds) Coral reefs in the Indian Ocean: their ecology and conservation. University Press, Oxford, pp 325–351 Scheer G (1971) Coral reefs and coral genera in the Red Sea and Indian Ocean. Symp Zool Soc Lond 28:329–367 Schuhmacher H, Loch K, Loch W, See WR (2005) The aftermath of coral bleaching on a Maldivian reef—a quantitative study. Facies 51:80–92 Sheppard CRC, Spalding M, Bradshaw C, Wilson S (2002) Erosion vs. recovery of coral reefs after 1998 El Nin˜o: Chagos reefs, Indian Ocean. Ambio 31:40–48 Sheppard CRC, Dixon DJ, Gourlay M, Sheppard A, Payet R (2005) Coral mortality increases wave energy reaching shores protected by reef flats: examples from the Seychelles. Estuar Coast Shelf Sci 64:223–234 Sheppard CRC, Harris A, Sheppard A (2008) Archipelago-wide coral recovery patterns since 1998 in the Chagos Archipelago, Central Indian Ocean. Mar Ecol Prog Ser 362:109–117 Smith LD, Gilmour JP, Heyward AJ (2008) Resilience of coral communities on an isolated system of reefs following catastrophic mass-bleaching. Coral Reefs 27:197–205

11 Spencer T, Viles H (2002) Bioconstruction, bioerosion and disturbance on tropical coasts: coral reefs and rocky limestone shores. Geomorphology 48:23–50 Spencer-Davies P, Stoddart DR, Sigee DC (1971) Reef forms of Addu Atoll, Maldive Islands. Symp Zool Soc Lond 28:217–259 Stoddart DR, Spencer-Davies P, Keith AC (1966) Geomorphology of Addu Atoll. Atoll Res Bull 116:13–41 Wilkinson C, Linden O, Cesar H, Hodgson G, Strong AE (1999) Ecological and socioeconomic impacts of 1998 coral mortality in the Indian Ocean: an ENSO impact and warming of future changes. Ambio 28:188–196 Wilson SK, Graham NAJ, Polunin NVC (2007) Appraisal of visual assessments of habitat complexity and benthic composition on coral reefs. Mar Biol 151:1069–1076 Woodroffe CD (1992) Morphology and evolution of reefs islands in the Maldives. Proc 7th Int Coral Reef Symp 2:1217–1226 Zahir H (2000) Status of the coral reefs of Maldives after the bleaching event in 1998. In: Souter D, Obura D, Linde´n O (eds) Coral reef degradation in the Indian Ocean. Cordio, Stockholm, pp 64–68

123