PII: S0025-326X(00)00201-0 Marine Pollution Bulletin Vol. 42, No. 7, pp. 554±568, 2001 Ó 2001 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-326X/01 $ - see front matter Temporal Variation in the Diversity and Cover of Sessile Species in Rocky Intertidal Communities Aected by Copper Mine Tailings in Northern Chile ~ JOSE MIGUEL FARINA* and JUAN CARLOS CASTILLA Departamento de Ecologõa, Facultad de Ciencias Biol ogicas, Ponti®cia Universidad Cat olica de Chile, Alameda 340, C.P. 6513677, Santiago, Chile Several coastal rocky shores in the northern Chile have been aected by the discharges of copper mine tailings. In spite of this, the temporal and spatial variation on the diversity and composition of their intertidal benthic communities has scarcely been studied. The objectives of the present study were to analyse and to compare quantitatively the temporal variation on the diversity, cover and composition of sessile species in rocky intertidal benthic communities of the northern Chilean coast, in relation to the presence of copper mine tailings. The results show that the drastic reduction on the sessile species diversity and the monopolization of the substrate exerted by the green algae Enteromorpha compressa, are common and permanent features of the intertidal rocky shores aected by copper mine tailings. Such spatial (between sites) and temporal (seasonal) variation of these changes has been associated with the relative concentrations of trace metals and inorganic particles of the mining wastes. Our results suggest that the mechanical eects of resuspended and settling tailings are a more likely cause. Ó 2001 Elsevier Science Ltd. All rights reserved. Keywords: copper; Chile; Enteromorpha compressa; rocky intertidal; ®ne ground wastes; diversity. Introduction Copper mining has historically been the most important economic activity in the northern Chilean region. The major copper mines and deposits in this region are found on the western slopes of the Andes Mountains, but minor mines and some processing plants are located on the coast (Castilla, 1983). As a consequence, for a long time, several sites of the coast had been aected by the dis- *Corresponding author. Fax: +56-2-6862610. E-mail address: [email protected] (J.M. Fari~ na). 554 charges of copper mine tailings (Miethke et al., 1992; Vasquez et al., 1999). In spite of this, the analysis of the eects of copper wastes on marine intertidal communities has been done mainly at one area aected by the El Salvador Copper Mine (Fig. 1) discharges (Castilla and Nealler, 1978; Castilla, 1983; Castilla, 1995; Correa et al., 1999, 2000; Pasko and Petiot, 1990). The occurrence of copper mine tailings in the seawater drastically change the composition and spatial distributions of the rocky intertidal communities, particularly on sessile species. One of the most dramatic changes reported has been a decrease in the number of sessile species and the monopolization of the rocky substrate by the green ephemeral alga Enteromorpha compressa (Castilla, 1995). Another result has been that in addition to the trace metals, copper mine tailings have a physical component (ground wastes) which modify drastically the coastal landscape (Castilla, 1983; Ellis, 1987; Pasko and Petiot, 1990). Nevertheless, intertidal communities' modi®cations have been explained solely with reference to the high concentration of trace metals (Correa et al., 1999, 2000), neglecting the possible role of the ground wastes as abrasive agents. So far, there have been no attempts to evaluate the temporal (i.e., seasonal) and/or spatial (i.e., between sites) variability in the changes exerted by copper mine tailings on the intertidal diversity and species composition. The aims of this work are to analyse the patterns of diversity on rocky intertidal communities of several northern Chilean coastal sites, with regard to the presence of copper mine wastes (trace metals and ®ne ground wastes), and to evaluate quantitatively their temporal and spatial variability. Materials and Methods Study sites The study was carried out on the rocky intertidal shores of four sites located on the northern Chilean Volume 42/Number 7/July 2001 Fig. 1 Location of the discharge and reference sampled (*) and previously described (Castilla, 1995) sites. coast: Enami, Las Conchas, Bandurrias and Santo Domingo (Fig. 1). Since the 1960s both Enami and Santo Domingo have been aected by the discharges of copper mine tailings derived from processing plants located close to the shore. At Enami, the euents are discharged southwards and have formed a tailing bed of approximately 2 km in length, along the southern side of the sampling site. At Santo Domingo, the waste discharges move northwards and have formed a tailing bed of approximately 10 km in length on the northern side of the sampling site. Las Conchas and Bandurrias, located about 15 km north of Enami and 19 km south of Santo Domingo, respectively, were considered to be non-contaminated sites, and used as reference sites. Seawater analysis Based on the results of previous studies, the main trace metals, Cu, Zn, and Cd, reported as abundant on Chilean copper mine orebodies and tailings euents were analysed (Castilla and Nealler, 1978; Veermer and Castilla, 1991). To evaluate the levels of these trace metals, six 1-l samples of seawater were taken from the shore of each site in July 1997, January 1998 and June of 1998. In the case of Enami and Santo Domingo, the samples were taken 1 km from the waste discharge points. Water samples were treated and analysed as indicated by Correa et al. (1996). At CESMEC Inc. lab- oratories, the samples were ®ltered through 0.45 lm Whatman GF/F ®lters and ®xed with nitric acid (Merck, supra pur). Dissolved trace metals in the samples were quanti®ed by potentiometric stripping analysis in stationary solution, using a computarized Radiometer ISS 820 analyser. To analyse the concentration of ®ne ground wastes, we used standard methods designed to measure the seawater concentrations of particulate inorganic (PIM) and organic matter (POM) (Bustamante, 1994; Rodriguez, 1999). During each sampling date, four samples of 0.5 l were ®ltered using Whatman GF/F glass ®ber ®lters. The ®lters, with a pore size of 0.45 lm, retain organic and inorganic particles of more than 0.7 lm in size. Concentrations of PIM and POM were determined by the dierences in weight between dried versus burned (at 500°C) ®lters. Prior to the drying and burning process the organic and inorganic particles caught in each ®lter were visually inspected using a stereomicroscope (Nikon SMZ-2T). This analysis allowed us to identify the possible sources for inorganic (i.e., sand or minederived sediments) and organic (i.e., small pieces of intertidal algae or planktonic organisms) particles. In the case of inorganic particles the dierent colours and textures of the sand (white in colour and smooth) and mine-derived (brown or black in colour and rough) particles, were used for their recognition. 555 Marine Pollution Bulletin Sampling design The sampling of the rocky intertidal at each site was carried out, every two months, from July 1997 to May 1998 (six sampling dates). A series of 20 plots of 0:25 0:25 m were randomly placed parallel to the shoreline, between the high and low intertidal levels. Plot randomization was developed using an equally 0.25 m spaced grid, which covered all the intertidal study area of each site. Each point of the grid was numbered and the random position of the plots in the grid was chosen taking the sequence numbers from a random numbers table and ranking them from the smallest to the largest (Kuehl, 2000). The levels were determined a priori using the high and low water marks predicted by tide tables, during days of similar tidal and sea conditions. Each plot was divided into a grid of 100 equally spaced intersection points. The sessile algae or ®lter feeding species occurring underneath each point were identi®ed to the lowest possible taxonomic level. The total cover of each species in the plot was obtained directly by the sum of their intersection points (Castilla, 1988). Data analysis The results of the seawater analysis (trace metals, PIM and POM concentrations) were contrasted using two-factor analysis of variance (ANOVA). The variations in the mean numbers and the mean covers of species were also contrasted using two-factor ANOVA (Winer, 1971). In both cases, sites and dates were considered as random factors because no a priori hypothesis was speci®ed about them, and because their levels represent one of the several potential combinations of sites and dates over which the study could be done (Underwood, 1997). After each analysis Tukey (HSD) multiple comparisons test was used (Day and Quinn, 1989). The normality of the data was tested using graphical procedures, and when appropriate (i.e., for cover), standard procedures of data transformations (i.e., Arc-sin) were used. Homogeneity of variance and independence of the data were veri®ed using Levene's and Durbing±Watson tests, respectively (Wilkinson et al., 1996). Spatial dominance and temporal incidence of the species To identify the most representative species occurring at each locality, we analysed the relationship between their spatial dominance and temporal incidence. We plotted the mean percentage of cover vs. the mean number of plots, in which each species was registered during the entire period of study, choosing in each case the species with signi®cant high cover and/or spatial incidence. Signi®cance (at a < 0:05) was calculated from the frequency distribution of the means generated using a bootstrap procedure, in which the original matrix containing both variables was re-sampled 1000 times (Manly, 1991). The patterns of spatial dominance of the sessile species at each date and sites were compared using rank/abundance plots (Magurran, 1988), consid556 ering the logged mean percentage of cover as an estimate of dominance (Clarke, 1990). Similarity on the species composition The Jaccard coecient of similarity (Jaccard, 1901; Sneath, 1957) was used to analyse the similarity and variability in the species composition observed at each site. This coecient, based on the presence ± absence of the species, has been widely used in ecology, and highly recommended for the analysis of species composition similarities (Hubalek, 1982). The patterns of similarity on the species composition were contrasted using one cluster diagram of the Jaccard coecients calculated for each combination of site and date. The cluster was constructed using un-weighted average linkage methods (Wilkinson et al., 1996) and signi®cant level of similarity was estimated using the distribution of the Jaccard coecients, calculated after bootstraping 1000 times the species composition matrix (Clarke, 1993). To analyse the temporal variability of species composition at each site, non-metric multidimentional scaling analysis (MDS) on the calculated matrix of Jaccard coecients was used. The number of dimensions to scale (2) was chosen considering the lowest value of the Kruskal MDS stress statistic calculated for 1±5 dimensions. The number of iterations (50), was selected considering the lowest value of the minimized Kruskal MDS stress statistics 0:068. The result of the MDS analysis was corroborated by the Sheppard diagram, which showed a signi®cant monotonic decreasing relation between the observed and estimated similarities (Clarke, 1993; Wilkinson et al., 1996). Using a cluster diagram of the Jaccard coecients, we compared the patterns of similarity on the species composition of the sites used in this study with those used in previous studies (Castilla, 1995). The comparison was done considering the species compositions reported on the rocky intertidal areas of four sites located near the city of Cha~ naral: Zenteno, La Lancha, Palito and Pan de Az ucar. La Lancha and Palito have been impacted by tailings waste from the El Salvador copper mine since the mid 1970s, while Zenteno and Pan de Az ucar have been considered non-contaminated (Castilla, 1995). Results Seawater analysis Dierent concentrations of copper (Fig. 2(a)) were observed in the seawater at each of the sites (F0:05;3 98:13, p < 0:0001). The sequence of signi®cant dierences was Santo Domingo 25:78 1:98 lg l 1 > Enami 12:23 1:90 lg l 1 > Bandurrias 3:08 1:04 lg l 1 and Las Conchas 1:53 0:36 lg l 1 . Bandurrias and Las Conchas were not signi®cantly dierent, and the pattern was persistent over time (F0:05;2 0:14, p 0:87). Volume 42/Number 7/July 2001 Fig. 2 Temporal variation of trace metal concentrations mean 1 EE in the seawater of the study sites. (a) copper, (b) zinc and (c) cadmium. In spite of the low concentrations of zinc (Fig. 2(b)), there were signi®cant dierences between sites (F0:05;3 29:08, p 0:0006. The sequence of dierences was Enami 1:98 0:28 lg l 1 > Las Conchas 0:45 0:18 lg l 1 > Bandurrias (less than 0:10 0:0 lg l 1 ) and Santo Domingo (less than 0:10 0:0 lg=l). Santo Domingo and Bandurrias were not signi®cantly dierent and the pattern was persistent over time (F0:05;2 0:55, p 0:61). For cadmium (Fig. 2(c)) there were signi®cant dierences between sites (F0:05;3 432:73, p < 0:0001). The concentration in Enami 3:76 0:62 lg l 1 was higher than that observed at Santo Domingo 1:94 0:07 lg l 1 , Las Conchas 1:56 0:19 lg l 1 or Bandurrias 1:02 0:08 lg l 1 . Santo Domingo, Las Con- chas and Bandurrias did not show signi®cant dierences, and the pattern was persistent with time (F0:05;2 1:18, p 0:368). High levels of Particulate Inorganic Matter in the seawater (Fig. 3(a)) were observed at Enami during September±October of 1997 and March±April of 1998. This site 221:91 212:12 mg l 1 showed signi®cant (F0:05;3 3:78, p 0:033) dierences with Santo Domingo 47:79 10:99 mg l 1 , Las Conchas 32:16 7:68 lg l 1 and Bandurrias 38:50 9:49 lg l 1 . The last three sites did not show signi®cant dierences between them. The concentration of POM in the seawater (Fig. 3(b)) did not show dierences between sites F0:05;3 2:13, p 0:14) and time (F0:05;5 1:38, p 0:28). However, 557 Marine Pollution Bulletin Fig. 3 Temporal variation mean 1 EE of the (a) PIM and (b) POM concentrations in the seawater of the sites. due to the high concentrations observed at Enami during September±October of 1997, the interaction between the factors of site and time was signi®cant (F0:05;15 30:08, p < 0:0001). Species composition and diversity patterns A total of 31 taxa were identi®ed in the 480 sampled plots (Table 1). Bandurrias and Las Conchas showed the higher number of taxa (26 and 29, respectively). Enami and Santo Domingo showed 10 and 8, respectively. The dierences in the number of taxa observed were due to the number of algae and to the number of ®lter feeding species. The mean number of species (Fig. 4(a)) showed differences between sites and time (Table 2(a)). Between sites, Enami 2:70 2:06 spp and Santo Domingo 3:22 1:70 spp had the lowest number of species and did not show signi®cant dierences between them. The highest mean numbers of species observed in Bandurrias 13:24 2:77 spp was signi®cantly higher than the one observed in Las Conchas 10:85 2:08 spp. Over time, the number of species observed during the periods of 558 July±August 8:85 5:54 spp and September±October of 1997 9:21 5:95 spp were signi®cantly higher than the observed in other dates (which ¯uctuated between 6.62±7.23 spp and did not show signi®cant dierences). This was due to the high mean number of species observed in Las Conchas and Bandurrias during these two periods. The mean number of algal species (Fig. 4(b)) followed the variations of the mean number of total species (see Fig. 4(a)). There were signi®cant dierences (F0:05;3 129:55, p < 0:0001) between the contaminated sites, Enami and Santo Domingo, and non-contaminated ones, Las Conchas and Bandurrias. Enami and Santo Domingo had the lower mean number of species (2:42 1:66 and 3:06 1:31, respectively) and there were no dierences between them. Las Conchas and Bandurrias showed the highest mean numbers (9:18 2:77 spp and 10:25 2:07 spp, respectively) and there were no signi®cant dierences between them. Over time, there were signi®cant dierences (F0:05;5 4:14, p 0:014). For Las Conchas, the period September± October of 1997 was signi®cantly higher in algal species 12:05 0:95 than the other periods. Volume 42/Number 7/July 2001 TABLE 1 List of the sessile species observed (X) at each site during the entire period of study. Taxa Algae Enteromorpha compressa Enteromorpha prolifera Ulva lactuca Chaetomorpha linum Ectocarpus confervoides Ralfsia expansa Colpomenia phaeodactyla Colpomenia sinuosa Petalonia fascia Scytosiphon lomentaria Glosophora kunthii Polysiphonia paniculata Porphyra columbina Gelidium chilense Gelidium lingulatum Corallina ocinalis Ceramium rubrum Hildenbrandtia lecannellieri Lithothamnion sp Baciliarophyta Filter feeding species Anthothoe chilensis Phymactis clematis Porifera Polchaeta-Sabellaridae Notochthamalus scabrosus Jehlius cirratus Balanus laevis Austromegabalanus psittacus Semimytilus algosus Perumytilus purpuratus Pyura chilensis Total Enami X X X X X X X X Las Bandurrias Santo Conchas Domingo X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X 10 26 29 X X X X X X 8 The pattern of variations in the mean number of ®lter feeding species (Fig. 4(c)), showed some dierences between sites F0:05;3 48:88, p < 0:0001. The sequence of dierence was: Bandurrias 2:99 1:07 > Las Conchas 1:67 0:86 > Enami 0:28 0:58 and Santo Domingo 0:16 0:48 spp. Enami and Santo Domingo did not show signi®cant dierences. Percentage of cover of the primary space The mean cover of species (Fig. 5(a)) did not show signi®cant dierences between sites or over time (Table 2(b)). However, due to the wide variability observed in Enami and Santo Domingo the interaction between sites and date was signi®cant (Table 2(b)). The mean cover of species observed in Enami during November±December of 1997 56:13 9:21% and in Santo Domingo during May±June of 1998 50:85 8:12%, were signi®cantly lower than all the other values registered (which ¯uctuated between 90% and 70%). For the mean cover of algal species (Fig. 5(b)), no signi®cant dierences were found between sites (F0:05;3 1:516, p 0:251) and over time (F0:05;5 0:608, p 0:695). Nevertheless, due to the important varia- tions observed within each of the four sites, the interaction between sites and date was signi®cant (F0:05;15 20:845, p < 0:001). In Enami, the mean cover observed during July±August 77:78 15:01% decreased through to November±December of 1997 55:90 9:08% and then it was followed by a recovery. For Las Conchas, from July±August of 1997 to January±February of 1998, there were no signi®cant dierences (with values near 77%). However, an important increase was observed from January±February of 1998 until May±June of 1998 90:57 5:42%. For Bandurrias a decreasing trend was observed from September± October of 1997 75:08 6:59% to March±April of 1998 56:98 5:73%. The trend was followed by a recovery. For Santo Domingo, from July±August of 1997 to March±April of 1998, there were no signi®cant differences (with values near 77%). However, a signi®cant decrease was observed during May±June of 1998 50:82 8:09%. As a result of all these changes the mean values observed at Enami during November±December of 1997, at Bandurrias from January to April of 1998, as well as at Santo Domingo and Las Conchas during May±June of 1998 were signi®cantly lower than the other values (see Fig. 5(b)). The mean cover of the ®lter feeding species (Fig. 5(c)) showed signi®cant dierences between sites (F0:05;3 27:57, p < 0:0001) but not over time (F0:05;5 0:31, p 0:899). Enami and Santo Domingo showed the lowest mean cover (0:15 0:44% and 0:02 0:06%, respectively) but there was no signi®cant dierence between them; while the highest covers of Bandurrias 16:92 8:66% and Las Conchas 5:69 5:64% were signi®cantly dierent. Over time within each site, Enami and Santo Domingo showed no signi®cant dierences. Important variations were observed at Bandurrias and Las Conchas. Due to that, the interaction between site and time was signi®cant (F0:05;15 13:90, p < 0:0001). For Las Conchas, from July±December of 1997 the mean cover increased, from 4:82 2:88% to 12:52 8:51%, and then decreased until May±June of 1998 2:02 2:14%. For Bandurrias, the most important variation was an increase in the mean cover during January to April of 1998, from 10:90 3:51 to 22:33 7:39%. Due to this, the mean cover of the ®lter feeding species during the period of January to April of 1998 were signi®cantly higher than the values observed in the other sites and dates. Spatial dominance and temporal incidence of the species The spatial dominance and incidence of the species at each site showed important dierences (Fig. 6). In both Enami and Santo Domingo the green algae E. compressa and `Bare Rock' were `items' with the highest dominance and incidence. The main dierence between these two sites was that at Santo Domingo the red encrusting alga Hildenbrandtia lecannellieri was important in terms of incidence. For Las Conchas, the green alga Ulva 559 Marine Pollution Bulletin Fig. 4 Temporal variation mean 1 EE on (a) the number of sessile species, (b) the number of algae species and (c) the number of ®lter feeding species, at the study sites. TABLE 2 Results of the 2-way ANOVA on: (a) the mean number and (b) the mean cover of sessile species, observed during the study period at each site. Source df MS (a) Site Date Site date Residual 3 5 15 456 34422.4 118.2 21.53 3.018 (b) Site Date Site date Residual 3 5 15 456 40110.4 11713.9 13587.9 663.3 560 F p 158.9 5.4 7.1 <0.0001 0.0045 <0.0001 2.9 0.8 20.4 0.06 0.52 <0.0001 Volume 42/Number 7/July 2001 Fig. 5 Temporal variation mean 1 EE on (a) the covers of sessile species, (b) the covers of algae species and (c) the covers of ®lter feeding species at the study sites. lactuca and `Bare Rock' were important in terms of incidence and dominance, while the brown algae Ectocarpus confervoides and H. lecannellieri were important in terms of incidence. For Bandurrias, the `Bare Rock' `item' showed high levels of dominance and incidence; U. lactuca and H. lecannellieri showed high levels of incidence and the barnacle Jehlius cirratus, the red algae Gelidium chilense and E. confervoides were important in terms of dominance. The dominance curve showed important dierences between sites. At Enami and Santo Domingo the rocky substrate was dominated by one or two `items' (E. compressa and/or `Bare Rock'). In Las Conchas and Bandurrias, there were no dominant species and the substrate was shared by several species. These dierences were consistent during the study period (Fig. 7). Similarity on the species composition Two main groups (Fig. 8), with a high and signi®cant level of similarity of their species composition, were separated in the cluster analysis: Enami ± Santo Domingo and Las Conchas ± Bandurrias. The subgroups separated within each main group showed a high level of similarity in the species compositions within each site. The diagram generated by the MDS analysis (Fig. 9), separated the group of Enami-Santo Domingo from the group of Las Conchas±Bandurrias. Enami was the site with the highest temporal variations. In the case of Las Conchas, Bandurrias and Santo Domingo, the temporal variations were restricted to a speci®c region of the diagram and followed a closed trend with cyclical tendencies. The species compositions of the contaminated and non-contaminated sites analysed in our study were in 561 Marine Pollution Bulletin Fig. 6 Spatial representation (% of cover, mean 1 EE) vs. Temporal incidence (mean no. of plots 1 EE) of sessile species at the study sites. The grey lines represent the limits at the 95% of the means. agreement with the results of Castilla (1995). The cluster analysis (Fig. 10) showed a signi®cant level of similarity between the non-contaminated sites Las Conchas, Bandurrias, Zenteno and Pan de Az ucar, and between the contaminated, Enami, Santo Domingo, La Lancha and Palito. In spite of their dissimilarity with the noncontaminated sites, the species composition patterns of the contaminated sites analysed by Castilla (1995) were dierent to the patterns observed in Santo Domingo and Enami. Discussion Seawater analysis The concentrations of trace metals and PIM in the seawater (Figs. 2 and 3) were in agreement with the subjective status of contaminated sites for Enami and Santo Domingo, and non-contaminated sites for Bandurrias and Las Conchas. Copper was the most important trace metal and their concentrations in both Enami and Santo Domingo were in the ranges reported in other copper contaminated coastal areas of Chile (Correa et al., 1999) and of the world (Bryan and Langston, 1992). The concentrations observed in Las Conchas and Bandurrias were 562 in the range of those observed in other non-contaminated sites of Chile (Castilla, 1983; Vasquez and Guerra, 1996) and of the world (Lewis, 1995). For zinc and cadmium, the concentrations observed in Enami and at Las Conchas, Bandurrias and Santo Domingo were in the range of other contaminated and non-contaminated sites respectively (Correa, 1999; Knauer and Martin, 1973). Both Enami and Santo Domingo presented tailing beds on their shores (Ingenierõa y Geotecnica, 1990). However, high concentrations of PIM were only detected in Enami. The dierence could be due to the particle size of the wastes occurring at each site. Based on stereomicroscope visual inspection, we found that sampled PIM at Santo Domingo was ®ner (less than 60 lm in average) than at Enami (more than 500 lm in average). Considering that the ®lters of both sites were saturated with PIM, it is probable that the method utilized (based on the weight dierences) does not re¯ect this pattern. The dierences in size of the particles sampled at Enami and Santo Domingo could be related with the mining extraction process used at each site. At Enami copper is puri®ed through lixiviation and at Santo Domingo by ¯otation (Cortez et al., 1996). Flotation produces ®ner particles (ranging between 50±100 lm) than lixiviation (ranging between 150±1000 lm). In Volume 42/Number 7/July 2001 Fig. 7 Dominance curves based on the mean cover of the sessile species occurring at each site, during the study period. ¯otation the mined rock is ground at least three times before the extraction, while in lixiviation the rock is ground only once (Biswas and Davenport, 1980). The high temporal variability of PIM concentration observed at Enami may be related to the occurrence of storms. As pointed out by Ellis (1987),in mining contaminated coastal waters, during windstorm a resuspension of the particles from tailing beds occurs. Hence PIM concentrations are highly dependent on the local oceanographic and atmospheric conditions. In the case of Enami, and for the northern Chilean coast, during September of 1997 and April of 1998, at least two important storms associated with the event of El Ni~ no Southern Oscillation (ENSO) of 1997 occurred (Glynn, 1988; Camus and Andrade, 1999). For POM, the high concentrations found at Enami during September±October of 1997 may also be related to the resuspension of ground wastes. Visual inspection showed that POM was composed of small pieces of green alga which perhaps were detached from the rocky intertidal zone by the abrasive eect of the resuspended PIM. In fact, after this period a signi®cant decrease on the mean cover of algae was observed at Enami (Fig. 5(b)). The high concentrations of PIM occurring in Enami during the period of March±April of 1998 were not associated with a high concentration of POM. During this period no algae particles were observed in the collected POM and moreover, no decreases of the mean cover of intertidal algae occurred at this site. Another aspect related with POM, is the dierence in the copper concentration between Enami and Santo Domingo. If the high concentration of POM observed at Enami provided more ligands for the complexation of copper (Sunda and Lewis, 1978), then it is possible that this locality showed a lower concentration of the dissolved metal in the water than Santo Domingo. The relationship between copper and POM must be analysed in future ecotoxicological studies. 563 Marine Pollution Bulletin Fig. 8 Cluster analysis of the species composition similarity of each site during the study period. The key for the sites is: E Enami, SD Santo Domingo, LC Las Conchas and, B Bandurrias. The dashed line represents the limit of similarity at a < 0:05. Species composition At Enami and Santo Domingo, we observed lower numbers and dierent compositions of sessile species than at Las Conchas and Bandurrias. The most important dierences in the species composition were related to the absence at the contaminated sites of ®lamentous Porphyra columbiana, and G. chilense and encrusting red algae C. ocinalis, as well as the absence of ®lter feeding species such as Jehlius cirratus, Notochthamalus scabrosus and Semimytilus algosus. Several factors may explain these dierences. Correa et al. (2000) proposed three hypotheses for the decreased diversity of algal species at one site of the northern Chilean coast aected by copper mine wastes. 1. High copper concentrations in the seawater prevent the growth of red and brown algae. Nevertheless, the result of their work showed that, under labora564 tory conditions, several species of red and brown Chilean algae are able to grow at high concentrations of copper (between 10 and 150 lg l 1 ). 2. The mixture of trace metals (Cu, Zn, and Cd) occurring on the seawater of contaminated sites prevented the growth of algae. Nevertheless, the result of their work showed that under controlled conditions, several species of red and brown Chilean algae were able to grow in the water of the contaminated sites (which contained the trace metal mixture). 3. The unusual high density of herbivore gastropods occurring on the contaminated site eliminated the normal algal diversity. To test this hypothesis, at the contaminated site, they conducted experimental exclusions of the grazers. This resulted in the fast colonization of red and brown algae on the treatment plots. It was concluded that the main explanation for the decreased algal diversity at the contaminated site was the high grazing pressure exerted by these gastropods. The last explanation (No. 3) has two problems. At their polluted site the gastropods had been observed for the last 6 years; however the pattern of low diversity of red and brown algal species has been observed for more than 20 years (J.C. Castilla pers. comm.). Likewise, during the entire period of our study, gastropods were absent (in Enami) or occurred in low densities (at Santo Domingo). However the pattern of low diversity in algal species and cover domination by E. compressa was observed at both sites. A complementary explanation for these patterns may be that the abrasive eects of tailings prevent the colonization of the algae, and moreover facilitate the growth of the ephemeral green algae. There are no studies directly related to the eect of ground mining-derived wastes on the diversity of rocky shore marine communities. However, in several studies the abrasive eects of naturally derived particles (i.e., sand) on the composition and diversity of marine organisms have been addressed (Airoldi, 1998; Daly and Mathieson, 1977; Menge et al., 1994; Gibbons, 1988; Graf, 1987; Moore, 1972; Robles and Cubit, 1981; Robles, 1982; Stewart, 1983). Daly and Mathieson (1977) working on the east coast USA demonstrated that highly sand-abraded rock surfaces, in the lower intertidal zone, were dominated by opportunistic annuals like Enteromorpha spp and showed a lower diversity of ®lter feeding species, like Mytilus edulis and Balanus balanoides. Robles (1982) showed that after the occurrence of storms, which drives sand on to the intertidal rocky shores, a decrease in the diversity of sessile species occurred. This decrease was followed by a temporary colonization and dominance by green algae, mainly Enteromorpha spp. Menge et al. (1994) reported that on intertidal rocky shores, the interactions between echinoderm predators and their ®lter feeding prey could be modi®ed by the burying eect of sand. The relationship between the occurrence of ®ne ground particles and the patterns of species composition Volume 42/Number 7/July 2001 Fig. 9 MDS plot of the species composition at each site during the study period. The key for the dates is 1 July±August 1997, 2 September±October 1997, 3 November±December 1997, 4 January±February 1998, 5 March±April 1998, 6 May± June 1998. Fig. 10 Cluster analysis of the similarity on the species composition between the sites analysed in this study (Enami, Las Conchas, Bandurrias and Santo Domingo) and the sites analysed in previous studies (La Lancha, Palito, Zenteno and Pan de Az ucar) (see text for details). The dashed line represents the limit of similarity at a < 0:05. at the sites aected by copper mine tailings, must be addressed in future studies. Temporal variations on the species mean numbers and cover In contrast to non-contaminated, the contaminated sites showed a low temporal variability in their number of species (Fig. 4). These patterns were observed for both algal and ®lter feeding species. There are no studies on the range and the temporal variation in the number of species at other contaminated sites of the northern Chilean coast. However, both the mean and the variation in the total number of species observed in Las Conchas and Bandurrias were similar to that observed at three Northern-Chile non-contaminated sites analysed during 1996±1997 (Camus and Andrade, 1999). During July±October of 1997 both Bandurrias and Las Conchas showed a high mean number of species but, due to the dierences in the mean number of ®lter feeding species (Fig. 4(c)) the values of Bandurrias were higher than Las Conchas (Fig. 4(a)). These dierences have also been observed between Chilean non-contaminated sites, and may be related with the local abundance of predators (i.e, sea stars) or with the local occurrence of upwelling (Camus and Andrade, 1999). Percentage of cover The mean percentage of cover ranged between 70± 90% at contaminated and non-contaminated sites. However, at non-contaminated sites the rock surface was occupied by algae and ®lter feeding species, while at contaminated sites it was almost solely occupied by algal species (Fig. 5(a)±(c)). Non-contaminated sites showed a lower temporal variability in the mean cover of species than contaminated sites. This dierence is related to the fact that at both Bandurrias and Las Conchas there was an inverse 565 Marine Pollution Bulletin temporal relation between the cover of algae and ®lter feeder species. This relation was not observed at Enami and Santo Domingo (compare Fig. 5(b) and (c)). At non-contaminated sites when a patch of bare rock is created, algae or ®lter feeder animals colonize it, while at contaminated sites it would either be colonized solely by algae or remain uncolonized (i.e., rock). Considering that primary substrate has been widely recognized as a limiting resource for intertidal communities (Paine, 1994), the results of our work indicate that at contaminated sites, apart from the changes in diversity, some important changes in the use and colonization of the substrate may occur. Spatial dominance and temporal incidence of the species In all sites, the `item' `Bare Rock' was important. The importance could be related with desiccation stress (Bertness and Leonard, 1997), especially important in the high intertidal zones of rocky shores located in desert areas (like the northern Chilean coast, Rojas et al., 2000). Apart from `Bare Rock', contaminated and noncontaminated sites showed important dierences for the rest of the analysed items. At Enami and Santo Domingo E. compressa dominated the substrate and the main dierence between both sites was the incidence of the red encrusting alga H. lecannellieri. This species was absent at Enami while at Santo Domingo it showed the same temporal and spatial incidence as at the non-contaminated sites. Considering that in terms of contamination the main dierence between Enami and Santo Domingo was related to the concentration, and more speci®cally to the size of PIM, this alga could be a good candidate to analyse the eects of ®ne ground wastes on intertidal organisms. In addition to the high incidence of H. lecannellieri, at Bandurrias and Las Conchas U. lactuca and E. confervoides were important. The main dierence between these sites was that the red alga G. chilense and the barnacle J. cirratus showed high dominance at Bandurrias and were not important at Las Conchas. At the contaminated sites, there was a spatial dominance of E. compressaand `Bare Rock'. In the case of non-contaminated sites, the spatial and temporal representation of `Bare Rock', U. lactuca, J. cirratus, E. confervoides, and H. lecannellieri have been recognized in other studies conducted in the northern Chilean coast (Camus and Lagos, 1996). During the period of study the contaminated sites showed a pattern of species dominance completely different from the one observed at non-contaminated sites. The main dierence was that at the contaminated sites a reduced number of species occurred and that only one of these species dominated the primary substrate. This pattern of dominance has been referred to as an indicator of highly polluted sites (Clarke, 1990; Warwick, 1986). The contribution of our study is the demonstration that the pattern of species dominance, at the sites aected by copper mine tailings, occurs permanently 566 over time, in spite of seasonal variation in the cover of other species. Similarity of the species composition During the study, the patterns of species composition observed at contaminated sites were signi®cantly different from the ones observed at the non-contaminated sites. Due to the major number of shared species, the non-contaminated sites showed a level of similarity in their species composition higher than that observed at the contaminated sites. The MDS diagram showed that within Bandurrias, Las Conchas and Santo Domingo, the pattern of species composition had restricted temporal variation, while in the case of Enami a high temporal variability was observed. These dierences were due to the fact that at Enami, in spite of the high incidence of `Bare Rock' and E. compressa, several species, like H. lecannellieri and E. confervoides, were observed for no more than one sampling date. This pattern could be related with the major temporal variability of some of the contaminants (like ®ne ground wastes). The comparative analysis of the species composition of our sites with the patterns of other sites located near the city of Cha~ naral, showed interesting results. In spite of the fact that the sites are separated by more than 200 km, the non-contaminated ones showed a high and signi®cant level of similarity. The contaminated sites of our study had signi®cant dierences with the contaminated sites of the Cha~ naral area. The high level of similarity at the non-contaminated sites may be related to the geographical characteristics of the intertidal communities on the northern Chilean coast. Based on a wide geographical analysis, Camus (1998) proposed that, due to the high levels of similarity in the species compositions of intertidal rocky shores communities, from 18°S to 33°S the northern Chilean coast should be recognized as a bio-geographic province. The pattern of dominance of E. compressa and `Bare Rock' has been observed in the four contaminated sites compared. The main dierence refers to the presence of rare species. Due to the occurrence of E. confervoides, R. expansa, and P. purpuratus (see Table 1), our contaminated sites showed a higher number of species (8±10) than those aected (4±5) by El Salvador copper mine discharges (Castilla, 1995). These dierences could be related to the concentrations of contaminants in the seawater. The sites located near the city of Taltal (our study) and the city of Cha~ naral (previous studies) have similar levels of dissolved trace metals (Correa et al., 1999) but they have important dierences in the incidence of ®ne ground wastes. There is no analysis published on the concentration of PIM in the seawater of the sites aected by El Salvador copper mine discharges, although the in¯uence of ®ne ground wastes in these sites has been widely recognized. Castilla and Correa (1997), pointed out that at least, 130 million tons of solid wastes have been discharged in the coast of Cha~ naral. Volume 42/Number 7/July 2001 Pasko and Petiot (1990) reported that these discharges formed arti®cial beaches more than 7 km long and so they had a huge eect on the coastal landscape. Finally, our study demonstrates that both the decreased diversity and the substrate monopolization exerted by the green algae E. compressa, are common and permanent features of intertidal rocky shores of the northern Chilean aected by copper mine tailings. The spatial (between sites) and temporal (seasonal) variation of this eect may be associated with the relative concentrations of trace metals and inorganic particles, on the mining wastes occurring at each locality. The explanations proposed in previous studies for these changes (Correa et al., 2000), based on the eects of herbivorous gastropods over the sessile species compositions, are not supported by our results. 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