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
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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 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
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Materials and methods
Ali Kuda Faru
Velidhoo-dhiggaa Kuda Giri
Ari
00
4°09 09 N
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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)
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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)
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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
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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
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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
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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,
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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
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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,
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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.
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