Volume 30, Issue 4 pp. 405-415

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Skeletal linear extension rates of the foliose scleractinian coral Merulina ampliata (Ellis & Solander, 1786) in a turbid environment

Angela Dikou,

Angela Dikou

Department of Ichthyology and Aquatic Sciences, University of Thessaly, Volos, Greece

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Angela Dikou,

Angela Dikou

Department of Ichthyology and Aquatic Sciences, University of Thessaly, Volos, Greece

Search for more papers by this author

First published: 20 November 2009

https://doi.org/10.1111/j.1439-0485.2009.00295.x

Citations: 10

Angela Dikou, Department of Ichthyology and Aquatic Sciences, University of Thessaly, Volos, Greece.
E-mail: [email protected]

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Abstract

Skeletal linear extension rates of a foliaceous, IndoPacific, skiophilous, heterotrophic, scleractinian Merulina ampliata (Ellis & Solander 1786) were obtained along a sediment/nutrient load gradient at the southern islands of Singapore. Measurements were made during November 1999– November 2000 using the alizarin red-S staining technique. Suspended particulate matter concentration (r²_adj = 0.76), turbidity (r²_adj = 0.59), the organic content of suspended sediments (r² = 0.50), and nitrite-nitrate concentration (r²_adj = 0.50) were significant predictors of the skeletal linear extension rate of M. ampliata. Maximum linear extension growth rates of M. ampliata (mean ± SD: 1.43 ± 0.67–3.26 ± 0.59 cm·year⁻¹) were comparable to 15-year-old accounts at the same research sites, indicating adaptation to low-light, high-sediment waters.

Problem

Human activities on land (e.g. agriculture, deforestation, coastal development) and at sea (e.g. dredging, aquaculture, municipal/industrial sewage disposal) alter the quality of coastal waters worldwide through the increases in sediments, nutrients, pollutants, and pathogens (GESAMP 2001; Hassan et al. 2005). In tropical and subtropical regions, skeletal growth of zooxanthellate scleractinian corals (linear extension, bulk density or calcification) has been used as a promising sublethal indicator of reef health (Dodge et al. 1974; Bak 1978; Tomascik & Sander 1985). In fact, coral skeletons can provide a record of the environmental conditions at the time of growth (Scoffin et al. 1989), while their growth integrates a number of physiological processes through the scope for growth (Brown & Howard 1985). However, following short-term or prolonged change in environmental conditions, some scleractinian coral species showed change in some but not all growth characteristics (Dodge & Brass 1984); divergent changes among growth characteristics (Edinger et al. 2000; Koop et al. 2001), or no change in any of their growth characteristics, despite evidence of marked changes in coral cover and diversity (Hudson et al. 1982; Brown et al. 1990; Chansang et al. 1992). It seems that the ‘sensitivity’ of scleractinian corals’ growth to environmental alteration varies with species and location and that ‘… A considerable amount of work is needed before we can begin to understand and, hopefully, predict which growth characteristic of which species is likely to respond to a given environmental change in a particular location…’ (Lough & Barnes 1997).

The variability in the response of skeletal growth of scleractinian corals to increases in terrestrially derived material, nutrients and sediments in particular, may reflect the differential importance of the four agents affecting coral growth: (i) dissolved inorganic nutrients; (ii) particulate organic matter; (iii) sedimentation; and (iv) turbidity, along with spatial, physical, hydrodynamic and biological properties of coral reefs, sediment type/quality, and frequency of sediment impact (reviews by Brown & Howard 1985; Pastorok & Bilyard 1985; Rogers 1990; Brown 1997; Fabricius 2005; Kruzic & Benkovic 2008). Furthermore, we now know that scleractinian corals can acclimatize/adapt to increased sediment and nutrient loads through morphological (e.g. changes in coral shape, form, and orientation, Todd 2008), physiological (e.g. changes in photosynthetic apparatus, Titlyanov 1981) and feeding plasticity (e.g. change in dependence on heterotrophy, Anthony & Fabricius 2000) or interactions among them (Anthony & Hoegh-Guldberg 2003; Hoogenboom et al. 2008) in order to optimize energy acquisition. Finally, up to date the bulk of anthropogenic impact studies on coral growth involved only a few massive (mainly of the genus Porites in the Indo-Pacific and of Montastrea annularis in the Caribbean) and branching species (mainly of the genus Acropora), whose abundance/cover distinguishes them as primary reef builders on reefs. The interplay of the aforementioned factors impedes the identification of widely applicable, exclusive, and ‘sensitive’ coral species and growth parameters when assessing the effects of increased nutrients and sediments. Consequently, we still have only a tentative speculation on threshold limits to coral growth under sediment and nutrient stress (Hawker & Connell 1989).

The reefs of the southern islands of Singapore are used as a case study to assess and evaluate the chronic effects of increase in sediment and/or nutrient loads on skeletal linear extension of the scleractinian coral Merulina ampliata (Ellis & Solander, 1786). Merulina ampliata, a potentially large (1–2 m in diameter) foliaceous species, is a widely distributed scleractinian on many Indo-Pacific coral reefs (Veron & Stafford-Smith 2000). The objectives of the study were to (i) determine whether the skeletal linear extension rate of M. ampliata varies among stations along a sediment/nutrient load gradient and (ii) relate skeletal linear extension rate to environmental variables along the gradient, particularly those generally thought to affect coral skeletal growth.

Material and Methods

Study sites

Coral reefs off the main island of Singapore (latitudes 1^o09′ N and 1^o29′ N, longitudes 103^o36′ E and 104^o25′ E; ≈ 3.5 million people; Fig. 1) have been subjected to increased sediment load during the last 40 years mainly due to reclamation and dredging activities. The sources of sediment load in the waters surrounding the reefs of the southern islands of Singapore are multiple, mobile and extend their effects at the spatial scale of a few kilometres. They have led to an increase in sediment load and, possibly, eutrophication, and a decrease in water clarity and light penetration (Dikou & van Woesik 2006). In the last 30 years a 30-fold increase in primary productivity has been found despite levels of nutrients remaining largely unaltered (Gin et al. 2000).

Details are in the caption following the image — **Figure 1**
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Map of the Republic of Singapore, the southern islands and studied reef sites. C, 01^° 15′ 26′′ N, 103^° 45′ 12′′ E; S, 01^° 12′ 10′′ N, 103^° 45′ 16′′ E; PH, 01^° 13′ 35′′ N, 103^° 44′ 48′′ E; R, 01^° 13′ 36′′ N, 103^° 44′ 53′′ E.

In the present work we studied four reefs at increasing distances from the main island of Singapore (Fig. 1). The Cyrene patch reef (C, 4.5 km distance) is situated in the middle of a fairway of maritime vessels proceeding to and from the nearby port, with petro-chemical and industrial facilities; ship groundings have been reported. The Pulau Hantu fringing reef (PH, 7.5 km distance) was reclaimed in 1974, losing most of its reef flat and obtaining a rock wall; today it is used by recreational SCUBA divers. The Semakau fringing reef (S, 8 km distance), which was inhabited till the mid-1970s, has functioned as earth spoils and solid waste dumping ground since 1990s; it is also used for subsidence fishing and reef collecting. The Raffles lighthouse fringing reef (R, 15 km distance), was reclaimed in 1976; most of its original reef flat was covered and a rock wall was build. No Acanthaster planci outbreaks have been reported on these reefs. Bleaching events occurred during the summers 1998 and 2002. Sampling sites of environmental variables, growth rates and benthic cover were uniformly set along the west coast of the four reefs studied (Fig. 1).

Environmental monitoring

The studied reefs are under the influence of the southwest monsoon from May to September and of the northeast monsoon from November to March (Chia 1974; Watts 1974). To assess the influence of the monsoons on the main physical seawater variables of the reefs, 10 seawater variables were sampled twice a month (when possible) from April 1999 to November 2000, along the west coast of the four reef sites at 4 m depth. They included physic-chemical factors such as salinity (SAL), temperature (T), and dissolved oxygen (DO) concentration. The sediment load on the studied reefs was assessed through suspended particulate matter (SPM) concentration, the downward flux of suspended particulate matter (DF-SPM) and the light extinction coefficient (K). To evaluate eutrophication, nitrite + nitrate (NO₂ + NO₃), phosphate (PO₄-P) and chlorophyll a (CHLA) concentrations were determined. The volatile portion of suspended particulate matter was used to assess the proportion of suspended sediment that is organic, i.e. the particulate organic matter (POM) concentration. Salinity was measured with an ATAGO hand refractometer. Turbidity was measured with a Secchi disk. The depth (D) of the Secchi disk in metres was used to calculate the light extinction coefficient K (= 1.7/D). Temperature and dissolved oxygen were measured with a portable YSI, model 57, oxygen meter at ≈ 4 m depth. A 2 l-volume Van Dorn sampler was used to collect seawater at ≈ 4 m depth. On deck, the seawater was sub-sampled for dissolved inorganic nutrients (nitrite + nitrate and phosphate), suspended particulate matter, and chlorophyll a. Samples for nutrients were temporarily stored in a cooler box during field trips and subsequently stored in −20 °C until laboratory analysis. Concentrations of nutrients were assessed with a flow injection analyser, model Technicon TRAACS 800 (Technicon Instruments Corporation, Tarrytown, NY, USA). One litre of each seawater sample was used for assessing total suspended solids and 1 l was used to assess chlorophyll a concentration. Suspended particulate matter was measured by filtering 1 l of seawater (n = 2) through a pre-combusted, pre-washed, and pre-weighed Whatman GF/C filter (42.5 mm Ø), drying the filter at 110 °C for at least 1.5 h and weighing. Combustion of the filter at 550 °C for 20 min gave the organic content of total suspended solids (Greenberg et al. 1985). Chlorophyll a concentration was measured following the standard procedure of Parsons et al. (1984). The downward flux of suspended particulate matter was measured with sediment traps (5 cm height × 13 cm diameter) secured on metal rods approximately 20 cm above the substrate (four sets of three traps in each site) at ≈ 4 m depth. The traps were retrieved monthly (when possible), and the sediment was filtered through a pre-weighed Whatman qualitative filter (150 mm Ø), dried at 60 °C for 2–3 days and subsequently weighed.

Skeletal linear extension monitoring

The growth of a number of specimens of M. ampliata was followed along the west coast of four reefs from April 1999 to November 2000 through SCUBA diving. In the field, colonies of M. ampliata were collected along the upper reef slope, at 3–4 m below MSL, fixed to concrete slabs (10 × 25 × 2.5 cm) with underwater cement (epoxy resin), tagged and repositioned at the four research sites and at the same depth of 3–4 m below MSL. To measure linear extension rate, alizarin red-S stain (12 mg·l⁻¹) was used in situ as a date marker following Dustan’s (1975) method. There were four staining periods (P1–P4): P1 – April–May 1999; P2 – June–November 1999; P3 – November 1999–March 2000; P4 – March–November 2000, Table 1). Staining periods P1 and P2 were test trials.

Table 1. Dates of application of alizarin stain at the four reef sites for the four periods of application (P1–P4). Duration of each period is given in number of days in parentheses.

Staining periods	Reef sites
Staining periods	Cyrene	Pulau Hantu	Semakau	Raffles
P1	7.4.99–2.6.99 (56)	7.4.99–2.6.99 (56)	–	7.4.99–1.6.99 (55)
P2	2.6.99–18.11.99 (136)	2.6.99–17.11.99 (135)	15.6.99–19.11.99 (124)	1.6.99–16.11.99 (135)
P3	18.11.99–30.3.00 (122)	17.11.99–4.3.00 (124)	19.11.99–18.3.00 (134)	16.11.99–20.3.00 (141)
P4	30.3.00–10.11.00 (225)	4.3.00–17.11.00 (258)	18.3.00–8.11.00 (233)	20.3.00–7.11.00 (230)

After corals were removed from the sea, they were left for 2 days inside plastic buckets containing freshwater and bleaching solution so that the dead tissue could easily be removed with a water jet. They were then re-tagged for convenience and their initial and final dimensions were recorded. Colonies were left to dry under the sun for approximately 2 months. A total of 17, 24, 20 and 31 coral specimens were collected from Cyrene, Pulau Hantu, Semakau and Raffles reef sites, respectively, during the mensurative experiment, but only 5, 11, 12, and 23 coral specimens were used for the extraction of linear skeletal extension measurements (Appendix I). Specimens that showed obvious signs of stress during the experiment, such as bleaching or partial mortality (see also Dodge et al. 1984), were excluded and substituted with new specimens. Thus, specimens carried a maximum of four and a minimum of two alizarin stain-rings at the end of the experiment (Fig. 2).

Maximum (n = 1 measurements on each specimen) and mean (n = 5 measurements on each specimen) skeletal linear extension measurements of M. ampliata were taken under a magnifying lens using a drafting compass. The position of maximum skeletal linear extension was easy to detect as all colonies were laminar and flat. The positions of the five independent measurements for the assessment of the mean skeletal linear extension rate were determined by generating random numbers between 1 and 360, which correspond to the 360^° of a cycle. The compass was used to measure with increased accuracy the distance between two successive alizarin marks and between the last alizarin ring and the edge of the colony on the same specimen. The compass was then placed on the top of a ruler and the distance between the end-points of the compass was recorded in mm.

To compare and contrast patterns of skeletal linear extension rates with patterns of M. ampliata colony size, the benthos of the four reef sites was surveyed from September 2000 to January 2001 using SCUBA to record the size (as areal cover in cm²) of M. ampliata colonies encountered under randomly positioned 1-m² quadrats (n = 12), along the reef crest at ≈ 4 m depth and at the same localities that seawater variables and skeletal linear extension monitoring took place.

Data analysis

Data analysis of both environmental variables and skeletal linear extension rates of M. ampliata involved only time periods P3 and P4, which correspond to a year’s cycle with convenient distinction between the two monsoons and maximum possible number of specimens for the four studied reefs. Differences in environmental variables and in skeletal linear extension rates among the four reef sites and two staining periods were evaluated through two-factor repeated measures analysis of variance (ANOVA, random effects or Model I). Prior to ANOVA, all datasets were tested for the basic assumptions of normality and homogeneity of variance with the Shapiro-Wilk W statistic and Levene’s test, respectively. To satisfy the assumptions of normality and homogeneity of variance, nitrite-nitrate concentration (NO₂ + NO₃), phosphate concentration (PO₄-P), and light extinction coefficient (K) required a logarithmic, a logarithmic, and a power (λ = −0.315) transformation, respectively. The rest of the environmental variables were analyzed with the non-parametric equivalent to ANOVA, the Kruskal–Wallis test. The Kruskal–Wallis test was also employed to test whether there were statistically significant differences in median colony size of M. ampliata in the field among the four studied reef sites.

To determine whether the skeletal linear extension rate of M. ampliata was independent of colony size, simple linear regression analysis was employed using measurements of linear extension rate of M. ampliata specimens from Raffles during the first trial staining period (P1; 7.4.99–1.6.99). To evaluate whether the staining technique interfered with coral growth during periods of study P3 and P4, four (one for each research site) two-way (factors: number of stainings, time) repeated measures ANOVAs were employed.

Simple linear regressions (n = 4 reefs × 2 time) of mean skeletal linear extension rates of M. ampliata with mean values of the 10 environmental variables were determined using Model I regression. Their performance in terms of variance explained was compared to corresponding logarithmic, quadratic, power and exponential regressions (n = 4 reefs × 2 time) to test for non-linear relationships and threshold responses. Also, the fit of the same models, i.e. linear, logarithmic, quadratic, power and exponential, were tested for the relationships between distance from the main island of Singapore (D) and mean annual values of the skeletal linear extension rate and of the 10 environmental variables (n = 4 reefs).

Results

Seawater monitoring indicated a turbid environment (Fig. 3). There were significant differences among the four reef sites in Box-Cox transformed (λ = −0.315) mean values of the light extinction coefficient (two-factor ANOVA, F_site = 19.6241, P < 0.05), median chlorophyll a concentration (Kruskal–Wallis test, H_3,138 = 7.9112, P < 0.05), median downward flux of suspended particulate matter (Kruskal–Wallis test, H_3,231 = 116.6037, P < 0.01), and median suspended particulate matter concentration (Kruskal–Wallis test, H_3,152 = 12.817, P < 0.01).

There were also significant differences between the two staining periods P3 and P4 in log(x) transformed mean values of PO₄-P (two-factor ANOVA, F_time = 8.3880, P < 0.01), median dissolved oxygen concentration (Kruskal–Wallis test, H_1,57 = 8.3970, P < 0.01), median salinity (Kruskal–Wallis test, H_1,68 = 14.0650, P < 0.01), median suspended particulate matter concentration (Kruskal–Wallis test, H_1,152 = 7.9290, P < 0.01), median temperature (Kruskal–Wallis test, H_1,65 = 23.4297, P < 0.01) and median particulate organic matter concentration (Kruskal–Wallis test, H_1,167 = 14.2460, P < 0.01) (Fig. 3).

The mean skeletal linear extension rate of M. ampliata was not dependent on colony size over the size range studied [t(9) = 0.5831, P = 0.5741]. Also, additional numbers of stain-rings did not retard growth at any of the four sites (2-way ANOVA Cyrene: F_stainings = 0.8162, P = 0.4329; Semakau: F_stainings = 14.9170, P < 0.01) but mean linear extension rate of colonies with two stain rings was smaller than that of colonies with three stain rings (Pulau Hantu: F_stainings = 0.3888, P = 0.69; Raffles: F_stainings = 0.66, P = 0.52).

Spatial and temporal variation in the maximum and mean skeletal extension rate of M. ampliata along the west coast of the southern islands of Singapore is presented in Fig. 4. There were significant differences in mean skeletal extension rate of M. ampliata among sites and between times (2-way ANOVA F_site = 8.0784, P < 0.01; F_time = 69.3801, P < 0.01). There was also a statistically significant interaction between the factors site and time (F_{site × time} = 16.7183, P < 0.01).

Simple linear regressions of mean skeletal linear extension rates of M. ampliata on mean environmental variables are presented in Table 2. Suspended particulate matter concentration was the best univariate predictor of skeletal linear extension rates. The corresponding linear regression indicated a coefficient of growth of 0.018 cm·mo⁻¹ per mg·l⁻¹ for the suspended particulate matter concentration range 4.07–15.22 mg·l⁻¹. The light extinction coefficient, nitrite-nitrate concentration and particulate organic matter concentration showed weaker significant relationships with the skeletal linear extension rate of M. ampliata. The corresponding linear regressions indicated coefficients of growth of 0.345, 0.006, and 0.072 cm·mo⁻¹ per unit change of the light extinction coefficient, nitrite-nitrate concentration and particulate organic matter concentration, respectively, for their respective range of values. Although linear models provided the best fit to the data for suspended particulate matter and particulate organic matter concentrations, the exponential and the logarithmic models were a better fit to the data for the light extinction coefficient (GR = 1.709e^−2.568K, r²_adj =0.72, P = 0.0049) and nitrite–nitrate concentration [GR = −0.175Ln(NO₂ + NO₃)+ 0.777], r²_adj = 0.53, P = 0.0238), respectively. The distance from the main island of Singapore was shown to be an effective surrogate predictor of the mean annual skeletal linear extension rate of M. ampliata and of environmental variables such as suspended particulate matter, particulate organic matter and dissolved oxygen concentrations, the downward flux of suspended particulate matter and the light extinction coefficient (non-linear responses), albeit replication was small and, thus, regressions were marginally significant (Table 3).

Table 2. Regression equations for predicting linear extension growth rates (GR in cm·month⁻¹) of M. ampliata at the southern islands of Singapore from light extinction coefficient (K in m), chlorophyll a concentration (CHLA in mg·m⁻³), downward flux of suspended particulate matter (DF-SPM in mg·cm⁻²·day⁻¹), dissolved oxygen concentration (DO in mg·l⁻¹), nitrite-nitrate concentration (NO₂ + NO₃ in ppb), phosphate concentration (PO₄-P in ppb), salinity (SAL in ‰), suspended particulate matter concentration (SPM in mg·l⁻¹), temperature (T in °C), and particulate organic matter concentration (POM in mg·l⁻¹).

Simple regressions	r²_adj	F test	P
1. GR = −0.018*SPM + 0.343	0.76	21.661	0.003
2. GR = −0.345*K + 0.496	0.59	10.979	0.016
3. GR = −0.006* NO₂ + NO₃ + 0.380	0.50	7.906	0.031
4. GR = −0.072*POM + 0.302	0.50	1.701	0.030
5. GR = −1.308*CHLA + 0.348	0.33	4.385	0.081
6. GR = 0.114*DO − 0.541	0.26	3.399	0.115
7. GR = 0.052*SAL − 1.529	0.13	2.047	0.204
8. GR = −0.014*PO₄–P + 0.368	0.09	1.701	0.239
9. GR = −0.050*T + 1.611	0.08	1.594	0.255
10. GR = −0.007*DFSPM + 0.217	−0.09	0.454	0.530

Table 3. Results of the best fit regression model among the linear, quadratic, exponential, power and logarithmic transformations, for predicting linear extension growth rate (GR in cm·year⁻¹) of M. ampliata, dissolved oxygen concentration (mean annual DO in mg·l⁻¹), downward flux of suspended particulate matter (mean annual SPM in mg·cm⁻²·day⁻¹), light extinction coefficient (mean annual K in m), and chlorophyll a concentration (mean annual CHLA in mg·m⁻³), nitrite-nitrate concentration (mean annual NO₂ + NO₃ in ppb), phosphate concentration (mean annual PO₄-P in ppb), salinity (mean annual SAL in ‰), suspended particulate matter concentration (mean annual SPM in mg·l⁻¹), temperature (mean annual T in °C), and particulate organic matter concentration (mean annual POM in mg·l⁻¹) from distance (D) from the main island of Singapore (n = 4 reefs).

Best fit regression model	r²_adj	F test	P
1. GR = −0.005D²+1.051D	0.98	97.866	0.071
2. DO = −0.010D²+0.206D	0.98	92.190	0.073
3. SPM = 0.174D²− 3.835D + 26.716	0.97	57.504	0.093
4. POM = 0.022D²− 0.490D + 3.932	0.96	35.461	0.118
5. DFSPM = −0.252Ln(D) + 27.532	0.88	22.385	0.042
6. K = 1.834*e^−0.348D	0.79	12.009	0.074
7. CHLA = 0.257*e^−0.352D	0.56	4.733	0.162
8. NO₂ + NO₃ = −6.973Ln(D) + 45.193	0.30	2.315	0.267
9. T = 0.001Ln(D) + 28.657	−0.25	0.391	0.596
10. PO₄-P = 11.792*e^0.007D	−0.29	0.314	0.632
11. SAL = 32.682*e^0.002D	−0.40	0.142	0.742

Although median colony size (in cm²) of M. ampliata in the field did not differ significantly among the four sites (Kruskal–Wallis test, H_3,22 = 5.8520, P = 0.1190) there was a larger range of colony sizes at Pulau Hantu (13.8–811.4 cm²), Semakau (57.2–1068.5 cm²) and Raffles (26.4–293.3 cm²) than at Cyrene (7.7–70.8 cm²) (Bartlett Chi-square test(2) = 8.589, P = 0.0136).

Discussion

Environmental conditions close to the main island of Singapore adversely affected skeletal linear extension rates of M. ampliata. Mean and maximum rates at the site closest to the main island of Singapore (Cyrene, mean ± SD: 1.02 ± 0.31 cm·year⁻¹; max ± SD: 1.43 ± 0.67 cm·year⁻¹) were 2.0 and 2.5 times, respectively, lower than those at the furthest site from the main island of Singapore (Raffles, mean ± SD: 2.46 ± 0.61 cm·year⁻¹; max ± SD: 3.26 ± 0.59 cm·year⁻¹). Lane (1991) reported a comparable maximum annual skeletal linear extension rate of 1.1 and 3.7 cm·year⁻¹ for M. ampliata (extrapolated from measurements within a 6-month interval) at Cyrene and Raffles, respectively, 15 years prior to this study. Furthermore, a larger colony size range was found at Raffles than at Cyrene in this study. Indeed, colonies larger than 1-m diameter of M. ampliata with apparent signs of fission were encountered at Semakau and Raffles during field assessment.

The effect of the factor time on the skeletal linear extension rate of M. ampliata depended on the reef site studied. Thus, M. ampliata at Cyrene and Semakau had significantly lower mean skeletal linear extension rates during period P4 (March–November) than during period P3 (November–March). Period P4 contains the inter-monsoon periods and the southwest monsoon (May–September), which is rainy with less sunshine and stronger currents compared to the northeast monsoon (November–March). Thus, average values of suspended particulate matter concentration, light extinction coefficient, particulate organic matter concentration, and nitrite-nitrate concentration for the four reef sites were respectively 1.7, 1.1, 2.4 and 1.4 times higher during period P4 compared to period P3. Increase in sediment load increases turbidity and reduces the light available for photosynthesis (Te 1997) but at the same time provides extra organic food that may compensate for the light reduction (Anthony & Fabricius 2000), at least for the mixotrophic coral species (Lewis 1977; Sebens 1987). Strong currents keep sediments in suspension inhibiting their settlement on corals and subsequent fission and/or smothering of corals and facilitate the removal of mucus nets trapping sediments. Similarly, skeletal linear extension of the branching scleractinian Acropora formosa was found to be approximately double during the dry northeast monsoon compared to the wet southwest monsoon at Phuket Island, Thailand (Charuchinda & Hylleberg 1984).

Merulina ampliata, however, is a shade-tolerant species normally found in deep waters (Maragos 1974; Sheppard 1980) under low-light environments (mean % subsurface irradiance of 0.23%, Dinesen 1983) or even below Acropora hyacinthus tables on reef flats (Sheppard 1981). Foliose corals, such as M. ampliata, are well-adapted to low levels of light because their large surface-to-volume ratio increases their ability to trap light energy for photosynthesis (Barnes 1973; Dustan 1975; Jokiel & Morrissey 1986). Sorokin (1982), however, estimated that the photosynthesis to respiration ratio was 0.9 for M. ampliata, whereas 52% of respiration requirements were covered through heterotrophy (predator feeding; feeding on DOM; feeding on bacteria). Apparently, M. ampliata is a shade-tolerant or even a skiophilous scleractinian species because it may depend heavily on heterotrophy to adequately cover its energy requirements. This interplay of morphological and feeding plasticity may be quite effective as their fast skeletal linear extension rates make them superior overtopping competitors compared to corals with other life forms (Lang & Chornesky 1990), and efficient space competitors that often dominate the reef slopes (Dai 1990, 1993). Furthermore, their dense skeletons (Hughes 1987) help them survive under strong currents. Also, mucus secretion and sloughing by M. ampliata was observed in the field. Although production of mucus nets is at the cost of metabolic energy (Riegl & Branch 1995) and may increase an inclination to infection (Hodgson 1990), it may be used by the meandroid M. ampliata for sediment rejection (Hubbard & Pocock 1972; Stafford-Smith 1993; Sofonia & Anthony 2008), as an energy source (Anthony & Fabricius 2000; Wild et al. 2004) or both (Brown & Bythell 2005). Finally, mass-coral spawning events, including mature colonies of the hermaphroditic broadcast spawner M. ampliata (5.0–10.0 cm in diameter for Southern Taiwan, Fan & Dai 1998), take place on reefs of Singapore in March (Guest et al. 2002).

Linear regression models indicated that the mean skeletal linear extension rate of M. ampliata at the southern islands of Singapore was significantly and negatively affected primarily by alteration in suspended particulate matter concentration. Specifically, for every mg·l⁻¹ increase in suspended solids concentration there is a 0.216 cm·year⁻¹ (= 0.018 cm × 12 mo) reduction in skeletal linear extension rate of M. ampliata for the range 4.07–15.22 mg·l⁻¹ of suspended particulate matter concentration. For the same increase in suspended particulate matter concentration there was a 0.283 cm·year⁻¹ reduction in skeletal linear extension rate of the facultative heterotroph the massive scleractinian M. annularis, measured in the range 4.26–7.11 mg·l⁻¹ suspended particulate matter concentration along a eutrophication gradient in Barbados (regression calculated based on raw data from Tables 2 and 7 of Tomascik & Sander 1985). On the other hand, average annual skeletal linear extension rates (range: 11.7–16.2 mm·year⁻¹) did not relate significantly with suspended particulate matter concentration (range: 4.49–28.91 mg·l⁻¹) for the massive scleractinian Porites lobata from 13 polluted (by sediments and nutrients) and unaffected sites in Indonesia (Edinger et al. 2000) and for the massive Porites lutea (range: 0.62–1.54 mm·month⁻¹) and the branching Acropora formosa (range: 3.0–7.6 mm·month⁻¹) on reefs affected by sedimentation and tin dredging (range: 2.5–10.5 mg·l⁻¹) along the southwest coast of Phuket Island, Thailand (Chansang et al. 1992). The quadratic regression model indicated that distance from the main island of Singapore was an almost perfect predictor of annual skeletal extension rate of M. ampliata, dissolved oxygen, suspended particulate matter and particulate organic matter concentrations, and revealed threshold responses.

Either because individual growth rates are impaired or because of partial mortality resulting in colony fission (Hughes & Jackson 1985), M. ampliata finds it difficult to attain a large size at the reef sites surveyed. The mean coral colony size of M. ampliata in the field based on maximum diameter (mean: 9.5 cm, range: 3.2–23.0 cm at the four reef sites) was comparable to the mean of maximum colony length of the same species found in shaded environments at the Great Barrier Reef (mean: 12.9 cm, range: 3.0–63.0 cm; Dinesen 1983). Finally, the growth form of M. ampliata in the field was laminar, not convoluted as found in better lit environments (Hughes 1987). Nonetheless, M. ampliata has retained comparable linear extension growth rates under highly turbid waters during the last 15 years (Lane 1991). Coral reefs of the southern islands of Singapore have experienced chronic exposure to increased sediment load, which has led to a dramatic decline in live coral cover since the 1970s, a dominance of benthic space by dead corals covered with sediment and filamentous algae, and survival of only sediment/turbidity-tolerant scleractinian taxa (Dikou & van Woesik 2006) just as Sanders & Baron-Szabo (2005) predicted (Fig. 4B and 5,6 drawing in their paper) for scleractinian assemblages under chronic sediment input. Acquisition of skeletal linear extension rates of M. ampliata from reference (unaffected) sites may help clarify whether this is another example of normal coral growth rates on dying reefs (Edinger et al. 2000) or not.

Conclusion

Suspended particulate matter concentration was the best predictor of skeletal linear extension rate of the foliaceous, skiophilous, heterotrophic, scleractinian M. ampliata in the turbid waters of the southern islands of Singapore. A 0.018 cm·month⁻¹ reduction in skeletal linear extension rate was predicted per mg·l⁻¹ increase in the suspended particulate matter concentration over the range 4.07–15.22 mg·l⁻¹.

Acknowledgements

I thank researchers of the Tropical Marine Science Initiative, postgraduate students of the National University of Singapore, and volunteer divers for valuable assistance in the field. The study was funded with a research scholarship to the author by the National University of Singapore.

Appendix

Appendix I

Staining periods (P1–P4) and initial coral colony size (surface area = 3.14 × max. length × max. width) for specimens of M. ampliata from Cyrene (C), Pulau Hantu (PH), Semakau (S) and Raffles (R) reef sites used for the extraction of skeletal linear extension rates at the end of the mensurative experiment.

Specimen i.d.	Staining period				Coral colony size
Specimen i.d.	P1	P2	P3	P4	Length max. (cm)	Width max. (cm)	Surface area (cm²)
CM4			+	+	16.5	14.5	751.2
CM6			+	+	13.0	9.0	367.4
CM8	+	+	+	+	8.5	7.5	200.2
CM10	+	+	+	+	5.9	3.4	63.0
CM11			+	+	6.1	5.7	109.2
HM6		+	+	+	8.5	7.4	197.5
PHM7	+	+	+	+	18.5	13.0	755.2
PHM8		+	+	+	8.5	7.5	200.2
PHM9		+	+	+	5.3	5.2	86.5
PHM12	+	+	+	+	15.1	11.2	531.0
PHM13		+	+	+	7.3	5.5	126.1
PHM14			+	+	5.3	5.1	84.9
PHM18			+	+	5.5	5.0	86.4
PHM19			+	+	14.0	10.0	439.6
PHM20	+	+	+	+	8.5	8.0	213.5
PHM24	+	+	+	+	10.2	8.2	262.6
SM1		+	+	+	10.0	9.2	288.9
SM2		+	+	+	5.1	5.0	80.1
SM3			+	+	6.3	4.2	82.1
SM4		+	+	+	14.0	12.0	527.5
SM5		+	+	+	10.5	6.5	214.3
SM6		+	+	+	19.5	13.0	796.0
SM9			+	+	5.8	5.0	91.1
SM10		+	+	+	8.8	4.4	121.6
SM11		+	+	+	8.0	6.5	163.3
SM13		+	+	+	9.5	9.0	268.5
SM16		+	+	+	11.5	10.8	390.0
SM17			+	+	3.2	2.8	27.2
RM2	+	+	+	+	12.5	11.0	431.8
RM3	+	+	+	+	13.3	12.2	509.5
RM5	+	+	+	+	6.5	5.8	118.4
RM6	+	+	+	+	7.5	7.0	164.9
RM7	+	+	+	+	7.8	7.0	171.4
RM9	+	+	+	+	8.3	7.5	195.5
RM11	+	+	+	+	8.1	7.8	198.4
RM12	+	+	+	+	8.0	6.5	163.3
RM13			+	+	9.3	5.5	160.6
RM14			+	+	11.0	11.0	379.9
RM15	+	+	+	+	7.5	6.0	141.3
RM16		+	+	+	7.0	5.0	109.9
RM17		+	+	+	6.0	5.0	94.2
RM18	+	+	+	+	7.2	6.5	147.0
RM19			+	+	8.0	6.5	163.3
RM20		+	+	+	6.0	5.3	99.9
RM21		+	+	+	11.5	10.0	361.1
RM22		+	+	+	5.8	5.2	94.7
RM23		+	+	+	4.5	5.0	70.7
RM25		+	+	+	19.0	17.0	1,014.2
RM26		+	+	+	14.1	9.5	420.6
RM27	+	+	+	+	12.4	9.3	362.1
RM28		+	+	+	23.0	18.0	1,300.0

References

Anthony K.R.N., Fabricius K.E. (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. Journal of Experimental Marine Biology and Ecology, 252, 221–253.
10.1016/S0022-0981(00)00237-9
CAS PubMed Web of Science® Google Scholar
Anthony K.R.N., Hoegh-Guldberg O. (2003) Variation in coral photosynthesis, respiration and growth characteristics in contrasting light microhabitats: an analogue to plants in forest gaps and understoreys? Functional Ecology, 17, 246–259.
10.1046/j.1365-2435.2003.00731.x
Web of Science® Google Scholar
Bak R.P.M. (1978) Lethal and sublethal effects of dredging on reef corals. Marine Pollution Bulletin, 9, 14–16.
10.1016/0025-326X(78)90275-8
Web of Science® Google Scholar
Barnes D.J. (1973) Growth in colonial scleractinians. Bulletin of Marine Science, 23, 280–298.
Web of Science® Google Scholar
Brown B.E. (1997) Disturbances to reefs in recent times. In: C. Birkeland (Ed.), Life and Death of Coral Reefs. Chapman and Hall, New York: 354–379.
10.1007/978-1-4615-5995-5_15
Google Scholar
Brown B.E., Bythell J.C. (2005) Perspectives on mucus secretion in reef corals. Marine Ecology Progress Series, 296, 291–309.
10.3354/meps296291
CAS Web of Science® Google Scholar
Brown B.E., Howard L.S. (1985) Assessing the effects of ‘stress’ on reef corals. Advances in Marine Biology, 22, 1–63.
10.1016/S0065-2881(08)60049-8
Web of Science® Google Scholar
Brown B.E., Le Tissier M.D.A., Scoffin T.P., Tudhope A.W. (1990) Evaluation of the environmental impact of dredging on intertidal coral reefs at Ko Phuket, Thailand, using ecological and physiological parameters. Marine Ecology Progress Series, 65, 273–281.
10.3354/meps065273
Web of Science® Google Scholar
Chansang H., Phongsuwan N., Boonyanate P. (1992) Growth of corals under effect of sedimentation along the northwest coast of Phuket Island, Thailand. Proceedings of the 7th International Coral Reef Symposium , 1, 241–248.
Google Scholar
Charuchinda M., Hylleberg J. (1984) Skeletal extension of Acropora formosa at a fringing reef in the Andaman Sea. Coral Reefs, 3, 215–219.
10.1007/BF00288257
Web of Science® Google Scholar
Chia L.S. (1974) Sunshine and solar radiation in Singapore. In: J.B. Ooi, L.S. Chia (Eds), The Climate of West Malaysia and Singapore. Oxford University Press, London: 48–79.
Google Scholar
Dai C.-F. (1990) Interspecific competition in Taiwanese corals with special reference to interactions between alcyonacean and scleractinian corals. Marine Ecology Progress Series, 60, 291–297.
10.3354/meps060291
Web of Science® Google Scholar
Dai C.-F. (1993) Patterns of coral distribution and benthic space partitioning on the fringing reefs of southern Taiwan. Marine Ecology, 14, 185–204.
10.1111/j.1439-0485.1993.tb00479.x
Web of Science® Google Scholar
Dikou A., Van Woesik R. (2006) Survival under chronic stress from sediment load: spatial patterns of hard coral communities in the southern islands of Singapore. Marine Pollution Bulletin, 52, 7–21.
10.1016/j.marpolbul.2005.07.021
CAS PubMed Web of Science® Google Scholar
Dinesen Z.D. (1983) Shade-dwelling corals of the Great Barrier Reef. Marine Ecology Progress Series, 10, 173–185.
10.3354/meps010173
Web of Science® Google Scholar
Dodge R.E., Brass G.W. (1984) Skeletal extension, density and calcification of the reef coral, Montastrea annularis: St Croix, US. Virgin Islands. Bulletin of Marine Science, 34, 288–307.
Web of Science® Google Scholar
Dodge R.E., Aller R.C., Thomson J. (1974) Coral growth related to resuspension of bottom sediments. Nature, 247, 574–576.
10.1038/247574a0
CAS Web of Science® Google Scholar
Dodge R.E., Wyers S.C., Frith H.R., Knap A.H., Smith S.R., Sleetr T.D. (1984) The effects of oil and oil dispersants on the skeletal growth of the hermatypic coral Diploria strigosa. Coral Reefs, 3, 191–198.
10.1007/BF00288254
Web of Science® Google Scholar
Dustan P. (1975) Growth and form in the reef building coral Montastrea annularis. Marine Biology, 33, 101–107.
10.1007/BF00390714
Web of Science® Google Scholar
Edinger E.N., Limmon G.V., Jompa J., Widjatmoko W., Heikoop J.M., Risk M. (2000) Normal coral growth rates on dying reefs: are coral growth rates good indicators of reef health? Marine Pollution Bulletin, 40, 404–425.
10.1016/S0025-326X(99)00237-4
CAS Web of Science® Google Scholar
Fabricius K.E. (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin, 50, 125–146.
10.1016/j.marpolbul.2004.11.028
CAS PubMed Web of Science® Google Scholar
Fan T.-Y., Dai C.-F. (1998) Sexual reproduction of the scleractinian coral Merulina ampliata in southern Taiwan. Bulletin of Marine Science, 62, 897–904.
Web of Science® Google Scholar
GESAMP 2001. Protecting the oceans from land-based activities. Land-based sources and activities affecting the quality and uses of the marine, coastal and associated freshwater environment. United Nations Environment Program, Nairobi: 168 pp.
Google Scholar
Gin K.Y., Lin X., Zhang S. (2000) Dynamics and size structure of phytoplankton in the coastal waters of Singapore. Journal of Plankton Research, 2, 1465–1484.
10.1093/plankt/22.8.1465
Web of Science® Google Scholar
Greenberg A.E., Connors J.J., Jenkins D., Franson M.A.H. (1985) Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, D.C.: 1134 pp.
Google Scholar
Guest J.R., Chou L.M., Baird A.H., Goh B.P.L. (2002) Multispecific, synchronous coral spawning in Singapore. Coral Reefs, 21, 422–423.
Web of Science® Google Scholar
Hassan R., Scholes R., Ash N.. (2005) Millennium Ecosystem Assessment. Island Press. Washington, D.C: 948 pp. Available from http://www.millenniumassessment.org/en/Condition.aspx
Google Scholar
Hawker D.W., Connell D.W. (1989) An evaluation of the tolerance of corals to nutrients and related water quality characteristics. International Journal of Environmental Studies, 34, 179–188.
10.1080/00207238908710526
Google Scholar
Hodgson G. (1990) Tetracycline reduces sedimentation damage to corals. Marine Biology, 104, 493–496.
10.1007/BF01314355
CAS Web of Science® Google Scholar
Hoogenboom M.O., Connolly S.R., Anthony K.R.N. (2008) Interactions between morphological and physiological plasticity optimize energy acquisition in corals. Ecology, 89, 1144–1154.
10.1890/07-1272.1
PubMed Web of Science® Google Scholar
Hubbard J.H., Pocock Y.P. (1972) Sediment rejection by recent scleractinian corals: a key to palaeo-environmental reconstruction. Geologischen Rundschau, 61, 598–626.
10.1007/BF01896337
Google Scholar
Hudson J.H., Shinn E.A., Robbin D.M. (1982) Effects of offshore oil drilling on Philippine reef corals. Bulletin of Marine Science, 32, 890–908.
Web of Science® Google Scholar
Hughes T.P. (1987) Skeletal density and growth form of corals. Marine Ecology Progress Series, 35, 259–266.
10.3354/meps035259
Web of Science® Google Scholar
Hughes T.P., Jackson J.B.C. (1985) Population dynamics and life histories of foliaceous corals. Ecological Monographs, 55, 141–166.
10.2307/1942555
Web of Science® Google Scholar
Jokiel P.L., Morrissey J.I. (1986) Influence of size on primary production in the reef coral Pocillopora damicornis and the macroalga Acanthophora spicifera. Marine Biology, 91, 15–26.
10.1007/BF00397566
Web of Science® Google Scholar
Koop K., Booth D., Broadbent A., Brodie J., Bucher D., Capone D., Coll J., Dennison W., Erdmann M., Harrison P., Hoegh-Guldberg O., Hutchings P., Jones G.B., Larkum A.W.D., O’Neil J., Steven L., Tentori E., Ward S., Williamson J., Wellowlees D. (2001) ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Marine Pollution Bulletin, 42, 91–120.
10.1016/S0025-326X(00)00181-8
CAS PubMed Web of Science® Google Scholar
Kruzic P., Benkovic L. (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea (Croatia), Marine Ecology an evolutionary perspective, 29 (1), 125–139.
10.1111/j.1439-0485.2008.00220.x
CAS Web of Science® Google Scholar
Lane D.J.W. (1991) Growth of scleractinian corals on sediment-stressed reefs at Singapore. Proceedings of the Regional Symposium on Living Resources in Coastal Areas, pp. 97–106.
Google Scholar
Lang J.C., Chornesky E.A. (1990) Competition between scleractinian reef corals – a review of mechanisms and effects. In: Z. Dubinsky (Ed.), Ecosystems of the World, Vol. 25: Coral Reefs. Elsevier, Amsterdam: 133–208.
Google Scholar
Lewis J.B. (1977) Suspension feeding in Atlantic reef corals and the importance of suspended particulate matter as a food source. Proceedings of the 3rd International Coral Reef Symposium , 1, 405–408.
Google Scholar
Lough J.M., Barnes D.J. (1997) Several centuries of variation in skeletal extension, density and calcification in massive Porites colonies from the Great Barrier Reef: a proxy for seawater temperature and a background of variability against which to identify unnatural change. Journal of Experimental Marine Biology and Ecology, 211, 29–67.
10.1016/S0022-0981(96)02710-4
Web of Science® Google Scholar
Maragos J.E. (1974) Coral communities on a seaward reef slope, fanning island. Pacific Science, 28, 257–278.
Web of Science® Google Scholar
Parsons T.R., Maita Y., Lalli C.M. (1984) A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, New York: 173.
10.1016/0306-4565(88)90023-X
Web of Science® Google Scholar
Pastorok R.A., Bilyard G.R. (1985) Effects of sewage pollution on coral-reef communities. Marine Ecology Progress Series, 21, 175–189.
10.3354/meps021175
Web of Science® Google Scholar
Riegl B., Branch G.M. (1995) Effects of sediment on the energy budgets of four scleractinian (Boume 1900) and five alcyonaceans (Lamouroux 1816) corals. Journal of Experimental Marine Biology and Ecology, 186, 259–275.
10.1016/0022-0981(94)00164-9
Web of Science® Google Scholar
Rogers C.S. (1990) Responses of coral reefs and reef organisms to sedimentation. Marine Ecology Progress Series, 62, 185–202.
10.3354/meps062185
Web of Science® Google Scholar
Sanders D., Baron-Szabo R.C. (2005) Scleractinian assemblages under sediment input: their characteristics and relation to the nutrient input concept. Palaeogeography, Palaeoclimatology, Palaeoecology, 216, 139–181.
10.1016/j.palaeo.2004.10.008
Web of Science® Google Scholar
Scoffin T.P., Tudhope A.W., Brown B.E. (1989) Corals as environmental indicators with preliminary results from South Thailand. Terra Nova, 1, 559–563.
10.1111/j.1365-3121.1989.tb00432.x
Web of Science® Google Scholar
Sebens K.P. (1987) Coelenterate energetics. In: F.J. Vernberg, T.J. Pandian (Eds), Animal Energetics, Vol. 1. Academic Press, New York: 1.
Google Scholar
Sheppard C.R.C. (1980) Coral fauna of Diego Garcia lagoon, following harbor construction. Marine Pollution Bulletin, 11, 227–230.
10.1016/0025-326X(80)90412-9
PubMed Web of Science® Google Scholar
Sheppard C.R.C. (1981) Illumination and the coral community beneath tabular Acropora species. Marine Biology, 64, 53–58.
10.1007/BF00394080
Web of Science® Google Scholar
Sofonia J.I., Anthony K.R.N. (2008) High-sediment tolerance in the reef coral Turbinaria mesenterina from the inner Great Barrier Reef lagoon (Australia). Estuarine, Coastal and Shelf Science, 78, 748–752.
10.1016/j.ecss.2008.02.025
Web of Science® Google Scholar
Sorokin Y.I. (1982) Aspects of the biomass, feeding and metabolism of common corals of the Great Barrier Reef, Australia. Proceedings of the 4th International Coral Reef Symposium , 2, 27–32.
Google Scholar
Stafford-Smith M.G. (1993) Sediment-rejection efficiency of 22 species of Australian scleractinian corals. Marine Biology, 115, 229–243.
10.1007/BF00346340
Web of Science® Google Scholar
Te F.T. (1997) Turbidity and its effect on corals: a model using the extinction coefficient (K) or photosynthetic active radiance (PAR). Proceedings of the 8th International Coral Reef Symposium , 2, 1899–1904.
Google Scholar
Titlyanov E.A. (1981) Adaptation of reef building corals to low light intensity. Proceedings of the 4th International Coral Reef Symposium , 2, 39–43.
Google Scholar
Todd P.A. (2008) Morphological plasticity in scleractinian corals. Biology Reviews, 83, 315–337.
10.1111/j.1469-185X.2008.00045.x
PubMed Web of Science® Google Scholar
Tomascik T., Sander F. (1985) Effects of eutrophication on reef-building corals. I. Growth rate of the reef-building coral Montastrea annularis. Marine Biology, 87, 143–155.
Google Scholar
Veron J.E.N., Stafford-Smith M. (2000) Corals of the World, Vol. 2. Australian Institute of Marine Science, Townsville: 378.
Google Scholar
Watts I.E.M. (1974) Rainfall of Singapore Island. In: J.B. Ooi, L.S. Chia (Eds), The Climate of West Malaysia and Singapore. Oxford University Press, London: pp. 80–131.
Google Scholar
Wild C., Huettel M., Klueter A., Kremb S.G., Rasheed M.Y.M., Jorgensen B.B. (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature, 428, 66–70.
10.1038/nature02344
CAS PubMed Web of Science® Google Scholar

Citing Literature

Volume30, Issue4

December 2009

Pages 405-415

Skeletal linear extension rates of the foliose scleractinian coral Merulina ampliata (Ellis & Solander, 1786) in a turbid environment

Abstract

Problem