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Estuarine, Coastal and Shelf Science 73 (2007) 243e248 www.elsevier.com/locate/ecss

Martin J. Attrill a,*, Francisco Kelmo a,b

a

Marine Biology and Ecology Research Centre, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, Devon PL4 8AA, UK b  Department of Human and Health Sciences, Universidade Salvador, Alameda das Espatodias, 915, Caminho das Arvores, Salvador, Bahia, Brazil, CEP 41820-460 Received 18 September 2006; accepted 8 January 2007 Available online 7 March 2007

Abstract

Keywords: coral reefs; Diadema; ENSO; Brazil; phase shift

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We present results from a seven year (1995e2001) study on the coral reefs in Bahia (Brazil), the reef invertebrate community being severely impacted by the 1997e98 El Ni~o Southern Oscillation event. Despite local extinction of some taxa, the urchin Diadema antillarum was the only n species out of a total of 678 enumerated demonstrating a signicant increase in population size following El Ni~o, indicating a unique response n of this species to the stresses associated with these events. Other species of echinoid did not show such a response, most disappearing from the fauna during the two post-El Ni~o years. The increasing Diadema numbers were most likely due to movement of individuals onto the reef sysn tems from deeper water, exploiting the conditions on the reefs caused by a reduction in competitors and, we speculate, an increase in available space on the reef allowing potential algal settlement to sustain this elevated urchin population. This increased grazing pressure may have prevented algae covering the reef, as seen in other Atlantic reef systems, allowing new coral settlement in 2001. 2007 Elsevier Ltd. All rights reserved.

1. Introduction

Large-scale phase shifts (Knowlton, 1992; Hughes, 1994) have been recorded in the coral reefs of the Western Atlantic, particularly the Caribbean (Hughes, 1994), where an ecosystem dominated by scleractinian corals has moved to an alternate state dominated by macroalgae. This latter community has been shown to persist potentially for at least a decade (Edmunds and Carpenter, 2001), with only one known example of a phase shift in the other direction (Edmunds and Carpenter, 2001). Phase shifts from coral to algal dominance can be triggered by a range of factors, both natural and anthropogenic (Lessios, 1988; Hughes, 1994; Lapointe, 1997), often in combination. In particular, large-scale bleaching can engender
* Corresponding author. E-mail address: m.attrill@plymouth.ac.uk (M.J. Attrill). 0272-7714/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2007.01.007

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a very rapid transition between coral and algal alternate states (Ostrander et al., 2000), although this response is inconsistent (Scully and Ostrander, 2001). A key organism in the transition between alternate states, and their subsequent persistence, is the herbivorous urchin Diadema antillarum. The species was effectively removed from many Caribbean reefs by an extensive disease in 1983 (Lessios, 1988), altering the balance between macroalgae and grazing pressure (Williams and Carpenter, 1988) and facilitating the establishment of a macroalgal-dominated community that prevented new coral settlement (Edmunds and Carpenter, 2001). Recent recovery of D. antillarum in Jamaica (and subsequently across the Caribbean) appears to have allowed, through grazing activity liberating reef space, the settlement of juvenile corals and thus initiate a shift back to a coral-dominated alternate state (Edmunds and Carpenter, 2001; Aronson and Precht, 2000, 2001;

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Opportunistic responses of Diadema antillarum (Echinodermata: Echinoidea) populations following the 1997e98 El Ni~o event in Bahia, Brazil n

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Carpenter and Edmunds, 2006). Modelling has also demonstrated that Diadema activity can impart great resilience to Caribbean reefs (Mumby et al., 2006). Here we report the results of a seven year (1995e2001) investigation into the faunal biodiversity of Bahian reefs (NE Brazil, Kelmo and Attrill, 2001; Kelmo et al., 2003; Attrill et al., 2004; Kelmo et al., 2004) which has documented changes to the community of corals and many associated groups of organism following the 1997e98 El Ni~o Southern n Oscillation event, the most severe on record according to McPhaden (1999), which occurred during the middle of the survey. We, therefore, had a unique opportunity to quantify El Ni~o impacts on a wide range of coral reef taxa, and, in parn ticular to investigate the response of Diadema antillarum to this major climatic perturbation that has resulted in catastrophic changes to other Atlantic reef systems where the urchin is less prevalent (Ostrander et al., 2000). 2. Materials and methods The studied reefs are 70 km from the city of Salvador (Ba hia, Brazil) and extend for 20 km between the beaches of Aba and Praia do Forte (see Fig. 1 of Kelmo et al., 2003). They are primarily rocky patch-reefs, with individual, generally small and spatially separated coral colonies growing on the substratum interspersed with other sessile organisms. They are located in the narrowest part of the Eastern Brazilian Continental Shelf (average width 15 km), the shelf edge being approximately 70 m deep (DHN, 1993). Two types of Holocene reef structures run parallel to the coastline in the study area: coastal emergent reefs (adjacent to the beaches), and shallow bank reefs (located a few kilometres off the coast). Coastal reef walls (CRW) and shallow bank reefs (SBR) were sampled at four locations, the dimensions of the sampled reefs varying from 500 m to 1800 m (long) and 400 to 500 m (wide). Water depth was between 10 m and 40 m. The coastal belt along the State of Bahia has a tropical humid climate; full details of meteorology and oceanography of the area are provided in Kelmo and Attrill (2001). Temporal analysis of changes in local environmental parameters (Kelmo et al., 2003) demonstrated that there were signicantly higher water temperatures, lower cloud cover and lower turbidity during the El Ni~o period (1998) than in other years, the latter two varin ables resulting in higher levels of UV radiation reaching the corals in 1998 than in non-ENSO years. From 1995 to 2000, data on the faunal community of the coastal and shallow bank reefs of Northern Bahia have been collected annually by SCUBA diving e the rst major study into the ecology of these reef systems. Quantitative samples were taken with 35 quadrats (1 m2) positioned randomly on each reef during each sampling occasion (Kelmo et al., 2003). In addition to 11 coral species (live colonies m2), the following groups have been quantied at the species level (live individuals or colonies m2): other cnidarians (40 species), sponges (62), ascidians (22), bryozoans (157), echinoderms (24), foraminiferans (284) and molluscs (78). The proportion of coral colonies demonstrating bleaching was

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3. Results

also recorded. Sites were revisited in 2001 and data for corals and echinoderms collected. Previous analysis has demonstrated no signicant effect of location on community data collected from within each habitat (Kelmo and Attrill, 2001), so for temporal comparisons a one-way ANOVA was used on pooled data for each reef to identify any signicant density or diversity variations within each habitat throughout the sampling period, differences between individual years following a signicant ANOVA being explored using post-hoc SNK tests. The survey was instigated to monitor the littleknown invertebrate biodiversity of the Bahian reefs, so algal cover was not directly measured and has been little studied (Costa et al., 2002). Generally, macroalgal cover is <40% in Bahian reefs (Costa et al., 2002) and is dominated by turf algae. In this study, it was possible to calculate the liberation of available space for potential algal (and other organism) colonisation due to all sessile faunal taxa being enumerated. Reduced space-occupation by corals and other invertebrates has been shown to be directly linked to increased algal cover (Williams and Polunin, 2001). We can, therefore, demonstrate trends in space liberation on the Bahian reefs, but we cannot directly assess changes in algal cover. The present analysis will, therefore, concentrate solely on the extensive faunal data from which changes to the reef ecosystem can be elucidated.

The 1997e98 ENSO event had an extensive impact on the coral reefs of Bahia in common with other reef systems around the globe (Linden, 1999; Aronson et al., 2000; Loya et al., 2001). Bleaching of coral species was signicantly higher in 1998 than pre-El Ni~o years for both studied n habitats, remaining comparatively high in subsequent years (ANOVA CRW: F6,21 29.79, p < 0.0001; SBR: F6,21 54.77, p < 0.0001; Fig. 1a). A further consequence was the signicant reduction in coral density in 1998 for both habitats (ANOVA CRW: F6,21 3.39, p 0.017; SBR: F6,21 61.39, p < 0.001; Fig. 1b), the decline continuing for two years after the El Ni~o event on the shallow bank n reefs (Fig. 1b). Analysis of other sessile taxa (bryozoans, sponges, ascidians, other cnidarians) revealed similar signicant decreases in their density in 1998 and the two subsequent years (ANOVA CRW: F5,18 25.05, p < 0.001; SBR: F5,18 14.09, p < 0.001; Fig. 1c), potentially increasing the availability of bare space on the reef system. In parallel with the sessile taxa, following El Ni~o there was a signin cant, and severe, decrease in overall echinoderm diversity (ANOVA CRW: F6,21 46.63, p < 0.001; SBR: F6,21 127.81, p < 0.001; Fig. 1d) and density (ANOVA CRW: F6,21 32.98, p < 0.001; SBR: F6,21 24.09, p < 0.001; Fig. 1e). This total density presented excludes Diadema, but includes other generally abundant echinoid species such as Echinometra lacunter, the only other echinoderm species still present on the CRW in 2000. However, Diadema antillarum abundances demonstrated a different trend from all other taxa, namely a signicant increase in

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density in the year following El Ni~o in both habitats n (ANOVA CRW: F6,21 20.05, p < 0.001; SBR: F6,21 45.57, p < 0.001; Fig. 1f). Densities of Diadema remained at a high level in successive years for the CRW habitat, but in the SBR returned to pre-El Ni~o densities n by 2000. Consequently, there was a signicant correlation between the proportion of bleached coral colonies and Diadema density for both habitats (Fig. 2). No juvenile coral settlement was recorded at any of the sites for three years following El Ni~o (1998e2000). Juvenile n colonies, particularly of the endemic Siderastrea stellata, were, however, apparent for the rst time in May 2001 (Fig. 3), reected in the increase in coral density recorded for this year (Fig. 1b). Similarly, there was a marked recovery in the diversity and density of the echinoderm fauna in 2001 (Fig. 1d,e) after a continued decrease in 1997e2000. Despite the dramatic impact on the Bahian reef fauna, there was, therefore, no evidence of a longer-term shift to a macroalgaldominated state as seen in parts of the Caribbean.

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Fig. 1. Results of faunal surveys from coastal reef walls and shallow bank reefs, Bahia. (a) %Bleaching of coral colonies, (b) total density of scleractinian coral colonies, (c) total density of all other sessile taxa, (d) total number of echinoderm species, (e) density of echinoderm species (excluding Diadema antillarum), (f) density of Diadema. A shallow bank reefs, , coastal reef walls (additional y-axis where necessary). For all variables, SNK tests demonstrated signicant differences (all p < 0.05) between 1998 and the three preceding non-El Ni~o years. n

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Fig. 2. Scattergrams displaying the relationship between Diadema density and proportion of coral colonies bleached. , coastal reef walls, r 0.701, p < 0.001; A shallow bank reefs, r 0.802, p < 0.001.

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4. Discussion Massive coral bleaching has been demonstrated to be a trigger for a rapid phase shift from coral- to algal-dominated states (Ostrander et al., 2000), bleaching resulting in a reduced coral abundance and thus liberated space for algal settlement (Ostrander et al., 2000; Lindahl et al., 2001; McClanahan et al., 2001). Once algal cover has been established beyond a certain point (Williams and Polunin, 2001), coral settlement is reduced (Aronson et al., 2002) and ultimately prevented (Edmunds and Carpenter, 2001), thus maintaining the algaldominated state (Hughes, 1996). In Bahia, the 1997e98 El Ni~o resulted in high and sustained levels of coral bleaching n and subsequent reduction in the abundance of corals, other sessile invertebrates and the majority of invertebrate grazing species over following years (Kelmo et al., 2003, 2004; Attrill et al., 2004). A large amount of free space was, therefore, liberated, providing the potential foundation for phase shifts witnessed in other parts of the Western Atlantic. New coral settlement (which does not occur when algal cover is complete (Edmunds and Carpenter, 2001)) was recorded for the rst time in 2001, three years after the El Ni~o, coupled with n a marked increase in coral abundance and echinoderm diversity that indicated the initiation of reef system recovery. Whilst

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Fig. 3. Juvenile Siderastrea stellata (a species endemic to Brazil) photographed in May 2001, the rst coral settlement since the 1997e98 ENSO. Scale bar 1 cm.

we have no quantitative data on algal cover, the extensive nature of our faunal data, therefore, gives us condence that patterns of faunal change and recovery are consistent with those observed in other systems (e.g. Carpenter and Edmunds, 2006) which have shown recovery from an algal-dominated state; these patterns would not have been observed if a phase shift had occurred on Bahian reefs. The question, therefore, arises as to the mechanism preventing a shift to an algal-dominated alternate state, as other potential factors were in place for Bahia reefs to follow the path of those in the Caribbean. In reefs unaffected by nutrication (Lapointe, 1997; Costa et al., 2000), the key factor controlling algal cover is grazing pressure, generally either by sea urchins and/or sh (Hay, 1984; Lewis, 1986; Morrison, 1988; Bythell et al., 2000), a clear inverse relationship between grazer abundance and algal cover being demonstrated in a number of studies (Williams and Polunin, 2001; McClanahan et al., 2001; Aronson et al., 2002). In Bahia, the majority of grazing invertebrate species (e.g. molluscs, most echinoids) demonstrated a severe decrease in density following El Ni~o. n To prevent algal dominance, grazing pressure had to have been maintained, or increased, to match algal settlement in liberated space. This increased level of grazing could be provided either by Diadema antillarum, the density of this urchin increasing signicantly coincident with El Ni~o, or by a sustained or eln evated population of grazing sh. Like the majority of marine taxa in NE Brazil, the sh assemblages have not been studied beyond large-scale biogeographical patterns (Floeter et al., 2001; Joyeux et al., 2001) and baseline assessment in certain localities (e.g. Rocha and Rosa, 2001), so this component of the Bahian reef system remains comparatively unknown. There is, however, a signicant shing community active in the area of the studied reefs (Costa et al., 2000), so there will be potential impact on the sh assemblage, though this is unlikely to be of a scale apparent in the Caribbean. The response of sh assemblages to 1997e98 El Ni~o in other parts n of the world has been equivocal, with signicant negative impacts apparent in Australia (Booth and Beretta, 2002) and Seychelles (Spalding and Jarvis, 2002), whilst an increase in grazing sh abundance was noted in Tanzania (Lindahl et al., 2001). Potentially, therefore, grazing sh in Bahia may have increased in abundance post-El Ni~o and contribn uted to preventing algal dominance, but we have no data (or reasons) to support this. In contrast, we do have evidence for a signicant increase in the density of the urchin, Diadema antillarum; an increase unique amongst the suite of nearly 700 species enumerated. This increase was coincident with increased temperatures during El Ni~o, rather than as a lagged response, so suggests n movements of adult urchins into the study area rather than increased post-El Ni~o recruitment; the majority of all urchins n enumerated were large adults. Such an explanation was invoked for Eucidaris thouarsii in the Galapagos (Glynn, 1988), which demonstrated marked increases post-El Ni~o, n the urchins moving onto dead coral frameworks at shallow depth. Before El Ni~o, Eucidaris was more abundant in offn reef and reef-edge areas (Glynn et al., 1979), so a similar

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The authors wish to thank CNPq, Brazil for supporting this research.

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scenario could be envisaged for Diadema in Bahia. Deeper reefs have not been studied, so potentially may represent a reservoir of Diadema that migrated into shallow reef areas to exploit the favourable post-El Ni~o conditions. n Diadema has been recognised as a keystone herbivore in Caribbean reefs (Lessios et al., 2001), its disappearance having been pivotal in inducing phase shifts in parts of the Western Atlantic (Lessios, 1988; Williams and Carpenter, 1988). The subsequent recovery of the urchin in parts of Discovery Bay, Jamaica (Edmunds and Carpenter, 2001) cleared patches within the algal cover enabling coral recruitment for the rst time in over a decade, highlighting the role of this species in maintaining the integrity of coral reef systems. This role has been claried across the whole Mediterranean as Diadema recovery has been clearly linked to subsequent coral recruitment (Carpenter and Edmunds, 2006). A post-El Ni~o increase in n urchin abundance has been noted in other studies (e.g. Glynn, 1988; Guzman and Cortes, 1992; Haley and Solandt, 2001; Aronson et al., 2002), with different inferred consequences for reef health that reect the contrasting roles Diadema can have within reef systems. The main concern of earlier studies, in particular, was the bioeroding impact of grazing urchins on the coral itself (Ogden, 1977; Sammarco, 1980) and thus population increases were viewed as a potential negative factor (Glynn, 1988; Mokady et al., 1996). However, it is now clear that urchin population increases also play a key role in preventing extensive macroalgal cover and maintaining coraldominated states (Aronson and Precht, 2000; Aronson et al., 2002). We, therefore, suggest that the increase in Diadema density observed in Bahia was in response to potential increased algal settlement on the quantied newly available bare substrata and, possibly with similar increases in grazing sh abundance, maintained grazing pressure at a high enough level to prevent complete algal cover of the Bahian reef system. This is evidenced by the rst subsequent post-El Ni~o n settlement of new coral juveniles in 2001, in parallel with the pattern observed in the Caribbean (Edmunds and Carpenter, 2001; Carpenter and Edmunds, 2006).

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