Coral Reefs (2003) 22: 541550 DOI 10.

1007/s00338-003-0343-0

R EP O RT

Francisco Kelmo Martin J. Attrill Malcolm B. Jones

Effects of the 19971998 El Nino on the cnidarian community of a high turbidity coral reef system (northern Bahia, Brazil)

Received: 10 April 2002 / Accepted: 9 June 2003 / Published online: 17 October 2003 Springer-Verlag 2003

Abstract We are reporting on the results of a 4-year study that allowed for the analysis of the eects of the 19971998 El Nino Southern Oscillation (ENSO) event on the cnidarian community of the naturally highturbidity reefs of northern Bahia, Brazil. Cnidarian densities were signicantly dierent between pre- and post-ENSO years, with signicant consequent changes in community composition. BIOENV analysis identied variations in turbidity, mean temperature variance, and cloud cover as the factors best explaining changes in the community. We suggest that the 19971998 ENSO event, the most intense on record, had a differential eect on the cnidarian community. Highest mortalities were suered by minute hydroid colonies, partial mortality by octocorals and actiniarians, while large hydroid colonies and scleractinians were the least aected. Such an ability to survive under the stressful environmental regime imposed by this ENSO event is attributed to the presence of morphological pre-adaptations (e.g., size of colony polyps, abundance of certain nematocyst types) and the inherent phenotypic plasticity that results from long-term exposure to naturally stressful conditions. Keywords ENSO Hydroids Octocorals Actiniarians Phenotypic plasticity Environmental stress

Introduction
The 19971998 El Nino Southern Oscillation (ENSO) event was the most intense on record (McPhaden 1999a; Mo and Hakkinen 2001; Eakin 2001) and was associated with record high seawater temperatures in many parts of the tropical oceans (McPhaden 1999b; Elliot et al. 2001; Pezzi and Cavalcanti 2001). These high temperatures resulted in large-scale coral bleaching (Berkelmans and Oliver 1999; Linden 1999; Obura 2001; Glynn et al. 2001), although current reports of the consequent eects on coral reef organisms tend towards the qualitative and anecdotal. Additionally, many coral reef assessments of such impacts are often limited in both space and time (e.g. a single survey of a reef undertaken only in 1 year). Thus, because a coral reef ecosystem is the integrated sum of past and present biotic and abiotic events (Glynn and Colgan 1992), such snapshots may not represent the true nature of a disturbance and its impacts when assessed over larger temporal and spatial scales. The coral reefs of northern Bahia (Brazil) are 70 km from the city of Salvador and extend for 20 km between the beaches of Aba and Praia do Forte (123280S/ 123823W; Fig. 1). The reefs lie on the shelf adjacent to the coastline that extends between the Sao Francisco and Doce Rivers. This is the narrowest part of the eastern Brazilian Continental Shelf (average width 15 km), and the shelf edge is approximately 70 m deep (DHN 1993). In this area, two types of Holocene reef structures (Nolasco 1987) run parallel to the coastline: coastal emergent reefs adjacent to the beaches and exposed during low tide, and shallow-bank reefs located a few kilometers o the coast (Fig. 1). The Bahian reefs have developed in highly unusual conditions of frequent and rapid sea-level uctuations. A transgressive phase reaching a maximum of 5 m above present-day sea level at 5.1 ka B.P. was followed by a general regressive phase punctuated by two short-lived ($200 years) and abrupt oscillations (Martin et al. 1979, 1985, 1996). As a result of a drop in sea level to its

F. Kelmo M. J. Attrill (&) M. B. Jones School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, Devon, PL4 8AA UK E-mail: mattrill@plymouth.ac.uk Present address: F. Kelmo Conselho Nacional de Desenvolvimento Cient co e Tecnologico, Brazilian Research Council, 70750-901 Bras lia, Brazil

542 developed either on rock outcrops of various ages or on lines of Holocene beachrock (Nolasco 1987). Their lateral contour is irregular, sometimes presenting well-developed, spur-and-groove systems on the fore-reef side, while the back-reef is usually less irregular. The reef tops, eroded due to sea-level uctuations, present irregular thin columnar structures, cavities, meandering channels, and small caves. The small Pojuca River (mean annual ow of 32 m3/s, which was reduced to 20 m3/s during ENSO) discharges in the proximity of these reefs (between Praia do Forte and Itacimirim), supplementing the sedimentary load from the two major rivers in the area, the Sao Francisco (ca. 200 km north of the studied reefs) and Doce (ca. 180 km south of the reefs). The mean annual discharge of the Sao Francisco River is 32,980 m3/s, which was reduced to 1,768 m3/s during the 1997 1998 ENSO event. For the Doce River, the mean annual discharge is 80.5 m3/s, which was reduced to 50.2 m3/s during the 19971998 ENSO period. The coastal belt of the State of Bahia has a tropical humid climate. Annual average rainfall ranges between 1,300 mm in the north of the study area to 1,900 mm around Salvador City to the south (Leao et al. 1997), with no marked seasonal rainfall pattern. Average daily air temperature ranges from 23 (winter) to 28 C (summer) (Leao et al. 1997), with mean daily surface water tem peratures ranging from 25 (winter) to 28 C (summer), the maximum SST occurring between December and February of each year. Annual average salinity varies little (3536), although within reeftop shallow pools, salinity can range from 35 to 39. The pH of seawater varies only between 8.1 and 8.2 (Leao et al. 1997), but with no clear seasonal patterns. In January and September, dominant easterly winds occur. From October to December and from February to March, northeasterly winds are frequent, while from April to August, stronger southeasterly winds occur during storms (DHN 1993).

Fig. 1 Location map showing the coral reefs of the northern Bahia region (after Leao et al. 1997)

present position ($3.1 ka B.P.), the coastal reefs became emergent. The lowering of the sea level placed the reefs closer to the coastline and mobilized the western continent-derived terrigenous sediment toward the eastern reef system. This exposed the coastal emergent reefs to heavy sedimentation, high levels of turbidity, and the remnant emergent community to intense solar radiation. Therefore, due to natural environmental stress and biogeographical barriers, the Bahian reefs have a coral fauna distinct from that of the Caribbean, including a high proportion of endemic taxa and no branching corals. Due to the lack of baseline information on the coral reefs of Bahia, a monitoring program was initiated in 1995. This program was originally aimed at recording quantitatively the temporal and spatial patterns of biodiversity and community composition of reef-associated invertebrates. However, during the investigation there was a marked increase in global seawater temperature (Pezzi and Cavalcanti 2001; Kumar et al. 2001) associated with the 19971998 El Nino Southern Oscillation (ENSO). Here we present the rst quantitative results of a multi-year (19951998) monitoring program of the cnidarian community that has developed under naturally turbid conditions. We discuss both the adaptability and susceptibility of these organisms to a large-scale natural environmental disturbance (coincident with the 1997 1998 ENSO event), as well as speculate on the ecological perspectives of such a disturbance for these reefs.

Sampling Benthic population density data on the cnidarian community of four shallow-bank reefs (submerged) of northern Bahia (Fig. 1) were collected annually (between April and May) from 1995 to 1998 by scuba diving. Quantitative samples were taken with 35 1)m2 quadrats positioned randomly on each reef (depths 1020 m), giving a total of 460 quadrats over the survey period. Macrospecimens (i.e., corals, anemones, zoanthids, and large hydroid colonies) were counted in situ. The majority of hard coral in Bahia is present as comparatively small, isolated coral heads rather than extensive reefs, so individual colonies would be easily enumerated using this quadrat size. Whole small hydroid colonies were collected for identication, and their quantication follows Gili and Ros (1985). Voucher specimens, collected each year, are stored at the scientic collection of the Departamento de Zoologia, University Federal of Bahia. Relative abundance analysis was assessed using the progressive scale proposed by Peixinho and Peso-Aguiar (1989), resulting in density values per m2. Large-scale environmental parameters for the survey area (sea surface temperature, solar irradiance, air temperature, rainfall, and cloud cover) were obtained from the Brazilian Meteorological Institute (INMET). INMET data are collected three times a day and the values presented in this paper represent the annual average of these data. INMET data are classied internationally in ISO9001. Local physicochemical data (seawater temperature, salinity, pH, and turbidity) were recorded across all four reef sites (10 replicates/reef giving 40 measurements spread over the sampling period). Such samples were taken every month for the rst 24 months to determine any seasonal patterns; these were only evident for temperature (Kelmo 1998), so replicated measurement of these variables across the sampling month only (due to logistical constraints following 1996) was considered adequate to allow comparison between years. Temperature, salinity, and pH were recorded using a YSI63 (Yellow Spring Industries) electronic eld meter, while turbidity was assessed using a secchi disk, both deployed from a boat. A number of studies has

Materials and methods

Study area The studied reefs (Fig. 1) are complex elongated structures varying from 500 to 1,800 m in length, from 400 to 500 m in width, and in water depths between 10 and 40 m. The reefs have

543 Table 1 Summary of physicochemical data recorded from the shallow-bank reefs throughout the sampling period (meanSE) Parameter recorded Large-scale (n=120) Sea-surface temperature (C) Solar irradiance (m W/m2) Air temperature (C) Rainfall (mm) Sky cover (MM) Local (n=40) Sea-water temperature (bottom; C) Salinity pH (H)1) Mean turbidity (Secchi in m) Turbidity range during survey period (Secchi in m) Mean value 1995 25.40.04 2120.02 25.80.01 1420.02 4.60.01 25.10.01 36.30.11 8.20.02 1.60.08 1.41.7 1996 25.40.01 2080.02 25.90.02 1950.02 4.60.01 25.00.01 36.30.04 8.20.01 1.60.11 1.42.2 1997 25.40.01 2190.05 26.60.01 1360.02 4.50.01 25.40.01 36.40.17 8.30.02 1.80.06 1.52.2 1998 27.60.02 2400.02 28.80.01 1160.02 4.00.01 26.90.01 36.70.09 8.20.02 2.50.05 2.22.7 1609.7 185513 11129 1819067 50867 482,488 1.925 2.111 21.711 p p p p p <0.001 <0.001 <0.01 <0.05 <0.001 F value Degree of signicance in 1998

p <0.001 p >0.05 p >0.05 p <0.001

shown high-frequency natural variation in water sediment content at coral reefs (e.g. Larcombe et al. 2001) related strongly to waves. Secchi disks are a relatively crude technology which can only provide a rough indication of variations in turbidity. As well as reecting the limited available equipment in the comparatively remote study area, we consider that Secchi measurements were sucient in reecting the overall suspended sediment regime in this naturally turbid region and would indeed indicate any major changes between years. Depth (below low tide) was recorded at each sampling station.

Results
Environmental parameters All environmental variables, except pH and sea-surface salinity, were signicantly dierent in 1998 compared with the three preceding years (Table 1). 1998 was characterized by warmer air and sea temperatures, reduced cloud cover and rainfall, higher incoming solar radiation, and reduced turbidity (due mainly to reduced river runo following decreased precipitation). There was no signicant dierence in any of the parameters between the reefs (ANOVA, all p >0.05), and within the rst 2 years (non-ENSO), there was little variability between months. The abnormal environmental conditions associated with ENSO commenced in mid-March 1997 and lasted until November 1998 (INMET).

Data analysis Univariate community parameters were calculated for each reef on each sampling occasion, namely Margalefs richness index (d), Shannon-Wiener diversity index (He), and Pielous Evenness index (J). The signicance of dierences between years was assessed using either ANOVA (cnidarian community parameters, normally distributed environmental variables) or Kruskall-Wallis (non-normal environmental data) tests. A triangular matrix of similarities between samples was computed using the similarity coecient of Bray and Curtis (1957), the cnidarian data rst being transformed [ln (x+1)] in order to reduce the inuence of dominant taxa (Clarke and Warwick 1994). The similarity matrix was subjected to clustering and ordination analyses using the PRIMER (Plymouth Routines in Multivariate Ecological Research) package (Carr 1996). Clustering was done by a hierarchical agglomerative method using group-average linking, resulting in a dendrogram. Ordination was by non-metric multidimensional scaling (MDS). The contribution of species to dissimilarities between the groupings observed in the cluster and ordination analyses was examined using the SIMPER procedure (similarity percentages; Clarke 1993). The BIOENV method (Clarke and Ainsworth 1993) was used to investigate the relationship between environmental variables (pre- and post- El Nino) and the cnidarian community data. This method is used as an exploratory tool in ways analogous to multiple regression (Clarke and Ainsworth 1993) and correlates the similarity matrix derived for the cnidarian communities with an equivalent for the suite of environmental measurements taken at each site. Results are expressed as a Spearmans correlation coecient (r), ranked in the order of which single variable or combination of variables best explains the observed community patterns (Clarke and Ainsworth 1993). The results (maximum of 1) indicate the proportion of variance in the community data explained by these environmental variables (see Clarke and Ainsworth 1993 for full details). Difference in cnidarian community composition between years was tested for signicance using ANOSIM (Clarke and Green 1988).

Cnidarian community Forty-eight species of cnidarian were recorded from the shallow-bank reefs (Table 2). Their proportional distribution within the phylum was as follows: Hydrozoa (30 spp.), Scleractinia (8 spp.), Octocorallia (5 spp.), Actiniaria (4 spp.), and Zoanthidea (1 sp.). There were similar abundance patterns in each year of the study. Among the hydroids, Thyroscyphus ramosus, Clytia hemisphaerica, and Clytia gracilis were the most abundant species, while Millepora alcicornis, Halecium tenellum, and Sertularella diaphana were the least abundant. For the octocorals, Carijoa riisei and Muriceopsis sulphurea were the most abundant, and Phylogorgia dilatata and Plexaurella dichotoma were the least abundant. Pseudoactinia melanaster and Actinia bermudensis were the most abundant actiniarians. Among the scleractinians, Siderastrea stellata and Favia gravida were the most abundant, while the endemic Mussismilia braziliensis and Montastrea cavernosa were the least abundant.

544 Table 2 Mean density (m2), standard error of mean, average dissimilarity in comparison with previous years, and degree of signicance in density variation of cnidarian species recorded on the four shallow-bank reefs assessed throughout the sampling period 19951998 Species Mean density 1995 Hydrozoa Turritopsis nutricula Rhizodendrium sterreri Parawrightia robusta Bimeria vestita Eudendrium carneum Pennaria disticha Millepora alcicornis Hebella scandens Halecium bermudense Halecium tenellum Monotheca margaretta Plumularia oridana Plumularia setacea Halopteris diaphana Halopteris polymorpha Monoastechas quadridens Aglaophenia dubia Aglaophenia latecarinata Macrorhynchia phillipina Clytia gracilis Clytia hemisphaerica Clytia linearis Clytia noliformis Obelia dichotoma Thyroscyphus ramosus Dynamena crisioides Dynamena disticha Sertularella diaphana Tridentata distans Tridentata marginata Octocorallia Muriceopsis sulphurea Carijoa riisei Plexaurella dichotoma Phylogorgia dilatata Neospongodes atlantica Actiniaria Pseudoactinia melanaster Bunodosoma cangicum Phyllactis praetexta Actinia bermudensis Scleractinia Agaricia agaricites Siderastrea stellata Porites astreoides Favia gravida Montastrea cavernosa Mussismilia braziliensis Mussismilia hispida Mussismilia harttii Zoanthidea Palythoa variabilis 1996 1997 1998 Average dissimilarity in 1998 0.26 0.05 0.12 0.03 0.01 0.12 0.08 0.02 0.41 0.19 0.25 0.18 0.41 0.52 0.32 0.32 0.51 0.31 0.17 0.89 1.35 0.56 0.47 0.05 0.21 0.76 0.09 0.62 0.37 0.06 0.47 0.15 0.05 0.03 0.04 0.18 0.19 0.29 0.16 0.22 0.71 0.08 0.57 0.22 0.07 0.07 0.25 0.29 Degree of signicance in 1998 p <0.001 p <0.01 p <0.01 p <0.001 p <0.001 p <0.001 p <0.001 p <0.05 p <0.01 p <0.01 p <0.01 p <0.01 p <0.01 p <0.001 p <0.01 p <0.001 p <0.001 p <0.01 p <0.001 p <0.001 p <0.001 p <0.001 p <0.001 p <0.001 p>0.05 p<0.001 p<0.001 p>0.05 p<0.05 p<0.001 p>0.05 p<0.01 p>0.05 p>0.05 p>0.05 p>0.05 p>0.05 p<0.05 p>0.05 p<0.05 p>0.05 p<0.001 p<0.05 p<0.001 p<0.01 p<0.001 p<0.001 p>0.05

0.270.06 0.290.03 0.190.02 0.580.04 0.690.05 0.890.08 0.120.02 0.660.12 0.140.03 0.120.02 0.930.15 0.370.05 0.290.05 0.200.03 0.110.03 0.720.08 0.550.06 0.630.12 0.430.06 2.100.25 2.470.11 1.690.12 1.560.14 0.670.10 2.300.12 0.670.07 0.570.13 0.170.04 0.870.14 0.630.06 0.990.12 1.910.12 0.080.08 0.060.03 0.480.10 0.630.07 0.250.07 0.440.03 0.430.14 0.690.07 1.020.04 0.880.07 1.020.03 0.620.03 0.310.02 1.010.08 0.720.05 0.370.05

0.440.05 0.400.05 0.270.04 0.630.04 0.780.05 1.010.08 0.070.01 0.720.12 0.300.07 0.140.02 1.130.17 0.470.06 0.350.07 0.270.04 0.180.07 0.850.08 0.570.09 0.740.11 0.530.06 2.360.22 2.430.11 1.700.20 1.840.19 0.730.08 2.330.15 0.750.07 0.660.14 0.150.06 1.070.19 0.850.09 1.020.12 2.120.20 0.080.08 0.080.05 0.510.10 0.670.11 0.330.08 0.470.03 0.430.17 0.660.08 1.050.06 0.990.07 1.050.05 0.670.04 0.330.02 0.980.06 0.830.03 0.380.04

0.280.04 0.340.04 0.210.03 0.570.02 0.730.05 0.940.08 0.070.01 0.750.10 0.300.04 0.140.02 1.080.16 0.440.06 0.320.04 0.290.04 0.210.03 0.920.07 0.640.10 0.760.10 0.550.05 2.410.20 2.440.15 1.860.19 1.980.20 0.860.10 2.440.15 0.730.05 0.650.10 0.130.04 1.150.18 0.910.06 0.940.11 1.990.20 0.070.07 0.070.06 0.450.10 0.660.11 0.230.04 0.430.05 0.510.16 0.590.07 1.050.05 0.960.08 1.020.06 0.510.03 0.270.01 0.920.09 0.750.05 0.340.04

0.080.03 0.150.04 0.080.03 0.260.05 0.320.02 0.350.06 0.020.01 0.310.08 0.020.01 0.020.01 0.330.09 0.130.04 0.050.02 0.010.01 0.010.01 0.170.04 0.150.05 0.240.08 0.010.01 0.170.09 0.570.13 0.440.10 0.770.18 0.240.07 2.220.22 0.270.06 0.090.03 0.000.00 0.440.08 0.370.02 0.740.13 1.020.11 0.040.04 0.040.04 0.210.07 0.360.05 0.070.03 0.300.04 0.150.09 0.380.06 1.010.05 0.450.03 0.870.02 0.350.03 0.150.04 0.440.07 0.460.04 0.260.03

All species declined in density in 1998 compared with preceding years. This decline was signicant for 77% of species. There was no signicant reduction in density for Thyroscyphus ramosus (Hydrozoa); Muriceopsis sulphurea, Plexaurella dichotoma, Phyllogorgia dilatata, and Neospongodes atlantica (Octocorallia); Pseudoactinia melanaster, Bunodosoma cangicum, and Actinia

bermudensis (Actiniaria); and Siderastrea stellata (Scleractinia) (Table 2). There were no signicant dierences in species density, richness, diversity, and evenness between reefs (ANOVA, all p >0.05). There were, however, signicant interannual dierences (Table 3). Species diversity (ANOVA-one-way, F=36.240, p <0.0001), species

545 Table 3 Mean values and standard deviation for density (m2), species richness (Margalef s d ), diversity (Shannon-Wiener H ), and evenness (Pielous J) of cnidarian communities sampled between 1995 and 1998 on the shallow-bank reefs of northern Bahia Year 1995 1996 1997 1998 Density 33.733.27 37.333.71 36.773.62 15.992.68 Richness 13.070.59 12.680.62 12.730.59 14.431.24 Diversity 3.560.03 3.590.03 3.560.03 3.310.07 Evenness 0.930.01 0.930.01 0.930.01 0.890.03

evenness (ANOVA-one-way, F=6.542, p <0.0072) and species density (ANOVA-one-way, F=36.503, p<0.0001; ANOSIM test, R=0.298, p=<0.02) were all signicantly lower in 1998 compared with preceding years. There was no signicant dierence in species richness in 1998 compared with preceding years (ANOVA, p >0.05). The dendrogram grouped all the reefs sampled from 1995 to 1997 into one cluster (average similarity of 95.6%) with each reef being clearly separated within a main group; samples from 1998 (average similarity of 88.4%) formed a separate cluster (Fig. 2). The SIMPER analysis indicated that the zooxanthellate Thyroscyphus ramosus, Siderastrea stellata, Carijoa riisei, Favia gravida, Muriceopsis sulphurea, and the azooxanthellate Clytia gracilis varied the least between year-clusters. The azooxanthellates Macrorhynchia phillipina, Sertularella diaphana, Halopteris diaphana, Halopteris polymorpha, and Halecium bermudense demonstrated the greatest change in abundance between years and contributed most to the dissimilarities (Table 2). MDS ordination illustrates the 1998 change (Fig. 3). This analysis clustered communities from the shallowbank reefs into two distinct groups including (1) the

Fig. 3 MDS ordination of the cnidarian community data from the shallow-bank reefs from northern Bahia throughout the sampling period, 19951998, based on [ln (x + 1)])transformed species densities and Bray Curtis similarities (stress 0.01). P Praia do Forte, I Itacimirim, G Guarajuba and A Aba

samples taken in 1998 (ENSO period) and (2) the samples collected before 1998 (non-ENSO period). However, when analyzed separately, each cnidarian group demonstrated a subtly dierent response pattern, with the specic direction of change in the community for 1998 varying between groups (Fig. 4AD). Two further multivariate analyses were undertaken following regrouping of data from each site into zooxanthellate and azooxanthellate species to investigate whether the

Fig. 2 Dendrogram (hierarchical clustering using group-average linking) of the cnidarian assemblages on the four shallow-bank reefs based on Bray Curtis similarity matrix of [ln (x+1)]) transformed species densities. P Praia do Forte, I Itacimirim, G Guarajuba, A Aba , Year 19951998

Fig. 4 MDS ordination of community data for four dierent taxa of cnidarians from the shallow-bank reefs from northern Bahia throughout the sampling period 19951998, based on [ln (x+1)]) transformed species densities and Bray Curtis similarities. A Hydrozoa (stress 0.01) B Octocorallia (stress 0.01), C Scleractinia (stress 0.03), D Actiniaria (stress 0.04). Dotted arrows indicate the direction of change

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two groups of organisms demonstrated dierent responses. The resulting ordinations (Fig. 5A, B) demonstrated patterns very similar to the community responses of the taxonomic group dominating each of these categories (i.e., hydroids for azooxanthellate, scleractinian corals for zooxanthellate). The ENSO event therefore had a notable, and similar, impact on species whether or not they contained symbiotic zooxanthellae. BIOENV analysis indicated that variation in turbidity (r=0.32) was the main environmental factor best explaining the community dierences on the assessed reefs in the years before El Nino (19951997). However, a combination of turbidity (r=0.65), mean temperature (r=0.64), and cloud cover (r=0.56) best explained the large changes in the community in 1998.

Discussion
Multivariate analysis demonstrated that the cnidarian community of the Bahian reefs in 1998 was signicantly dierent from that of previous years. All cnidarian groups were similarly aected, with only subtle dierences in responses between taxa. Considering the documented large-scale eects of the 19971998 El Nino Southern Oscillation on coral reefs (Wilkinson and Hodgson 1999), it is reasonable to attribute the notable reduction in species density in 1998, linked with dierences in environmental variables (increased temperature and solar radiation, reduced turbidity, cloud cover, and rainfall), to the 19971998 ENSO. Species containing zooxanthellate did not demonstrate a dierent response to azooxanthellate species that was independent of taxonomic grouping; azooxanthellate species displayed a similar pattern of change to hydroids, whereas zooxanthellate patterns were similar to the ordination for hard corals (which represent the vast majority of zooxanthellate species present in the study region). It is therefore unclear whether the subtle dierences in responses of the two groups is due to the presence of symbiotic
Fig. 5 MDS ordination of community data for zooxanthellate and azooxanthellate cnidarians from the shallow-bank reefs from northern Bahia throughout the sampling period 19951998, based on [ln (x+1)])transformed species densities and Bray Curtis similarities. A Zooxanthellate (stress 0.03), B Azooxanthellate (stress 0.01). Arrows indicate the direction of change

zooxanthellae or simply reects dierences in responses of the two taxonomic groups. Certainly, there is no rm evidence to suggest that, for example, zooxanthellate species (of whatever taxon) are less susceptible to the stresses imposed by the ENSO event than azooxanthellate species, but further investigation is required to elucidate any dierences between these two categories of organisms. During the 19971998 ENSO period, the northeastern coast of Brazil experienced sustained and strong surface warming (Pezzi and Cavalcanti 2001), which resulted in prolonged increased sea-surface temperatures for the entire period, unprecedented in recent times (Kumar et al. 2001). Such an anomaly is normally accompanied by reduced nutrient replenishment to sunlit surface waters (Barber and Chavez 1983) with consequent depression of the phytoplankton production (Barber and Chavez 1986; Glynn 1988). This causes a disruption of trophic links to a variety of consumer groups (Glynn 1990), resulting in irreversible damage to the coral-reef-associated assemblages. During the 1997 1998 ENSO event in northern Bahia, mean seawater temperature increased about 1 C above previous maxima. At the same time, reduced rainfall contributed to a reduction of the continental sediment load brought to the sea by the local rivers, reducing turbidity, increasing penetration of solar radiation, and causing prolonged warming of shoal waters. The impact of solar radiation was accentuated by a signicantly reduced cloud cover during the ENSO event, all resulting in high ultra-violet radiation (UVR) reaching the reef community. While measurements of rainfall and solar radiation are robust (continual meteorological monitoring), measurements of turbidity were taken on-site using a Secchi disk over the month of sampling (April/May), and therefore potentially only reect specic conditions during that month. However, the consistency of data collected by this method over the years prior to ENSO highlights the natural background situation in these Bahian reefs, namely high and continual turbidity due to river runo (the maximum Secchi value outside 1998 was only 2.2 m). The sampling period in 1998 occurred at the height of the ENSO event and Secchi values taken over this month were signicantly higher than all values in previous years (and outside the range of sampling during a continuous 24 months), indicating a reduced overall turbidity regime. Due to the limited temporal

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period of sampling, we can only denitely state that lower turbidity conditions occurred during this month of 1998, while low rainfall and river discharge were features of the months preceding the ENSO in this region, and we regard it as fair to assume that such low-turbidity waters were present over the reefs for 16 months during the ENSO period. Whatever the time period, it is clear that the reefs were receiving higher UVR during ENSO than at any time previously recorded, and measurements taken in subsequent years (19992000) revealed a return to pre-ENSO turbid conditions (Kelmo 2002). The extensive warming and meteorological anomalies experienced in NE Brazil are consistent with the impact of ENSO events in the study region (Hastenrath 1978; Horel et al. 1986) and reect environmental changes experienced elsewhere in 1998 (Glynn et al. 2001). The two most likely explanations for the noted impact on the cnidarian community are therefore the disruption of trophic links caused by the extensive warming event and the detrimental impact of increased UVR reaching the organisms. Experimental manipulations of coral reef organisms in the eld have conrmed that UVR could be an environmentally relevant stressor able to cause death, inhibition of growth, and bleaching (Shick et al. 1996). Jokiel (1980) has demonstrated that cryptic reef epifauna were killed by acute exposure to solar UVR in shallow water and suggested that the structure of coral reefs was aected by relative UV tolerances of their constituent species. Sublethal eects of the UV component of sunlight include depressed calcication and skeletal growth (Roth et al. 1982). Glynn (1993) has demonstrated that increased penetration of solar radiation (including UVR and PAR) into clear seawater is able to induce coral bleaching and mortality. A further, and simultaneous, potential stressor arises from the decline in productivity and subsequent reduction of the food supply following the ENSO warming period. This leads to the disruption of many trophic links for both zooxanthellate and azooxanthellate cnidarians and therefore can have an additional impact on the cnidarian community. In the case of the zooxanthellate species (e.g. coral, anemones, zoanthids), the undernourished polyps/colonies provide fewer nutrients to the symbiotic zooxanthellae (Brown and Ogden 1993), which are subsequently lost. Both azooxanthellate and zooxanthellate species can therefore be aected, and although mechanisms of impact may vary, the immediate eects of this process for both groups are (1) an increase in respiratory metabolism and (2) a decline in cnidarian proteins, lipids, and carbohydrates (Glynn et al. 1985; Hoegh-Guldberg and Smith 1989; Kleppel et al. 1989; Glynn and DCroz 1990; Goreau and Macfarlane 1990; Szmant and Gasman 1990; Glynn 1993). The combination of these two eects reduces growth and/or calcication rates and impairs reproduction (Glynn 1993). It is possible, therefore, that cnidarians lacking either morphological or physiological preadaptations are unable to compete for food during periods of stress, and can potentially disappear from the

reef environment. On the other hand, phenotypically plastic species manage to keep feeding and, although their densities may be reduced, the population survives on the reef during periods of environmental stress such as that caused by an ENSO event (Kelmo and Attrill 2001). Among the putative cosmopolitan hydroids recorded in the present study, it was possible to identify two different immediate responses to environmental stress including (1) density and richness remained fairly constant, and (2) reduction of both densities and richness. For example, Thyroscyphus ramosus (Leptothecatae, Thyroscyphidae) has a variable phenotype and is able to colonize a wide range of habitats where there is a hard substratum for attachment (Kelmo and Peixinho 1996). This species demonstrates a reduced colony growth rate under stress conditions and a consequent decrease in colony biomass (Kelmo and Peixinho 1996). However, when under stress, T. ramosus is able to increase the abundance of microbasic mastigophores around the tentacles (Kelmo et al., unpublished data), allowing an increased food capture rate. Similarly, Clytia hemisphaerica and C.gracilis (Leptothecatae, Campanulariidae) show an adaptive phenotype (e.g., size of hydrotheca/ tentacles, and abundance of certain types of nematocyst; Kelmo and Attrill 2002) under stressful physical conditions such as those experienced in colonies inhabiting areas of soft sediment. These campanulariids are usually smaller than those reported from Europe (Cornelius 1982, 1995) or from Bermuda (Calder 1991). It seems, therefore, that hydrozoans with phenotypic responses to environmental conditions are better able to survive changed conditions following periods of environmental stress. The second type of response among hydrozoan groups (reduction in both density and richness) occurs in species that require very specic environmental conditions (e.g. the zooxanthellate Millepora alcicornis, and the azooxanthellates Halecium tenellum and Sertularella diaphana). These organisms appear to lack morphological/phenotypic exibility since all specimens of these species examined in this study were remarkably similar to the literature descriptions (Calder 1988, 1991; Migotto 1993; Cornelius 1995; Souza 1997) with very little variation in the population evident. Scleractinian corals from the studied reefs seem to be quite resistant to environmental stress. There was a signicant decrease in the density of colonies but the richness remained fairly constant and the response to stress conditions was similar for all reefs (Fig. 4C). The physical characteristics of the species recorded here were similar to literature descriptions (Laborel 1969), and no evident phenotypic modication was noted. It is important to note that a peculiar coralline fauna exists in the south Atlantic with several endemic species (e.g. Mussismilia braziliensis, M. hispida, M. harttii, and Favia gravida; Laborel 1969; Leao 1982, 1994). The size of the polyps and the ciliar mechanism of the corals are responsible for the settlement success of these species in

548

the south Atlantic (Leao and Ginsburg 1997), favoring either the colonization of turbid waters or facilitating prey capture. In addition, all species recorded in this study form massive colonies (with high metabolic rates), which, as Gates and Edmunds (1999) tentatively concluded, potentially acclimatize more eectively to environmental changes than those with low metabolic rates such as branching species. While further experimental evidence for this theory has yet to be obtained, it can be speculated that the coralline fauna from northern Bahia displays evolutionary modications in behavior, morphology, and physiology, enabling them to photoacclimate to changing light conditions (Gates and Edmunds 1999). However, the taxonomy of scleractinian corals from Brazilian waters has not been properly addressed, and a detailed taxonomic review is required to verify the distinctiveness of these endemics, including data on molecular biology and ecology, endosymbionts, and behavior. Kelmo (1998) described seven species of scleractinian corals from Bahia, commenting on their behavior under stressed conditions, with emphasis on coral bleaching and mortality. He suggested that these species were well adapted to the naturally occurring conditions of high turbidity and temperature found o the northern coast of Bahia. However, species such as Porites astreoides and Agaricia agaricites seem to be less tolerant to environmental changes than other scleractinians; they are the rst to bleach, and the last to recover (Kelmo 1998). In addition, data from the present study suggest that P.astreoides and A. agaricites were the most sensitive scleractinians to the environmental stress of 1998 with marked decrease in their density. In contrast, Siderastrea stellata did not show any signicant reduction in density in 1998, and it is the most resistant scleractinian species recorded in the south Atlantic. This species presented the minimum degree of bleaching and mortality on the northern coast of Bahia (Kelmo 1998). Sessile cnidarians require specic environmental conditions for continued existence, namely warm waters with low turbidity and luminosity (Castro 1990, 1994). Additionally, many facets of the biology and ecology of these organisms remain poorly understood, and further studies are required urgently before any robust conclusion about the groups response to stress can be developed. The eect of environmental changes on cnidarian distribution is dicult to predict for the phylum as a whole due to dierences in responses of individual classes (Kelmo and Attrill 2001). However, we suggest that aspects of cnidarian biology that potentially have inuence on the response expressed by disparate taxa within the phylum include: size of colony/polyps, phenotypic plasticity, life cycles, feeding and reproductive behavior, geographic distribution, and nematocyst complement. In summary, the Bahian coral community has evolved and developed under natural conditions of high temperatures and high turbidity. Together with biogeographical barriers, these prevent the colonization of large numbers of coral taxa that are common elsewhere

in the Atlantic. The corals and other cnidarians of Bahia are remarkably resistant to these natural stresses that might result in catastrophic eects on other reef systems, but despite this, the 19971998 ENSO event had major impacts on Bahian coral reefs. This was the most severe ENSO on record, and whether the responses documented in this study are a consistent feature of all ENSOs or just this exceptionally severe event, remains unclear because no previous data from Brazil are available. Further monitoring, however, will allow the impact of any other ENSO event to be determined. The highest mortalities following the 19971998 ENSO were suered by the minute hydroid colonies, partial mortality by octocorals and some actiniarian species, and the lowest mortality by large hydroids and scleractinians (except Agaricia agaricites and Porites astreoides). If this response of cnidarians is typical of periods of intense sea warming, then more frequent episodes of such warming would have signicant longterm eects on the surviving coral reef cnidarian population. These would include changes in functioning such as increased predation and bioerosion (Glynn 1990, 1993). The capacity for coral reef recovery is still unknown for the studied site, but it is expected that after each disturbance event the cnidarian community would become progressively diminished (Glynn 1990). Moreover, it is reasonable to assume that continued high temperature events will favor the colonization of the reef by tolerant species with short periods of time between generations (Pitelka 1988; Bradshaw and Hardwick 1989). The implications of such potential changes are yet to be fully understood.
Acknowledgements This investigation was made possible by nancial support from CNPq-Brazil. Constructive criticism of the manuscript by Dr. Daphne Fautin (University of Kansas, USA) is gratefully acknowledged. Gratitude is extended to Dr. Jose Maria Landin Dominguez of the Laboratory of Coastal Studies, and to Dr. Marlene Campos Peso Aguiar of the Laboratory of Malacology and Benthic Ecology (both from Universidade Federal da Bahia, Brazil) for the technical facilities provided during the rst years of this research. Special gratitude is extended to Carlos Neves, Larissa de Siqueira, Rilza da Costa Tourinho Gomes, Simone Souza de Moraes, and Yonara Souza Braga for their encouragement of this research over the past few years, and for all their help and assistance during the eldwork.

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