AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

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1 AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS Aquatic Conserv: Mar. Freshw. Ecosyst. (2007) Published online in Wiley InterScience ( Actual status of the sea urchin Diadema aff. antillarum populations and macroalgal cover in marine protected areas compared to a highly fished area (Canary Islands } eastern Atlantic Ocean) JOSE CARLOS HERNA NDEZ a,b, *, SABRINA CLEMENTE a, CARLOS SANGIL c and ALBERTO BRITO a a Departamento de Biologıá Animal (Ciencias Marinas), Facultad de Biologı a, Universidad de La Laguna, Tenerife, Islas Canarias b Department of Biology, Villanova University. Pennsylvania, USA c Departamento de Biologıá Vegetal (Botanica), Facultad de Farmacia, Universidad de La Laguna, Tenerife, Islas Canarias ABSTRACT 1. The aim was to determine the status of subtidal rocky benthic assemblages in three marine protected areas (MPAs) of the Canary Islands: (1) La Graciosa; (2) Mar de Las Calmas; (3) La Palma. Sea urchin (Diadema aff. antillarum) populations and non-crustose macroalgal cover were surveyed, and used as an indicator of conservation status in the three MPAs as well as in a highly fished area (HFA-Tenerife Island). 2. Comparing characteristics between each MPA and the HFA, and considering issues of management and design, it was concluded that the three MPAs each have a different conservation status. Mar de Las Calmas marine reserve was found to have the most desirable conservation status, followed by La Palma marine reserve based on sea urchin populations and non-crustose macroalgae assemblages. 3. Conversely, La Graciosa had the highest density of D. aff. antillarum and the lowest cover of non-crustose macroalgae out of the three MPAs. Values were comparable to those at the HFA, which shows La Graciosa to have the undesired conservation status. 4. Different spatial distribution patterns of non-crustose macroalgal as well as different algal composition cover were observed between the three MPAs and the HFA. These differences were principally attributed to the intensity of grazing activity of the key herbivore D. aff. antillarum. It is suggested that the different study areas correspond to different phase shifts that imply differing resilience of systems that should be taken into a count in future conservation strategies. Copyright # 2007 John Wiley & Sons, Ltd. Received 16 October 2006; Revised 25 July 2007; Accepted 17 August 2007 KEY WORDS: marine protected areas (MPAs); highly fished area (HFA); Diadema aff. antillarum; macroalgal assemblages; conservational status; spatial distribution patterns; Canary Islands *Correspondence to: J.C. Hernández, Department of Biology, Villanova University, Pennsylvania, USA. josecarlos.hernandez@villanova.edu Copyright # 2007 John Wiley & Sons, Ltd.

2 J.C. HERNA NDEZ ET AL. INTRODUCTION Herbivorous grazing activity is a factor determining marine community organization (Tegner and Dayton, 1981; Vadas, 1985; Sala et al., 1998; Guidetti et al., 2003). Several species of echinoids play a key role, even more important than other herbivores, as controllers of epibenthic communities (Lawrence, 1975; Lawrence and Sammarco, 1982; Verlaque and Néde lec, 1983; Verlaque, 1984; Carpenter, 1986; Fantzis et al., 1988; McClanahan and Shafir, 1990; Vadas and Elner, 1992; Sala, 1997). A number of factors, including size and motility, allow sea urchins to maintain intense grazing activity (Luckens, 1974; Dayton, 1975; Dayton et al., 1977). Feeding preferences vary between different species of echinoids, producing different effects on benthic communities (Vadas, 1977; Lubchenco, 1978; see also Lawrence and Sammarco s review, 1982). Echinoids can be found in very high density (Moore, 1966; Lawrence, 1975; Estes and Duggins, 1995; Shears and Babcock, 2002; Gagnon et al., 2004; Valentine and Johnson, 2005; Herna ndez, 2006; Guidetti and Dulcˇ ic, 2007) and can live for several years (Ebert, 1975). The main consequence of intense grazing activity is a shift from large areas of complex macroalgal beds to areas termed urchin barrens or barren grounds (Lawrence, 1975; Mann, 1982; Himmelman and Ne de lec, 1990; Vadas and Elner, 1992; Sala et al., 1998; Hereu, 2004), which are dominated by crustose coralline algae and some sessile invertebrates. The occurrence of such areas has been reported along temperate coastlines (Estes and Palmisiano, 1974; Mann, 1977; Scheibling and Stephenson, 1984; Miller, 1985; Duggins, 1989; McShane and Naylor, 1991; Vadas and Elner, 1992; Andrew, 1993; Sala et al., 1998; Guidetti et al., 2003) and subtropical coastlines (Aguilera et al., 1994; A lves et al., 2003; Brito et al., 2004; Tuya et al., 2004a), as well as in tropical regions (Ogden et al., 1973; Sammarco, 1982; Hay, 1984; John et al., 1992; McClanahan, 2000). In the Canary Islands, there are relatively small barren grounds generated by Paracentrotus lividus (Lamarck, 1816) in tide pools, and by Arbacia lixula (Linnaeus, 1758) around artificial jetties (JC Herna ndez pers. obs.). However, barren grounds generated by Diadema aff. antillarum are more extensive and commonly spread throughout the entire Archipelago (Aguilera et al., 1994; Brito et al., 2004; Tuya et al., 2004a) reaching to 50 m depth and covering about 89% of the total littoral rocky bottoms (e.g. Tenerife Island; Barquin et al., 2004). D. aff. antillarum densities present a negative correlation with water turbulence and a positive correlation with depth (Alves et al., 2001; Tuya et al., 2007), thus barren grounds are more common and severe in calm areas (Brito et al., 2004). In the eastern Atlantic, D. aff. antillarum is recognized as having a key ecological role in the development of barren (Alves et al., 2003) habitats. The species is also documented to be involved in the existence of stable alternate state systems (Knowlton, 2004; Tuya et al., 2005a) which damage the resilience of marine systems with the subsequent establishment of undesired conservation states (Knowlton, 2004; Hughes et al., 2005). The damaged resilience of undesired states may mean they display high resistance to system restoration (Steneck, 1998; Guidetti and Sala, 2007). Knowledge of alternate states and the functioning of the phase shifts may have implications for future management strategies focused on mediating transitions between these states. Many factors are involved in the expansion of sea urchin populations, such as overfishing of the urchins natural predators (Sala and Zabala, 1996; Sala et al., 1998; McClanahan, 2000; Pinnegar et al., 2000; Sala, 2004; Tuya et al., 2004a; Guidetti et al., 2005) and other natural factors such as recruitment, topography, substrate composition and some particular oceanic events can also play an important role in expansion of the sea urchin populations (Sala et al., 1998; Pinnegar et al., 2000; Hereu, 2004). Owing to the control of fishing effort within marine protected areas (MPAs), these areas could be capable of influencing sea urchin abundance naturally, as they facilitate development of predators and indirectly aid the regeneration of benthic communities (Sala et al., 1998; Babcock et al., 1999; McClanahan et al., 1999; McClanahan, 2000; Shears and Babcock, 2002; Tuya et al., 2004a; Guidetti, 2006). In this sense, measuring community changes at no-take MPAs relative to adjacent fished areas is a valuable experimental procedure for assessing the effects of fishing where baseline data are not available (Sala et al., 1998). Moreover, at this particular latitude, macroalgae are the main biological engineers; high macroalgal cover is a well-known indicator of good benthic conservation status in the absence of coral reef formations (Tuya et al., 2005a). The aim of this study was to evaluate conservation status of rocky macrobenthic communities within MPAs of the Canary Islands, with comparison to a highly fished area (HFA). In order to do so, the study incorporated surveys of macroalgal cover combined with investigation of the key herbivore D. aff. antillarum (population density, biomass and test diameter). The main objectives were to: (1) compare the conservation status of the three MPAs of the Canary Islands and a HFA (Tenerife Island), assessed on the basis of sea urchin populations, algal assemblages and the occurrence of barren grounds as an effect of undesired conservation state ; (2) determine the status of D. aff. antillarum populations and non-crustose macroalgal assemblages at each MPA and the HFA, and ascertain their spatial distribution patterns (variation among sites and depths); (3) assess the influence of sea urchin biomass on non-crustose macroalgal cover and its effect on algal assemblage composition throughout the MPAs and the HFA.

3 DIADEMA. AFF. ANTILLARUM AND MACROALGAL COVER IN CANARY ISLANDS MPAS METHODS Study areas This study was carried out at sites located within the three MPAs of the Canary Islands: Isla Graciosa e Islotes del Norte de Lanzarote; Punta de La Restinga-Mar de Las Calmas; and Isla de La Palma; and one HFA: Tenerife Island (Figure 1). Throughout this study locations are referred to as La Graciosa, Mar de Las Calmas, La Palma and Tenerife, respectively. The Canary Islands are situated on the eastern border of the subtropical gyre of the North Atlantic Ocean at a latitude of about 288N. The archipelago extends about 400 km west, and the eastern boundary of the archipelago is separated from the coast of the African mainland by a distance of 90 km. Their geographical location between the cool, nutrient-rich water from the north-west African coastal upwelling, and the warmer, nutrient-poor open ocean waters, means the Canary Islands are considered a Coastal Transition Zone (Barton et al., 1998). In addition, the archipelago itself acts as an obstacle to the Canary Current, which flows NNE to SSW through the archipelago, and to the Trade Winds, thus giving rise to a variety of mesoscale phenomena that have strong implications for the productivity of the region (Molina and Laatzen, 1986; Barton, 1994; Aristegui et al., 1997). This particular geographical situation creates an oceanographic gradient where differences in sea water temperature ( 28C), nutrients and primary productivity are found between the eastern and western boundaries of the Archipelago (Barton et al., 1998; Davenport et al., 2002). La Graciosa, established in 1995, is located on the eastern part of the Archipelago (Figure 1), covering an area of ha and extending throughout territorial waters linked to Figure 1. Locality of the studied sites at the three MPAs of the Canary Islands and the HFA Tenerife Island. Numbers correspond to the different sites listed in Table 1.

4 J.C. HERNA NDEZ ET AL. State General Administration and littoral waters managed by the Autonomous Community Government of the Canary Islands. This MPA comprises one circular no-take area, which surrounds the Roque del Este islet with a 1 mile radius; outside of this is a buffer area stretching a further 2 miles around the no-take area; and beyond which, outside of the other two zones, is one large restricted fishing area (Figure 1). In the notake area all fishing, harvesting and scuba diving activities are forbidden and only scientific activities are allowed. In the buffer area, commercial anchoring and traditional fishing methods targeting Sarpa salpa and migratory pelagic species are also allowed. In the restricted fishing area controlled scuba diving and certain recreational fishing line activities are authorized over 500 m from the shore. Mar de Las Calmas, established in 1996, is located on El Hierro Island on the south-western part of the Archipelago (Figure 1). The MPA has an area of 775 ha, extending across both territorial and littoral waters, and encompassing one notake area; two buffer areas (one either side of the no-take area); with a restricted fishing area adjacent to each buffer area (Figure 1). In the no-take area all fishing, harvesting and scuba diving activities are forbidden apart from tunid fishing and scientific activities. In the buffer areas commercial line fishing and controlled scuba diving are also allowed. Traditional fishing by local fishermen is authorized in the restricted fishing areas. La Palma, established in 2001, is located on La Palma Island in the north-western part of the Archipelago (Figure 1) covering 3719 ha of territorial waters. This MPA comprises one central no-take area and a restricted fishing area surrounding it (Figure 1). In the no-take area all fishing, harvesting and scuba diving activities are forbidden and only scientific activities are allowed. In the restricted fishing area commercial line fishing, tunid fishing and capture of small pelagic species as fishing bait are allowed, as well as controlled scuba diving activities. All kinds of commercial and recreational fishing occurs outside the MPAs. Therefore Tenerife Island (Figure 1), which is also a highly populated island (Aguilera et al., 1994; Fernández-Palacios et al., 2004) can be considered a HFA. Sampling was carried out at La Graciosa from September to October in 2001 at six sites: Roque del Este; Punta La Mareta; Cuevas Coloradas; Montan a Amarilla; Caleta del Sebo; and Punta Fariones (Table 1, Figure 1). At Mar de Las Calmas sampling was performed during October 2001 at eight sites: Tecoro n; Cueva del Diablo; Punta Las Lapillas; Punta Las Can as; Roque Chico; Cueva de Los Frailes; Punta Las Frailes; and La Herradura (Table 1, Figure 1). At La Palma, the study was conducted during December 2004 at six localities: Punta Bogullos; Punta El Remo; Punta Banco; Siete Islas; La Resbaladera; and Punta Larga (Table 1, Figure 1). At Tenerife sampling was carried out during 2004 at six sites: Teno; Palm-Mar; La Jaca; Abades; Poris de Abona; and Boca Cangrejo (Table 1, Figure 1). Sea urchin populations and non-crustose macroalgal cover At each locality the belt transect method was used to count all D. aff. antillarum individuals thus providing estimates of sea urchin population densities. In the Mediterranean Sea, this simple technique has been successfully carried out to estimate population density of the sea urchins Arbacia lixula and Paracentrotus lividus (Harmelin et al., 1980; Turo n et al., 1995; Sala and Zabala, 1996). However, in the present study certain modifications have made this technique more suitable for the benthic communities investigated. Shorter transects of 10 2 m were used, allowing for more replicates. Transects were run parallel to the coastline using a metric tape at two different depth bands (band 1: from 0 to 10 m; and band 2: from 10 to 20 m.). At least 10 replicates were carried out at each site. The percentage of non-crustose macroalgal cover was also estimated at each transect, as well as percentage cover of barren ground, represented by surfaces covered with crustose macroalgae and bare rock (modified from Guidetti, 2006). A representative sample of sea urchins was measured at every site to estimate mean test diameter. The total number of individuals to be measured was calculated following Kingsford (1998) sampling effort indications. Sea urchin biomass was defined as sea urchin dry weight (g) per area (m 2 ). Urchin dry weights were obtained using the following regression model [UDW ¼ 0: ðtd 2:57867 Þ]; where: UDW¼ sea urchin dry weight in grams and TD ¼ individual test diameter in millimetres. The regression model was obtained using dry weight data of 2760 urchins (D. aff. antillarum) of all size classes collected from different habitats in a previous study throughout the Canary Islands (Herna ndez, 2006). Therefore sea urchin biomass was able to be calculated at every site and depth by way of multiplying population density by sea urchin dry weight. Community-level patterns of macroalgal assemblages Composition of the algal assemblage was evaluated by analysing 18 images (sampling area m 2 ) taken from each site within the MPAs and HFA (see Table 1, Figure 1). Quadrats were placed randomly at each site and images were taken using an underwater digital camera. In total, 468 images were downloaded to a computer and images were analysed for estimations of algal cover. In situ identification was also completed and unknown algae were collected and identified in the laboratory using Afonso and Sanso n (1999). For the statistical analysis, five morpho-functional algal groups were considered (Guidetti, 2006): (a) algal turf with 18 identified species; (b) unbranched-erect macroalgae with four identified species; (c) branched-erect macroalgae with 21

5 DIADEMA. AFF. ANTILLARUM AND MACROALGAL COVER IN CANARY ISLANDS MPAS Table 1. Descriptive statistics of density (no. indiv. m 2 ), test diameter (mm) and biomass (g urchin m 2 )ofdiadema aff. antillarum and of noncrustose macroalgae cover (%) at the surveyed sites in the MPAs and the HFA Studied areas and sites Diadema aff. antillarum Non-crustose macroalgae cover Density Test diameter Biomass 1. La Graciosa MPA N Mean SD N Mean SD Mean SD N Mean SD 1. Roque del Este Pta. La Mareta Cuevas Coloradas Montaña Amarilla Caleta del Sebo Pta. Fariones Total Mar de Las Calmas MPA 7. Tecorón Cueva del Diablo Pta. Las Lapillas Pta. Las Cañas Roque Chico Cueva Los Frailes Pta. Los Frailes La Herradura Total La Palma MPA 15. Pta. Bogullos Pta. El Remo Pta. Banco Siete Islas La Resbaladera Pta. Larga Total Tenerife HFA 21. Teno Palm-mar La Jaca Abades Poris de Abona Boca Cangrejo Total identified species; (d) calcified-erect macroalgae with three identified species; and (e) crustose macroalgae with four identified species (Table 2). These groupings facilitate the ecological interpretation of algal assemblages influenced by D. aff. antillarum. It is necessary to point out that reference to the crustose group means uncovered crustose algae (M. Sanso n and J. Afonso, pers. commun.). Data analysis In order to contrast sea urchin density, test diameter and biomass, as well as percentage cover of non-crustose macroalgae among areas, sites and depth levels, distancebased permutational ANOVAs (Anderson, 2001) were performed rather than a traditional univariate ANOVA. In these analyses the F-statistics are calculated but P-values are obtained by permutation, thus avoiding any assumption about the nature of the distribution of the original variables (Anderson, 2001; Anderson and ter Braak, 2003). A threeway design was performed when analysing urchin density and biomass and non-crustose macroalgal cover, in which Area was treated as a fixed factor with four levels (3 MPAs: La Graciosa, Mar Calmas, La Palma and 1 HFA: Tenerife), Depth as a fixed factor with two levels (1: 0 10 m and 2: m), and Site as a random factor nested within Area. A twoway design was performed when analysing urchin test diameters, in which Area was treated as a fixed factor and Site as a random factor nested within area. All analyses were

6 J.C. HERNA NDEZ ET AL. Table 2. List of surveyed algae species categorized as non-crustose (turf; unbranched erect; branched erect and calcified erect) and crustose macroalgae at the sampling sites, MPAs (La Graciosa, Mar de Las Calmas, La Palma) and HFA (Tenerife Island) Non-crustose macroalgae Turf Unbranched erect Branched erect Calcified erect Amphiroa spp. Colpomenia sinuosa Asparagopsis taxiformis Corallina elongata Asparagopsis taxiformis (tetrasporofite) Hydroclathrus clathratus Cystoseira abies-marina Liagora ceranoides Ceramium echionotum Lobophora variegata Cystoseira compressa Liagora tetrasporifera Cottoniella filamentosa Padina pavonica Cystoseira foeniculacea Cianophytes (unidentified) Cystoseira sp. Caulerpa webbiana Dasya baillouviana Filaments (unidentified) Dictyota cervicornis Gelidiopsis intricata Dictyota crenulata Herposiphonia secunda Dictyota dichotoma Jania adhaerens Dictyota fasciola Jania pumila Dictyota pfaffii Lophocladia trichoclados Dictyota sp1. Polysiphonia furcellata Dictyota sp2. Psedochlorodesmis furcellata Galaxaura rugosa Pseodotetraspora marina Hypnea spinella Sphacelaria cirrosa Laurencia spp. Spyridia hypnoides Pterosiphonia pennata Wrangelia penicillata Sargassum desfontainesii Sargassum sp. Stypocaulon scoparium Stypopodium zonale Crustose macroalgae Crutose coralline algae (unidentified) Lithothamnium coralloides Mesophyllum canariense Pseudolithoderma adriaticum based on Euclidean distances in the original raw data, with all P-values obtained using 4999 permutations of the appropriate exchangeable units (Anderson and ter Braak, 2003). Significant terms in the full model were examined individually using appropriate a posteriori pairwise comparisons. The computer program PRIMER 6 & PERMANOVAþ ( was used to perform all theses procedures. Several relationships among studied variables were assessed: the log-linear relationship between sea urchin biomass (g m 2 ) and non-crustose macroalgal cover (%); the exponential relationship between sea urchin abundance (number of individuals m 2 ) and macroalgal species richness (number of species); and the linear relationships between urchin abundance and test diameter (mm), and between macroalgal species richness and urchin test diameter. All regression models were performed using SPSS-14 statistical package. Whole macroalgal assemblages were analysed using a distance-based permutational multivariate analysis of variance (PERMANOVA; Anderson, 2001), with Area treated as a fixed factor and Site as a random factor nested within Area. Sources of variation were tested using 4999 random permutations of the data. Significant terms in the full model were examined individually using appropriate a posteriori pairwise comparisons. Relative dissimilarities among algal assemblages observed in different areas were visualized using principal coordinate analysis (PCO; Gower, 1966), also known as metric multi-dimensional scaling (mmds). All multivariate methods were based on Bray Curtis dissimilarities calculated among square root transformed data. RESULTS Spatial variation of sea urchin populations and noncrustose macroalgae in MPAs and HFA: influence of sea urchins on non-crustose macroalgal cover and macroalgal composition Permutational ANOVA results revealed a highly significant effect of the factor Area (Table 3). A posteriori pairwise analyses showed that the HFA, where maximum sea urchin densities were recorded (Table 1, Figure 2), differs significantly between La Graciosa, Mar de Las Calmas and La Palma

7 DIADEMA. AFF. ANTILLARUM AND MACROALGAL COVER IN CANARY ISLANDS MPAS Table 3. Results of permutational ANOVA designs comparing density (n8 indiv. m 2 ), test diameter (mm) and biomass (g m 2 )ofdiadema aff. antillarum and non-crustose macroalgae cover (%) between the surveyed depth levels ((1) 0 10 m and (2) m) and sites in four areas of the Canarian Archipelago (1. La Graciosa MPA; 2. Mar de las Calmas MPA; 3. La Palma MPA; 4. Tenerife HFA) Source of variation df SS MS Pseudo-F P (perm) Density Test diameter Biomass Non-crustose macroalgae cover Area Depth Site (Area) Area Depth Depth Site (Area) Residual Total Area Site (Area) Residual Total Area Depth Site (Area) Area Depth Depth Site (Area) Residual Total Area Depth Site (Area) Area Depth Depth Site (Area) Residual Total Figure 2. Comparison of mean standard deviation of density, test diameter and biomass of Diadema aff. antillarum and non-crustose macroalgal cover among sites and depth levels in the MPAs and in the HFA. (white bars ¼ depth level 1 (0 10 m) and shaded bars ¼ depth level 2 (10 20 m)).

8 J.C. HERNA NDEZ ET AL. Non-crustose macroalgal cover (%) F= p< y = Ln(x) R 2 = N = (A) Sea urchin biomass (gr. m - ² ) Macroalgae richness (no sp) (B) Abundance Diadema aff. antillarum m - ² F= p<0.01 y = 10.42e x R 2 = N=26 Figure 3. (A) Log-linear relationship between sea urchin biomass and non-crustose macroalgal cover. (B) Exponential relationship between sea urchin abundance and macroalgae richness. (Black circles ¼ MPAs; white circles ¼ HFA:) 15 MPAs (t ¼ 3:19; P50.01; t ¼ 5:46; P50.01; t ¼ 3:67; P50.01, respectively). When comparing La Graciosa and La Palma (t ¼ 0:91; P ¼ 0:384), both with intermediate urchin densities (Table 1, Figure 2), significant differences were not obtained. Finally, Mar de Las Calmas, found to have the lowest urchin densities of all (Table 1, Figure 2), was significantly different from the other MPAs (t ¼ 3:99; P50.01 and t ¼ 4:30; P50.01, respectively). Also significant interaction of factors Depth Site (Area) was obtained (Table 3), meaning that the density of D. aff. antillarum differs at the scale of sites in relation to the depth band considered (Figure 2). Test diameter is very different between areas (Table 3). A posteriori pairwise analyses showed that the HFA, where the smallest sea urchins were recorded (Table 1, Figure 2), differs from La Graciosa, Mar de Las Calmas and La Palma MPAs (t ¼ 4:75; P50.01; t ¼ 2:40; P50.05; t ¼ 2:24; P50.05, respectively). In La Graciosa, where the largest individuals were found (Table 1, Figure 2), test diameters were significantly different from test diameters in Mar de Las Calmas and La Palma (t ¼ 2:34; P50.05; t ¼ 2:10; P50.05, respectively). No difference in test diameter was found between Mar de Las Calmas and La Palma (t ¼ 0:05; P ¼ 0:955), which both contained medium sized sea urchins (Table 1, Figure 2). Also Site (Area) shows significant differences (Table 3, Figure 2). When comparing sea urchin biomass, there were once again highly significant differences between areas (Table 3). A posteriori pairwise analyses showed that in the area with the greatest sea urchin biomass, the HFA (Table 1; Figure 2) biomass differed significantly from both La Palma and Mar de Las Calmas MPAs (t ¼ 4:77; P50.01; t ¼ 8:29; P50.01, respectively) but not significantly from La Graciosa (t ¼ 1:75; P ¼ 0:099). Differences obtained between La Graciosa and La Palma, where intermediate urchin biomasses were recorded (Table 1, Figure 2), were also not significant (t ¼ 2:05; P ¼ 0:078). Finally, Mar de Las Calmas with the lowest recorded urchin biomass scores (Table 1; Figure 2), was found to be significantly different to the other MPAs (t ¼ 4:64; P50.01 and t ¼ 4:89; P50.01, respectively). Also the interaction of factors Depth Site (Area) was significant (Table 3), denoting that sea urchin biomass differs at the scale of site in relation to the depth band considered (Figure 2).

9 DIADEMA. AFF. ANTILLARUM AND MACROALGAL COVER IN CANARY ISLANDS MPAS Non-crustose macroalgal cover data showed significant interaction of the main factors Area Depth (Table 3), meaning that algal cover differs in a different manner between areas depending on depth band (Figure 2). A highly significant log-linear relationship was detected between sea urchin biomass and non-crustose macroalgal cover (Figure 3A). The scatter plot of sea urchin biomass versus non-crustose macroalgal cover showed more variability in percentage of algal cover at the lowest levels of urchin biomass. At intermediate levels of biomass this variability starts to decrease and at a threshold biomass of about 50 g urchin m 2 non-crustose macroalgal cover remains below 30%. However, an urchin biomass of less than 10 g m 2 assures a percentage macroalgal cover which is always above 35% (Figure 3A). The linear relationship between D. aff. antillarum abundance and macroalgal species richness was found to be significant, with a general trend to decreasing variability in macroalgal richness with increasing urchin abundance (Figure 3B). Moreover, a higher variability in macroalgal richness at MPAs, always related to low medium urchin abundances (54 individuals m 2 ), rather than at the HFA, where it can easily be detected from the scatter plot (Figure 3B). Community-level patterns of macroalgal assemblages in MPAs and HFA In total, 50 algal taxa were recorded in the 468 quadrats sampled at the 26 sites studied. In Tenerife 12 algal species were present; 27 in La Graciosa; 29 in Mar de Las Calmas; and 20 in La Palma. Algal assemblages varied greatly between areas (Table 4). A posteriori pairwise analysis showed that the HFA differs from both Mar de Las Calmas and La Palma MPAs (t ¼ 10:22; P50.01; t ¼ 3:92; P50.01, respectively) but not from La Graciosa (t ¼ 1:08; P ¼ 0:322) (Figure 4). There were additional differences between the three MPAs in terms of algal assemblages (La Graciosa versus Mar de Las Calmas t ¼ 6:75; P50.01; La Graciosa versus La Palma t ¼ 3:31; P50.01 and Mar de Las Calmas versus La Palma t ¼ 3:13; P50.01) (Figure 4). Differences were found to be significant at the scale of Site (Area) (Table 4). The unconstrained PCO plot also suggested distinction between algal assemblage structure in different areas (Figure 5). PCO1 (73% of total variation) split Mar de Las Calmas and La Palma (with higher percentage cover of unbranched erect algae) from La Graciosa and higher crustose macroalgal cover, and from the HFA. Assemblages inside the HFA (closed triangles) and La Graciosa (light grey circles) occurred generally in the lower left half of the plot, while assemblages from Mar Calmas and La Palma occurred generally in the right half of the plot (Figure 5). However, in the left part of the diagram, La Graciosa and HFA surveys are quite well mixed Table 4. Results of PERMANOVA on the basis of the Bray Curtis dissimilarity for square root transformed morphofunctional algal groups cover data, comparing macroalgal assemblages between the surveyed sites in four areas of the Canarian Archipelago (1. La Graciosa MPA; 2. Mar de las Calmas MPA; 3. La Palma MPA; 4. Tenerife HFA) Source of variation df SS MS Pseudo-F P (perm) Area Site (Area) Residual Total showing that these two types of assemblage did not separate clearly in two dimensions on the unconstrained plot (Figure 5). PCO2 (18.1% of total variation) split sites inside MPAs with higher cover of branched erect, calcified erect and turf algae than sites with lesser cover of those algal groups (Figure 5). In addition, the variation among La Palma sites was just as large as any observed differences between communities from MPAs and the HFA (i.e. assemblages from MPAs tended to be just as far away from each other as assemblages from HFA) (Figure 5). Relationship between sea urchin density and test diameter, influence of macroalgal richness A significant linear relationship was found between sea urchin abundance and test diameter (Figure 6A), meaning that D. aff. antillatum test diameter is negatively density dependent. Although the slope value was low, higher variability in test diameter was found at low urchin densities found at MPAs (Figure 6A). The linear relationship between macroalgal species richness and D. aff. antillarum test diameter was found to be positive and highly significant (Figure 6B). The scatter plot showed little variability of urchin size and macroalgal richness within the HFA, where urchins did not exceed 46 mm in size and a maximum of nine species of macroalgae was recorded. However, greater variability of both parameters was found at the MPAs (Figure 6B). DISCUSSION The simultaneous study of macroalgal cover and sea urchin populations is useful in evaluating conservational status of macrobenthic communities (McClanahan and Shafir, 1990; McClanahan, 2000; Piazzi et al., 2002; Shears and Babcock, 2002). In the Canary Islands macroalgal cover is a well-known indicator of benthic conservation status (Tuya et al., 2005a); an area with low density and biomass of D. aff. antillarum and a high cover of non-crustose macroalgae can potentially be considered a less disturbed system, controlled by top down

10 J.C. HERNA NDEZ ET AL. Macroalgal cover (%) Non-crustose macroalgae Turf Unbranched erect Branched erect Calcified erect Crustose macroalgae 0 La Graciosa Mar de Las Calmas La Palma Tenerife Marine Protected Areas Highly Fished Area Figure 4. Percentage cover (mean SD) of macroalgae morphofuctional groups (non-crustose and crustose macroalgae) in algae assemblages at MPAs (La Graciosa, Mar de Las Calmas and La Palma) and HFA (Tenerife Island). 100 Branched erect Turf MPAs HFA La Graciosa Mar de Las Calmas La Palma Tenerife PCO2 (18.1% of total variation) 50 0 Crustose macroalgae Calcified erect Unbranched erect PCO1 (73.4% of total variation) Figure 5. Ordination plot of the first two PCO axes (explaining 91.49% of the original variability) based on Bray Curtis dissimilarities of square root transformed morphofunctional algal groups, showing algal assemblage at different areas and sites. forces. Conversely, high urchin biomass or density and consequently low non-crustose macroalgal cover can be related to a system degraded by overfishing, which restricts predation upon urchins (Aguilera et al., 1994; Brito et al., 2004; Tuya et al., 2004a, b, 2005b; Herna ndez, 2006; Clemente et al., in press) (Figure 7). According to Tuya et al. (2004a), D. aff. antillarum is a key herbivore that controls non-crustose macroalgal cover in the Canary Islands. Therefore the studied MPAs and HFA can be considered within a successional trajectory of marine ecosystem degradation which is principally controlled by this species of sea urchin. At medium urchin biomasses (50 g urchin m 2 ) non-crustose macroalgal assemblages are drastically reduced and cover remains around 30% or less. However, low urchin biomass below 10 g urchin m 2 assures noncrustose macroalgal cover above 35%. In this case, higher

11 DIADEMA. AFF. ANTILLARUM AND MACROALGAL COVER IN CANARY ISLANDS MPAS Test diameter (mm) F = p<0.01 y = x R 2 = N = (A) 5 10 Abundance Diadema aff. antillarum m - ² Test diameter (mm) (B) F = p<0.001 y = x R 2 = N = Macroalgae richness (n sp) Figure 6. (A) Linear relationship between sea urchin density and test diameter. (B) Linear relationship between macroalgal richness and sea urchin test diameter. (Black circles ¼ MPAs; white circles ¼ HFA:) variability of non-crustose macroalgal cover was found, which means that a set of environmental factors ( bottom up resources, wave exposure, substrate availability, habitat complexity, etc.) come into play, driving macroalgal assemblage composition. In addition, no relationship was found between urchin abundance and macroalgal richness, maybe due to the importance of other factors mentioned by Tuya and Haroun (2006). These authors highlight the important role of bottom-up resources in explaining the algal composition gradient found in the Canarian Archipelago, although low replication and high variability of results within islands may be obscuring the hypothesized regional pattern. The magnitude of urchin control over macroalgal cover in the studied areas may be masking any clear macroalgal pattern due to other environmental factors. Alternatively, when top down control on urchin populations is low or non-existent, as in urchin barrens of the Canary Islands (Clemente et al., in press), bottom up forces seem to be reflected by the herbivores by way of increased variability of the urchin population (Sala and Zabala, 1996; Hereu et al., 2004; Herna ndez, 2006; Guidetti and Sala, 2007). Important differences in the spatial distribution patterns of sea urchin populations as well as in extension of barren grounds and consequently in non-crustose macroalgal cover at the MPAs and HFA are reported here. Tenerife shows, as expected owing to its overfished condition, the worst conservation status of all studied areas. The status of Tenerife can be considered the undesired state in which, despite some site variation, urchin biomass is always over 40 g urchin m 2. Barren ground covered 96% of the surveyed area, in concordance with the occurrence of urchin dominated habitat shown by Barquin et al. (2004), who describe rocky bottoms of Tenerife as being in a critical situation. At La Graciosa, the conservation status was found to be poor, unexpected for a MPA with 12 years of fishing restriction measures, which should be increasing fish populations that includes urchin predators. Similar to other non-protected areas (e.g. Tenerife) of the Canary Islands (Herna ndez, 2006), La Graciosa was shown to have a considerable amount of barren ground (83% cover). At La Palma, mid-values of urchin biomass and percentage cover of non-crustose macroalgae were obtained. Barren grounds at La Palma occupy about 52% of total substrate, a much lower value, which is probably a consequence of denser fish predator populations as a result of the implementation of fishing restrictions throughout the MPA, which has led to improved control over sea urchin abundance. At Mar de Las Calmas sea urchin densities and biomasses were very low, similar to the status reported in periods previous to the implementation of the MPA (Brito et al.,

12 J.C. HERNA NDEZ ET AL. Mar de Las Calmas MPA HIGH CONSERVATION Lowest urchin desities (0.11 ± 0.11 indv. m -2 ) Medium urchin size (46.12 ± mm) Lowest urchin biomass (2.41 ± 2.62 gr. urchin m -2 ) Highest non-crustose macroalgae cover (85.67 ± %) Lowest ocurrence of barren grounds (13.25 ± %) La Palma MPA Medium urchin desities (1.64 ± 1.50 indv. m -2 ) Medium urchin size (47.51 ± mm) Medium urchin biomass (26.81 ± gr. urchin m -2 ) Medium non-crustose macroalgae cover (47.25 ± %) Medium ocurrence of barren grounds (52.75 ± %) Non-crustose macroalgae La Graciosa MPA Turf Umbranched erect Branched erect Medium urchin desities (2.15 ± 1.51 indv. m -2 ) Highest urchin size (55.70 ± mm) High urchin biomass (56.53 ± gr. urchin m -2 ) Low non-crustose macroalgae cover (16.81 ± %) High ocurrence of barren grounds (83.19 ± %) Tenerife HFA Highest urchin desities (7.38 ± 3.75 indv. m -2 ) Lowest urchin size (36.26 ± 8.58 mm) High urchin biomass (81.63 ± gr. urchin m -2 ) Lowest non-crustose macroalgae cover (3.98 ± 5.24 %) Highest ocurrence of barren grounds (96.02 ± 5.24 %) Calcified erect Barren grounds LOW CONSERVATION UNDESIRED STATE Diadema aff. antillarum Figure 7. Diagram illustrating the actual conservation status of the three MPAs of the Canary Islands compared to a HFA (Tenerife Island), regarding urchin densities, biomass and test diameter; non-crustose macroalgal structure and occurrence of barren grounds (percentage of bare rock surface and percentage of rock covered by crustose macroalgae). 1998), with high non-crustose macroalgal cover and very low percentages of barren grounds cover (13%). Barren grounds can also be formed as the result of the simultaneous foraging activity of several abundant algae feeders, such as Sparisoma cretense, Pseudocaranx dentex and Diplodus cervinus (Bortone et al., 1991; Falcon et al., 1996; Tuya et al., 2004a, 2006) other than D. aff. antillarum. These results suggest a constant conservation status throughout this MPA in terms of the effects of urchin grazing activity over ecosystem complexity, denoting a well structured and stable system that can be considered an example of the desired state. In general, medium high urchin biomass appears to control algal composition and structure. In this sense, turf and unbranched erect algae are the non-crustose macroalgal groups found along with urchins of this density, as seen in the HFA and La Graciosa, despite the clear dominance of crustose macroalgae in structuring rocky reefs. This macroalgal structure and composition is typical for degraded urchin barrens, also found in other parts of the world (Estes and Duggins, 1995; Shears and Babcock, 2003; Guidetti and Sala, 2007). Where urchins are scarce or absent, as in Mar de Las Calmas and most sites of La Palma, unbranched erect algae are the dominant group that structure algal assemblages on rocky bottoms, in which Lobophora variegata is the most abundant species. This group dominance could be due to the lower grazing pressure, which enables algae to flourish, as well as to the species efficiency in avoiding urchin grazing as a result of its lower palatability to urchins (Bouderesque and Verlaque, 2001). Similar patterns have been observed in Mediterranean (Guidetti, 2006) and in New Zealand (Shears and Babcock, 2002) rocky reefs. Cover of crustose, turf and branched erect algae are more restricted, appearing occasionally in patches and coupled to the low percentage of barren grounds. High variability of algal structure was found at medium urchin densities (as in La Palma, where only the calcified erect algal group was recorded), as a consequence of intermediate grazing pressure, which enhances algal complexity (Sammarco, 1982). This algal structure gradient is consistent with the general pattern described by Guidetti (2006) between protected and unprotected locations in the Mediterranean Sea. However, several differences were found with the pattern proposed by Tuya and Haroun (2006), where fucoid species (comprising the branched erect group) should increase in the eastern islands compared to the western ones, while turf and bush-like algae,

13 DIADEMA. AFF. ANTILLARUM AND MACROALGAL COVER IN CANARY ISLANDS MPAS principally Lobophora variegata (comprising turf, unbranched erect and calcified erect groups) should increase in the western islands. In this study the non-crustose unbranched erect group always presented the highest cover, independent of location (eastern or western), although it is possible that inconsistencies in methodology (selected depth range and sampling effort) could explain these differences. Different patterns of variation of urchin populations and macroalgae with depth have been reported at the studied areas. Areas with a higher percentage of rocky substrate covered by barren grounds, such as Tenerife and La Graciosa, show higher urchin biomasses at the shallower band. On the other hand, in areas with medium or low barren ground cover, urchin biomass is higher at the deeper level, as reported at La Palma, where a decrease of non-crustose macroalgal cover and an increase in sea urchin abundance was observed with depth. This pattern could be explained as a migratory strategy of urchins that tend to accumulate forming fronts just below algal stands, as has been observed in Strongylocentrotus droebachiensis (Lauzon-Guay et al., 2006; Lauzon-Guay and Scheibling, 2007). Therefore, in Tenerife and La Graciosa, where high barren cover occurs, algal beds subsist only at the shallower level and urchin biomass is accumulated in this band where more food is available. However, Mar de Las Calmas showed homogenous status throughout all the bathymetric levels studied. To help understand the interactions between fishing pressure, predators, urchins and benthic macroalgae, the test diameter of sea urchins can be measured (Levitan, 1992). There is a negative relationship between urchin test diameter and population density, where smaller urchin sizes occurred in high urchin density habitat where food is a limiting resource (Levitan, 1991). Since fishing reduces predation pressure on the urchins, HFAs display a high density of small urchins (Levitan, 1992); a similar negative relationship between urchin density and size was also found in the current study, the smallest individuals being recorded at Tenerife. At Mar de Las Calmas and La Palma, where the percentage macroalgal cover is the highest, urchins smaller than those at La Graciosa were found where higher urchin densities and lower macroalgal cover was recorded. Macroalgal assemblage composition could be limiting the test diameter in Mar de Las Calmas and La Palma. In fact, test diameter has been shown to depend on macroalgal richness: assemblages with low algal richness (less algal species available) tend to support urchins with smaller test sizes. At Mar de Las Calmas and La Palma the unbranched erect algal group showed the highest percentage cover, comprising only four species, of which Lobophora variegata was the most abundant in the rocky benthic community (Tuya et al., 2005b; Tuya and Haroun, 2006, and this paper). Therefore, it is likely that D. aff. antillarum cannot make efficient use of this species, as has been reported for other echinoids (Arnold et al., 1995; Targett and Arnold, 1998; Bouderesque and Verlaque, 2001). Moreover, mixed algal diets or even mixed animal and algal diets are known to significantly enhance the growth of sea urchins and gonad production compared with single-species diets (Larson et al., 1980; Nestler and Harris, 1994; Meidel and Scheibling, 1999; Vadas et al., 2000). Further evidence comes from previous studies on D. aff. antillarum, which have shown that specimens recovered from species-rich algal environments had a greater number of algal species in their guts, and had greater test and gonad sizes (Herrera-Lo pez et al., 2003; Herna ndez et al., 2006; Herna ndez et al., 2007). In Tenerife, a situation of food shortage leads to a reduction in urchin body size to enhance survivorship, as has been suggested by Levitan (1989) in tropical areas. However, when high urchin densities coexist with algal assemblages that comprise branched erect and turf algae, which are highly palatable and preferred by D. antillarum (Sammarco, 1977, 1982; John et al., 1992) and D. aff. antillarum (Tuya et al., 2001; Herrera-Lo pez et al., 2003; Herna ndez et al., 2007), larger individuals are found, as occurred in La Graciosa despite this area having high urchin densities. Alternatively, selective predation combined with the amount of suitable refuges available to avoid predators may limit the test size of D. aff. antillarum, as in other sea urchin species (Sala and Zabala, 1996; McClanahan, 1999; Guidetti et al., 2003). At Mar de Las Calmas a high abundance of potential predators has been recorded (Bortone et al., 1991; Falcon et al., 1996; Tuya et al., 2004a) and urchins are restricted to crevices or holes accordingly, as a predator avoidance strategy. Consequently, a low mean test size along with low urchin biomass and high macroalgal cover can constitute a useful indicator of a healthy supply of predators and good conservation status, as reported at Mar de Las Calmas and La Palma. The present study shows different conservation states at the MPAs and HFA of the Canary Islands due to sea urchin grazing activity. Mar de Las Calmas has the most desirable conservation status of the three MPAs, with an insignificant extent of urchin barrens, followed by La Palma which also has a relatively low prevalence of barrens. La Graciosa was found to have the poorest conservation status of the MPAs, similar to a HFA, where urchin barrens are common. The larger dimensions and complexity of this MPA, along with it only possessing one small no take area, may lead to added difficulties enforcing regulations (Tuya et al., 2006), thus resulting in a high occurrence of poaching of important top predators. It is also important to note that a previous study of benthic assemblages at La Graciosa (Reyes et al., 2000), showed large areas occupied by Cystoseira sp. (so-called Cystoseira de los Roques ), Lobophora variagata, Sypocaulon and Sargassum beds at the rocky reefs. These same reefs have

14 J.C. HERNA NDEZ ET AL. been re-surveyed in this study after five years and are now dominated by urchins and with extensive barren grounds. These data emphasize that despite the measures taken to restrict fishing within the MPA, there has been replacement of macroalgal beds with urchin barrens and the establishment of an undesired state due to urchin grazing. Several natural factors that affect recruitment and mortality should be involved in \to the transitions between alternative algae urchin states. Also more than just one point in time surveys should be taken into consideration to clarify forces implied in the shift between these alternative states. Trophic cascade processes seem to be involved in the patterns observed at two MPAs (La Palma and Mar de Las Calmas), which indicates these MPAs have well structured systems (Sala and Zabala, 1996; Shears and Babcock, 2002; Tuya et al., 2004a, 2005b). This result is also supported by previous studies in which commercial fish species are shown to be more abundant in Mar de Las Calmas than in La Graciosa and other non-protected areas (Falco n et al., 1996; Tuya et al., 2006). Such well structured systems seem to avoid the general trend of ecosystem shifts and establishment of urchin barren stable states (Scheffer and Carpenter, 2003; Guidetti, 2006). In this sense, a complex interplay between abiotic and biotic factors, such as wave action, substrate complexity, depth, light, competition, predation and recruitment, may also be important in determining urchin abundance (Menge and Sutherland, 1987; Pinnegar et al., 2000; Hereu, 2004; Hereu et al., 2004; Herna ndez, 2006, Guidetti and Sala, 2007; Lauzon-Guay and Scheibling, 2007). Differences in fish communities throughout the Canary Islands and the presence of predators that could potentially prey on D. aff. antillarum, such as the balistids Balistes capriscus and Canthidermis sufflamen and the diodontid Chilomycterus reticulata in the western islands (Bortone et al., 1991; Falcon et al., 1996; Tuya et al., 2004a, 2006) are likely to explain this pattern. However, observational and tethering experiments to evaluate predation levels, as conducted by McClanahan and Muthiga (1989), Sala and Zabala (1996), Shears and Babcock (2002), Guidetti (2006), and Clemente et al. (in press) are needed, inside and outside MPAs. This study throughout the Canarian Archipelago has provided the opportunity to better understand the functioning of ecosystems at different scales of anthropogenic disturbance by removal of top predators, which causes dramatic shifts in the organization and structure of the coastal communities. However, these results lack an accurate study of urchin predator populations and only indirect assumptions of the current protection measures and their implications are given. Knowledge of the transitions between alternative states is needed to elucidate which processes mediate them, especially as undesired states seem to present high resistance to restoration. Differing resilience of systems has been detected in a small, although highly environmentally variable, area, which must be taken into account for management strategies. Management should focus on preserving the ecological conditions so that a reverse of marine ecosystem degradation is assured. This paper calls for an urgent change in current conservation strategies, such as creation and implementation of protected areas, more restrictive fishing regulations and others short-term strategies which could help to reverse the undesired situation. ACKNOWLEDGEMENTS We are indebted to two referees and the editor of this journal who greatly improved this paper. Thanks to J. Manning for translation labor and suggestions that always improve our manuscripts. La Palma: We would especially like to thank Sangil s family who were always at our disposal making our stay at La Palma easier and more comfortable. Thanks to A. Martı n Concepcio n of Agencia Insular del Mar (Insular Sea Agency) for his cooperation and interest. Thanks also to R. Ca ceres Ventura and R. Castro Martı n of Cueva Bonita diving club at Tazacorte, for their kindness. Mar de Las Calmas: thanks to J. M. Falco n, G. Gonza lez, A. Sancho and P. Pascual for their good advice and cooperation. Thanks to Francisco of Meridiano Cero diving club and to the crew and skipper of the MPA vigilance ship and to the fishing inspection ship, especially to Juan. La Graciosa: thanks to J. M. Falco n, G. Gonza lez, A. Sancho, F. Espino and P. Martı n for having so much fun during the hard days of work. Thanks to the crew and skipper of MPA vigilance ship and to the fishing inspection ship especially to the crew of A ngeles : Mingo, Jose and Juan Jose. Tenerife: Thanks to Tania Diaz-Villa for her help during the field data collection. REFERENCES Afonso J, Sanso n M Algas, hongos y fanero gamas marinas de las Islas Canarias (clave analı tica). Servicio de Publicaciones de la Universidad de La Laguna. Aguilera F, Brito A, Castilla C, Díaz A, Ferna ndez-palacios JM, Rodrı guez A, Sabate F, Sa nchez J Canarias, economıá, ecologıá y medio ambiente. Francisco Lemus editor, La Laguna. Alves FMA, Chícharo LM, Serrao E, Abreu AD Algal cover and sea urchin spatial distribution at Madeira Island (NE Atlantic). Scientia Marina 65: Alves FMA, Chı charo LM, Serrao E, Abreu AD Grazing by Diadema antillarum (Philippi) upon algal communities on rocky substrates. Scientia Marina 67: