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Environmental Monitoring and Assessment (2005) 104: 353–367 DOI: 10.1007/s10661-005-1621-9

c Springer 2005

METAPROTELLA SANDALENSIS (CRUSTACEA: AMPHIPODA: CAPRELLIDAE): A BIOINDICATOR OF NUTRIENT ENRICHMENT ON CORAL REEFS? A Preliminary Study at Mauritius Island J. M. GUERRA-GARCÍA1,∗ and M. S. KOONJUL2 1

Laboratorio de Biolog´ıa Marina, Departamento de Fisiolog´ıa y Zoolog´ıa, Facultad de Biolog´ıa, Universidad de Sevilla, Sevilla, Spain; 2 Albion Fisheries Research Centre, Ministry of Fisheries, Albion, Petite Rivière, Mauritius (∗ author for correspondence, e-mail: [email protected])

(Received 26 November 2003; accepted 28 May 2004)

Abstract. The population of the caprellid Metaprotella sandalensis Mayer (Crustacea: Amphipoda) associated with the seaweed Turbinaria ornata (Turner) J. Agardh was studied on a spatial scale in relation to the influence of physico-chemical factors on the coral reef system at Mauritius Island. Some areas of the coast of Mauritius are currently subject to disturbance due to industrialisation and rapidly growing tourist development programmes, meanwhile other sites of the island are still unaltered. T. ornata was sampled at 12 stations, distributed around the whole island to represent the heterogeneous conditions. The density of Metaprotella sandalensis living on T. ornata was measured. The linear regression and the multivariate analysis showed a strong correlation between the densities of the caprellid and the physico-chemical parameters. The highest densities of M. sandalensis were found in the most stressed sites characterised by the highest values of nitrate, phosphate, chemical oxygen demand and silting. According to these results and taking into account that M. sandalensis and T. ornata are widely distributed in most of the tropical ecosystems, we preliminarily propose usage of the density of this caprellid as a new monitoring tool on coral reefs or, at least, as a first diagnosis for the detection of nutrient enrichment on these ecosystems. Keywords: coral reefs, pollution, nutrient enrichment, Caprellidae, bioindicator, Mauritius

1. Introduction Coral reefs are among the most spectacular marine ecosystems on the planet and they are renowned for their biological diversity and high productivity (Koop et al., 2001). Despite their importance, coral reefs have been considered as one of the most threatened marine ecosystems (Wilkinson, 1998; Hoegh-Guldberg, 1999) and the most sensitive to excess nutrients (Goreau, 1992). With the generalised continuous nutrient-enrichment of coastal waters, eutrophication constitutes an increasing threat to the health and biodiversity of coral reefs. Severe effects of nutrient enrichment on corals have been demonstrated throughout the coral reef literature: reduced reproductive success (Ward, 1997; Koop et al., 2001), reduced skeletal density (Koop et al., 2001), reduced coral growth (Stambler et al., 1991), increased turf and macroalgae growth which reduces light penetration

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to the coral colonies and inhibits the settlement of new coral larvae (Bell, 1991; Costa et al., 2000). Due to the great importance of these ecosystems, there is a recent increase in the interest of the coral reef monitoring programs (e.g. MFMR, 1998; Jordan and Samways, 2001; Bythell et al., 1993). Usually, a multidisciplinary approach is used for monitoring the state of the coral reef ecosystems. Together with the line-intercept transect method, recommended by the Global Coral Reef Monitoring Network (GCRMN) to determine coral and other benthos percentage cover, the values of physico-chemical parameters are used in monitoring programmes (Chineah et al., 2001). Additionally, notes on physical coral damage, disease and bleaching are also recorded (Jordan and Samways, 2001). Despite this multidisciplinary approach, the non-diagnostic nature of most coral reef monitoring programmes limits the ability of scientists, managers, and agency staff to communicate trends in the condition of coral reef systems to the public or politicians. Recently, multimetric indexes are being proposed using the sessile epibenthos, benthic macroinvertebrates, fish, macrophytes, phytoplankton and zooplankton in an integrated approach to assess degradation caused by human actions (Jameson et al., 2001). The caprellids (Crustacea: Amphipoda) are an important trophic link as one of the dominant secondary producers between unicellular algae and fishes in coastal water ecosystems including coral reef ecosystems (Ohji et al., 2002a; GuerraGarc´ıa, in preparation). Recently, the use of caprellids in monitoring temporal and spatial changes in baseline concentrations of butyltins has been proposed (Takeuchi et al., 2001; Ohji et al., 2002a,b) and this group of crustaceans has turned out to be an excellent bioindicator of environmental conditions in Mediterranean ecosystems of Northern Africa (Guerra-Garc´ıa and Garc´ıa-Gómez, 2001). Thomas (1993) stressed that amphipods are also the ideal candidates for studies in tropical ecosystems because they are ecologically and trophically important, numerically dominant, exhibit a high degree of niche specificity, have a documented sensitivity to a variety of pollutants and toxicants and have relatively low dispersal capabilities. However, there are no studies investigating the potential use of the Caprellidae in coral reef monitoring programmes. The caprellid M. sandalensis (Figure 1) is one of the most common coral reef caprellids (Müller, 1990). During a preliminary survey at Mauritius Island, this caprellid has been found living on Turbinaria ornata, showing different densities depending on the sites. The seaweed T. ornata (Figure 2) is one of the most abundant and widely distributed seaweeds on the coral reef ecosystems (Goreau, 1992; Schaffelke, 1999; Stiger and Payri, 1999a,b) with extensive populations settling on the reef throughout the whole year. The main objective of the present study was to investigate if the abundance of the caprellid M. sandalensis on T. ornata could be used as bioindicator of environmental conditions, especially nutrient enrichment, in coral reef ecosystems.

METAPROTELLA SANDALENSIS: A BIOINDICATOR OF NUTRIENT ENRICHMENT

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2. Material and Methods 2.1. S TUDY

AREA

The republic of Mauritius, situated in the South-west Indian Ocean, consists of one major island, Mauritius Island (19◦ 59 –20◦ 32 S, 57◦ 18 –57◦ 47 E), on which the present study was conducted, and a group of outer surrounding islands and islets (Figure 3). Mauritius Island is of volcanic origin and has a land area of 1865 km2 , a coastline of 200 km and 150 km of coral reef enclosing lagoons with a total area of about 245 km2 . The coastline is bathed continuously by the waters of the South Equatorial current and the island has shores of heterogeneous environments imposed by the natural configuration of the coast as well as by intense port activity near Port Louis.

Figure 1. Metaprotella sandalensis Mayer. Lateral view. A, male; B, female. Scale bar: 1 mm.

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Figure 2. Turbinaria ornata (Turner) J. Agardh collected from the Mauritius Island. Scale bar: 1 cm.


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Figure 3. Map of Mauritius showing the sampling stations. See Table I for details.

Some areas of the coast of Mauritius are currently subject to disturbance due to industrialisation and rapidly growing tourist development programmes. Fagoonee (1990) and Gendre et al. (1994) pointed out that untreated industrial waste, agricultural runoff and sewage are polluting the lagoon ecosystems. It has become increasingly important to carry out investigations on Mauritius ecosystems on


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a continuous basis to understand the changes that could be occurring as a result of anthropogenic activities. In fact, the Government of Mauritius with inputs from the Albion Fisheries Research Centre, Ministry of Fisheries and assistance of the International Centre for Ocean Development (ICOD) and the Japan International Co-operation Agency (JICA) has been developing monitoring programmes considering the biological communities, specially corals, and the physico-chemical parameters around the island (MFMR, 1998; Chineah et al., 1999, 2001) 2.2. S AMPLING

AND ANALYTICAL PROCEDURE

The seaweed T. ornata was selected for the study (Figure 1). The same species of alga was selected as a substratum in all the sites to eliminate the variation in community structure caused by the configuration of the different substrata (SánchezMoyano and Garc´ıa-Gómez, 1998; Guerra-Garc´ıa and Garc´ıa-Gómez, 2001). T. ornata is one of the most abundant and widely distributed seaweeds around the Mauritius Island and its population settles on the reef throughout the whole year (Stiger and Payri, 1999a,b). A total of 12 stations distributed around the coast of Mauritius was chosen (Figure 3). The sites and types of coastal development are given in Table I. Stations were selected approximately at the same depth (between 2 and 4 m) to avoid TABLE I Stations selected for the study and types of coastal development in each one Code Station

Justification

CM

Cap malheureux

Relatively undeveloped with potential for further development of tourism and industry

TD BV BB IB FF AL PS PL

Trou d’Eau Douce Bambous Virieux Blue Bay Ile aux Bénitiers Flic en Flac Albion Pointe aux Sables Port Louis

BT1 BT2 TB

Relatively undeveloped with some input of fresh water Discharge from Grande Rivière Sud-Est Relatively undeveloped, proposed Marine Park Relatively undeveloped, fishing village Fish kills Site of the Marine Shrimp Experimental Station, input of fresh water Directly influenced by the harbour activities Close to the Port Louis harbour (shipping activities, sewage, industrial effluents. . . ) Bahie du Tombeau 1 Directly influenced by the harbour activities, fish kills, algal blooms and discharges from textile industries Bahie du Tombeau 2 Directly influenced by the harbour activities, fish kills, algal blooms and discharges from textile industries Trou aux Biches Tourism activities, recreational use by the public


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depth-related effects (Guerra-Garc´ıa and Garc´ıa-Gómez, 2001). T. ornata was collected using snorkelling in July 2002 in all stations. Each sample was placed in a plastic bag and fixed with a 10% formalin-seawater solution. Three replicate samples were taken at each station. All the replicate samples of T. ornata were selected with approximately the same size (volume 80–100 mL, length 20–25 cm) to eliminate the contribution of this factor to the caprellid populations living on the seaweed. The samples were sieved through a 0.5 mm mesh (Sánchez-Moyano et al., 2000) and sorted out under a dissecting microscope. The caprellids were separated, preserved in 70% ethanol and counted. The abundance data were expressed as number of individuals per 100 mL alga. The volume of algae was estimated by displacement of water in a manometer (Sánchez-Moyano and Garc´ıa-Gómez, 1998). In connection with the chemical parameters of water, the Albion Fisheries Research Centre (AFRC) has been developing a monitoring programme since 1991, collecting water samples around the whole island to measure the Chemical Oxygen Demand (COD) and nutrients such as Nitrate-Nitrogen (NO3 N) and phosphate (PO4 ) adopting the standard procedures described by Chineah et al. (1999). The mean values of COD, NO3 –N and PO4 of the data series collected since 1991 were used in the present study. The data have been taken from annual internal reports of the Albion Fisheries Research Centre-Ministry of Fisheries, the guidelines for coastal water quality published by the Ministry of Environment and Human Resource Development and Employement with input for the AFRC (MFMR, 1998), and complementary publications (Chineah et al., 1999, 2001). To estimate the sedimentation rate in each station, five replicates of Turbinaria were collected and the volume of sediment trapped in the alga was measured. This volume of sediment referred to 100 mL of alga was used as a comparative estimation of silting, since we can assume that this seaweed behaves like a sediment trap due to its morphology. To measure the cover of T. ornata in each station, two transects of 25 m each were carried out. The line-intercept transect method, as recommended by the Global Coral Reef Monitoring Network (GCRMN) was used and the percentage of T. ornata was measured. 2.3. S TATISTICAL

TREATMENT

Multivariate analyses (classification and ordination) were carried out using the programs PC-ORD version 3.05 (McCune and Mefford, 1997) and PRIMER version 5 (Clarke and Gorley, 2001). The affinities among stations on the basis of physico-chemical parameters (sedimentation, COD, nitrate-nitrogen and phosphate) were established through cluster analysis using the UPGMA (Unweighted Pair-Group Method using Averages) (Sneath and Sokal, 1973) based on the euclidean distance. A Principal Component Analysis (PCA) was also carried out. A linear-regression model was used to test the relationship between

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the physico-chemical parameters and the density of the caprellid Metaprotella sandalensis.

3. Results and Discussion 3.1. E NVIRONMENTAL

VARIABLES

The highest concentrations of nitrate–nitrogen, phosphate and COD were measured in Port Louis (PL) close to the harbour, and the nearby areas, specially Bahie du Tombeau (BT1 and BT2) but also in Pointe aux Sables (PS) (Figure 4). The sediment trapped in T. ornata was also higher in the Bahie du Tombeau. In Port Louis and Pointe aux Sables no Turbinaria was found and, consequently, data of sedimentation are not available. The higher nutrient levels and oxygen demand in the Port Louis site were expected because the area is affected by intense port based activities, shipping, sewage (sewer outfalls) and industrial effluents. In Albion (AL) the values of nitrate–nitrogen and phosphate were also considerably high as they were influenced by fresh water effluents carrying nutrients and organic loads from land-based sources. The Cluster analysis (Figure 5) using the environmental matrix of physicochemical parameters (nitrate–nitrogen, phosphate, COD and sediment trapped in the seaweed) showed two groups of stations. The first included the Port Louis station (PL) close to the harbour, together with the Baie du Tombeau sites. The second group included the remaining stations. This group splits into two subgroups. On the one hand, the stations PS, AL and CM, with intermediate values of nitrate–nitrogen, phosphate and COD, and on the other hand the stations IB, BV, FF, BB, TD and TB showing the lower nutrient concentrations. The first axis of the PCA analysis (Figure 6), which explained the 82.3% of the total variance, correlated significantly with all the variables (nitrate, r = −0.93; phosphate, r = −0.93; COD, r = −0.94; sediment, r = −0.83; p< 0.01 in all cases). 3.2. B IOLOGICAL

DATA

3.2.1. Turbinaria ornata Populations The seaweed T. ornata was present in all the stations except in Port Louis (PL) and Pointe aux Sables (PS) (Figure 7) probably due to the negative effects associated to the shipping activities near the harbour. T. ornata is tough, unpalatable to fish and adapted to live in many different environmental conditions, occurring inshore as well as on reefs further offshore (Payri, 1984; Goreau, 1992). The tendency for fertile thalli of T. ornata to float over long distances, combined with its oogonia stock and high settlement efficiencies, could account for its great capacity to colonise, its rapid establishment and maintenance of local populations (Stiger and Payri, 1999a). Due to its high adaptation capability, T. ornata presents a


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Figure 4. Mean values and standard deviation of the physico-chemical parameters measured in the stations. (n = 50–125 for nitrate, phosphate and chemical oxygen demand (COD) and n = 5 for the sedimentation).

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Figure 5. Dendrogram of similarity between the stations based on the physico-chemical parameters.

Figure 6. PCA ordination of the stations according to the physico-chemical parameters.

high ecological range and can be classified as r -strategy species (Stiger and Payri, 1999b). In the present study, T. ornata was represented in most of the stations, but the percentage of cover did not correlate significantly with any of the physico-chemical parameters. This indicates that the distribution of this seaweed is not influenced by the nutrients concentrations, COD and sedimentation, and other factors such as the current pattern, substrate nature, and light intensity could be further affecting the seaweed distribution. This result is supported by recent experiments which have demonstrated that the alga T. ornata does not respond to nutrient addition with higher production but accumulating 15 to 20% more tissue nutrients than untreated thalli (Schaffelke, 1999).


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Figure 7. Percentage cover of the seaweed Turbinaria ornata at the stations.

3.2.2. Density of Metaprotella sandalensis as Bioindicator of Environmental Variables Regardless of the cover of T. ornata at each site, the density of the caprellid M. sandalensis was significantly correlated with all the physicochemical parameters (Figure 8). The number of specimens in 100 mL seaweed increased with higher concentrations of nitrogen and phosphate, and higher values of COD and sedimentation rate. This tendency is supported when the density values are represented with the scores of the first axis of the PCA analysis (Figure 9), which explained 82% of the total variance. The correlation was significant (r = 0.91, p < 0.001). Coral reefs are the most sensitive of all marine ecosystems to excess nutrients (Goreau, 1992). Unfortunately, traditionally, nutrient standards for coral reefs have been adopted from cold developed countries. Most of these standards were developed for estuary ecosystems and are dangerously inappropriate for tropical coral reef ecosystems. Presently, more appropriate nutrient standards for coral reefs are being adopted; levels of phosphate higher than 0.04 mg/L are a matter of concern in relation to the health of the corals of a region (Chineah et al., 2001; MFMR, 1998). Values nitrate–nitrogen higher than 0.2 mg/L can also be considered a matter of concern (MFMR, 1998). In the areas close to the harbour, where the concentrations of nitrate–nitrogen and phosphate were higher than 0.04 and 0.2 mg/L, respectively, the biggest densities of the caprellid M. sandalensis were registered. M. sandalensis is a very common caprellid in shallow waters of the tropical IndoPacific Ocean. Recently, Müller (1990) redescribed the species in detail pointing out that morphologically it is a highly variable species with regard to the number and arrangement of acute projections on head and pereonites 2–3 as well as to the shape of the male propodal palm. During a sampling programme in the Great Barrier Reef, the first author of this study also found M. sandalensis with a considerable variety of morphological forms and habitats (Guerra-Garc´ıa, in preparation). This could indicate the probable existence of a complex of different species inside the M. sandalensis from the Great Barrier Reef. Further taxonomic and genetic studies are necessary to investigate if the variation among specimens of this area is intra or interspecific.

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Figure 8. Linear regression relationships between the physico-chemical parameters and the density of the caprellid Metaprotella sandalensis living on Turbinaria ornata.

Today, society is increasingly demanding quick environmental studies in coastal areas, especially in the threatened coral reef ecosystems. This precludes developing long-temporal series of data with complex matrices of various taxonomic groups, whose identification requires great effort (Guerra-Garc´ıa and Garc´ıa-Gómez, 2001). The present study, although preliminary, points to the use of the density of M. sandalensis as a new monitoring system on coral reefs or, at least,


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Figure 9. Representation of the density values of the caprellid Metaprotella sandalensis in relation to the PCA scores obtained with the physico-chemical parameters.

as a first diagnosis for the detection of nutrient enrichment on these valuable ecosystems. Acknowledgements The authors are very grateful to the Albion Fisheries Research Center for the facilities provided during the study. Special thanks to J. P. Luchmun, V. Mangar, K. Mungry and C. Samyan for assistance during the sampling programme in some of the stations. Thanks are also due to H. Terashima (Japan International Cooperation Agency) for help and advises, and to V. Chooramun, in charge of the monitoring of physico-chemical parameters. The first author (JMGG) also thanks to D. Goorah, Principal Fisheries Officer at the AFRC, for supporting the visit, and Y. Emandi for hospitality and encouragement during the stay in Mauritius. This study was supported by a grant AP 98 28617065 from the Ministry of Education, Culture and Sport of Spain.

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References Bell, P.R.F.: 1991, ‘Status of eutrophication in the Great Barrier Reef lagoon’, Mar. Pollut. Bull. 23,89–93. Bythell, J.C., Bythell, M. and Gladfelter, E.H.: 1993, ‘Initial results of a long-term coral-reef monitoring program. Impact of hurricane Hugo at Buck Island Reef National Monument, St. Croix, United States Virgin Islands’, J. Exp. Mar. Biol. Ecol. 172, 171–183. Chineah, V., Chooramun, V., Nallee, M., Basant Rai, Y., Moothien Pillay, R., Jayabalan, N., Terashima, H. and Terai, A.: 2001, Status of the Marine Environment of the Flic en Flac Lagoon, Mauritius, Food and Agricultural Research Council, Mauritius. Chineah, V., Munbodh, M., Chooramun, V., Nallee, M., Basant Rai, Y., Hurbungs, M., Paupiah, C.N., Mosaheb, J.I., Terashima, H., Terai, A. and Jayabalan, N.: 1999, ‘Status of the Marine Environment of the Albion Lagoon’, in: the Proceedings of the Annual Meeting of Agricultural Scientists, Mauritius. Clarke, K.R. and Gorley, R.N.: 2001. Primer v5: User Manual /Tutorial. Primer-E, Plymouth, pp. 1– 91. Costa, O., Leão, Z., Nimmo, M. and Attrill, M.: 2000, ‘Nutrification impacts on coral reefs from northern Bahia, Brazil’, Hydrobiologia 440, 307–315. Fagoonee, I.: 1990, ‘Coastal marine ecosystems of Mauritius’, Hydrobiologia 208, 55–62. Gendre, F., Beck, C., Ruch, P. and Kubler, B.: 1994, ‘Human impacts on coral ecosystems at Mauritius island: Coprostanol in surface sediments’, Eclogae Geologica Helvetica 87, 357–367. Goreau, T.J.: 1992, ‘Bleaching and reef community changes in Jamaica: 1951–1991’, Am. Zoologist 32, 683–695. Guerra-Garc´ıa, J.M. and Garc´ıa-Gómez, J.C.: 2001, ‘The spatial distribution of Caprellidea (Crustacea: Amphipoda): A stress bioindicator in Ceuta (North Africa, Gibraltar area)’, P. S. Z. N. Mar. Ecol. 22, 357–367. Hoegh-Guldberg, O.: 1999, ‘Climate change, coral bleaching and the future of the world’s coral reefs’, Mar. Freshw. Res. 50, 839–866. Jameson, S.C., Erdmann, M.V., Karr, J.R. and Potts, K.W.: 2001, ‘Charting a course toward diagnostic monitoring: A continuing review of coral reef attributes and a research strategy for creating coral reef indexes of biotic integrity’. Bull. Mar. Sci. 69, 701–744. Jordan, I.E. and Samways, M.J.: 2001, ‘Recent changes in coral assemblages of a South African coral reef, with recommendations for long-term monitoring’, Biodivers. Conserv. 10, 1027– 1037. Koop, K., Booth, D., Broadbents, 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.O., Steven, A., Tentori, E., Ward, S., Williamson, J. and Yellowless, D.: 2001, ‘ENCORE: The effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions’, Mar. Pollut. Bull. 42, 91–120. McCune, B. and Mefford, M.J.: 1997, PC-ord. Multivariate Analysis of Ecological Data, Mjm Software Design, Gleneden Beach, USA, pp. 1–47. MFMR-Ministry of Fisheries and Marine Resources: 1998, Status of Coral Reefs and PhysicoChemical Characteristics of Nearshore Waters of Mauritius: A Baseline Study, Government of Mauritius, Mauritius, pp. 1–108. Müller, H. G.: 1990, ‘New species and records of coral reef inhabiting Caprellidae from Bora Bora and Moorea, Society Islands (Crustacea: Amphipoda)’, Rev. Suisse Zool. 97, 827– 842. Ohji, M., Arai, T. and Miyazaki, N.: 2002a, ‘Effects of tributyltin exposure in the embryonic stage on sex ratio and survival rate in the caprellid amphipod Caprella danilevskii’, Mar. Ecol. Prog. Ser. 235, 171–176.


367

Ohji, M., Takeuchi, I., Takahashi, S., Tanabe, S. and Miyazaki, N.: 2002b, ‘Differences in the acute toxicities of tributyltin between the Caprellidea and the Gammaridea (Crustacea: Amphipoda)’, Mar. Pollut. Bull. 44, 16–24. Payri, C. E.: 1984, ‘The effect of environment on the biology and morphology of Turbinaria ornata (Phaeophyta) from the Tiahura Reef (Moorea Island, French Polynesia)’, Bot. Mar. 27, 327–333. Sánchez-Moyano, J. E., Estacio, F. J., Garc´ıa-Adiego, E. M. and Garc´ıa-Gómez, J. C.: 2000, ‘The molluscan epifauna of the alga Halopteris scoparia in Southern Spain as a bioindicator of coastal environmental conditions’, J. Mollus. Stud. 66, 431–448. Sánchez-Moyano, J. E. and Garc´ıa-Gomez, J.C.: 1998, ‘The arthropod community, especially Crustacea, as a bioindicator in Algeciras Bay (Southern Spain) based on a spatial distribution’, J. Coastal Res. 14, 1119–1133. Schaffelke, B.: 1999, ‘Short-term nutrient pulses as tools to assess responses of coral reef macroalga to enhanced nutrient availability’, Mar. Ecol. Prog. Ser. 182, 305–310. Sneath, P.H.A. and Sokal, R.R.: 1973, Numerical Taxonomy. The Principles and Practice of Numerical Classification, WH Freeman and Company, San Francisco, pp. 1–573. Stambler, N., Popper, N., Dubinsky, Z. and Stimson, J.: 1991, ‘Effects of nutrient enrichment and water motion on the coral Pocillopora damicornis’, Pacific Sci. 45, 299–307. Stiger, V. and Payri, C.E.: 1999a, ‘Spatial and temporal patterns of settlement of the brown macroalgae Turbinaria ornata and Sargassum mangarevense in a coral reef on Tahiti, Mar. Ecol. Prog. Ser. 191, 91–100. Stiger, V. and Payri, C.E.: 1999b, ‘Spatial and seasonal variations in the biological characteristics of two invasive brown algae, Turbinaria ornata (Turner) J. Agardh and Sargassum mangarevense (Grunow) Stechell (Sargassaceae, Fucales) spreading on the reefs of Tahiti (French Polynesia)’, Bot. Mar. 42, 295–306. Takeuchi, I., Takahashi, S., Tanabe, S. and Miyazaki, N.: 2001, ‘Caprella watch: A new approach for monitoring butyltin residues in the ocean’, Mar. Environ. Res. 52, 97–113. Thomas, J.D.: 1993, ‘Biological monitoring and tropical biodiversity in the marine environments: A critique with recommendations, and comments on the use of amphipods as bioindicators’, J. Nat. Hist. 27, 795–806. Ward, S.: 1997, The Effects of Elevated Nitrogen and Phosphorus on the Reproduction of Three Species of Acroporid Corals, Ph. D. Thesis, Southern Cross University, Australia. Wilkinson, C. R.: 1998, Status of Coral Reefs of the World. Global Coral Reef Monitoring Network, Australian Institute of Marine Science, Townsville.