ICES Journal of Marine Science: Journal du Conseil Advance Access published online on November 9, 2008
ICES Journal of Marine Science: Journal du Conseil, doi:10.1093/icesjms/fsn176
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Evidence of the top–down role of predators in structuring sublittoral rocky-reef communities in a Marine Protected Area and nearby areas of the Canary Islands
1 Departamento de Biología Animal (Ciencias Marinas), Universidad de La Laguna, Avenida Francisco Sánchez s/n 38206, La Laguna, Islas Canarias
2 Biology Department, Villanova University, Villanova, PA, USA
Correspondence to S. Clemente: tel: +34 922 318387; fax: +34 922 318311; e-mail: msclemen{at}ull.es.
Clemente, S., Hernández, J. C., and Brito, A. 2009. Evidence of the top–down role of predators in structuring sublittoral rocky-reef communities in a Marine Protected Area and nearby areas of the Canary Islands. – ICES Journal of Marine Science, 66.Differences in the sea urchin Diadema aff. antillarum population structure, which have been attributed to removal of predatory fish through overfishing, are observed throughout the Canary Islands. Low urchin abundances and a "desired conservation state" are currently found in Mar de Las Calmas Marine Protected Area and nearby fished areas (FAs) in El Hierro Island, in contrast to the occurrence of high urchin densities and the "undesired conservation state" in the highly FAs (HFAs) of Tenerife Island. Under these different levels of fishing pressure, we consider a set of ecological variables potentially affecting urchin populations (settlement, recruitment, adult urchin densities, predation rates, and abundance of urchin fish predators) to infer their magnitude and relative importance in addressing community-wide changes. No differences in settlement and recruitment rates were found, but predation pressure was higher in El Hierro, where adult density was low and predation rates were high. The combination of these factors provides evidence of a top–down control of sublittoral reef communities. Although the effect of protection was less clear, we demonstrate the positive effects of reduced fishing effort in enhancing trophic cascade processes and reducing the establishment of barren grounds.
Keywords: fish abundance, fishery restrictions, predation index, sea urchin abundance, sea urchin recruitment, sea urchin settlement
Received 26 October 2007; accepted 2 June 2008.
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Introduction |
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 Top Introduction Material and methodsResultsDiscussionReferences |
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Sea urchins play a key role in structuring infralittoral benthic communities. At high densities, they can drastically reduce the algal cover on rocky bottoms and transform wide extensions of the rocky littoral zone from complex and productive algal communities into simplified barren grounds, which are dominated by encrusting coralline algae (Lawrence, 1975; Vadas and Elner, 1992). Therefore, they have been suggested as being involved in mediating transitions between alternate stable states (Knowlton, 2004), which occur when more than one type of community can persist in a single environmental regime (see review in Beisner et al., 2003).
Sea urchin abundance is highly variable in time and space (Pearse and Hines, 1987; Turón et al., 1995; Sala et al., 1998a; Hernández et al., 2008a), and relatively small fluctuations can lead to severe effects on the benthic system. Therefore, the key to understanding the transition from erect algal communities to barrens is the regulation of sea urchin population dynamics (Sala et al., 1998b).
In the Canary Islands (eastern Atlantic), barren areas generated by the sea urchin Diadema aff. antillarum are common (Brito et al., 2004; Tuya et al., 2004; Hernández et al., 2005a) and extensive, occupying 
75% of rocky bottoms, with a major impact on coastal ecosystems (Hernández et al., 2008a). Population dynamics of this key herbivore appear to be partially controlled by a complex interplay of settlement, recruitment, and predation events (Hernández, 2006; Clemente, 2007; Clemente et al., 2007a), as has been suggested for other species (Sala and Zabala, 1996; Sala et al., 1998b; Tomas et al., 2004; Hereu et al., 2005). The influence of settlement and subsequent recruitment events in determining the sea urchin population dynamics has been studied widely (Ebert, 1983; Roughgarden et al., 1985; Watanabe and Harrold, 1991; Balch and Scheibling, 2001). In situations with high larval supply and low post-settlement mortality, settlement can increase urchin abundance (Andrew, 1993; Hereu et al., 2004, 2005; Hernández, 2006), leading to the formation of coralline barrens (Hart and Scheibling, 1988; Hereu et al., 2004). Alternatively, low urchin settlement rates can also shape communities when supply is limited, thus preserving algae communities (Roughgarden et al., 1985; Scheibling, 1986). Moreover, strong recruitment episodes may increase urchin abundance and determine size distributions (Watanabe and Harrold, 1991; Sala and Zabala, 1996), whereas low recruitment rates may be enough to maintain urchin populations and the barren ground habitat whenever urchin predators are scarce, and produce low levels of adult urchin mortality (Sala et al., 1998b). Understanding natural patterns of temporal and spatial variability in settlement and recruitment is essential when evaluating their role in controlling urchin populations (Ebert, 1983; Balch and Scheibling, 2001; Hereu et al., 2004; Hernández, 2006; Hernández et al., 2006).
Previous studies in the Canary Islands have assessed spatio-temporal fluctuations in settlement and recruitment of D. aff. antillarum, describing a mean annual settlement peak during August–October and an annual recruitment peak during November–December, both consistent between years and sites, although variable in magnitude (Hernández, 2006; Hernández et al., 2006). Recruitment appears to be a controlling force for D. aff. antillarum populations in the absence of effective predators in overexploited areas (Hernández, 2006; Clemente et al., 2007a). However, it has often been suggested that predation is the main process determining sea urchin population structure (Tegner and Dayton, 1981; McClanahan and Muthiga, 1989; Sala et al., 1998b; Shears and Babcock, 2002; Hereu et al., 2005), and that it can control any fluctuation expected in urchin density as a consequence of variable settlement and recruitment episodes (Sala and Zabala, 1996; Sala et al., 1998a, b; Hereu et al., 2004, 2005) through size-selective predation.
In this study, we evaluate the significance of these three ecological variables (settlement, recruitment, and predation) as causative forces for the distribution of the key herbivore D. aff. antillarum and the establishment of barren grounds in the Canary Islands. We conducted several specific experiments and compared urchin and predator populations in a Marine Protected Area (MPA; Mar de Las Calmas) and in nearby fished areas (FAs) of El Hierro Island, as well as in a more distant unprotected area of Tenerife Island. All these areas support distinct fisheries and represent the different exploitation conditions found in the Canarian Archipelago, where predator abundance is likely to be more abundant inside the MPA. We hypothesize that lower levels of effective urchin settlement in El Hierro explain the persistence of algae communities and low urchin densities (Hernández et al., 2008a, 2008b) through natural mortality. Conversely, if larval supply and settlement rates do not differ in El Hierro from common barren grounds of Tenerife Island (Hernández et al., 2008a, 2008b) but increased urchin mortality caused by predation occurs, a top–down control of sublittoral rocky-reef communities would take place and determine the functioning of the system.
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Material and methods |
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Study sites
The study was carried out in the Mar de Las Calmas MPA (Canary Islands), in a nearby unprotected and fished area (FA) off El Hierro Island and in a more distant, highly FA (HFA) off the central island of Tenerife (Figure 1). Between September and December 2006, we surveyed two sites in the Mar de Las Calmas MPA no-take area, where all fishing, harvesting, and scuba diving activities are forbidden, and only scientific activities are allowed; two sites in the unprotected coast of El Hierro, which support sustainable fisheries and low levels of fishing pressure, with 0.14 fishing boats km–1 of the island’s perimeter (Bortone et al., 1991; Bas et al., 1995; Tuya et al., 2006); and two more sites in the HFA of Tenerife that encompass a fishing fleet of 0.74 ships km–1 of the island’s perimeter (Bas et al., 1995; Tuya et al., 2006), where all types of commercial and recreational fishing occur (Figure 1). No fishing management or any protection regime, such as an MPA, is implemented in Tenerife Island, where the highest levels of fishing pressure in the Canarian Archipelago take place (Bortone et al., 1991), so the protection treatment could not be appropriately replicated. However, we have included the case of Tenerife in the sampling design to provide a view of the overall situation of the whole archipelago, including a scenario with much denser urchin populations and higher fishing effort, which is the general situation in the archipelago in contrast to El Hierro Island.
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Diadema aff. antillarum settlement rates
We define settlement as the appearance of post-larvae and early juvenile urchins on experimental samplers over a 1-month interval (Tomas et al., 2004; Hernández et al., 2006). We used the technique described by Hernández et al. (2006) in which 100 moulded 3.9-cm diameter plastic balls, originally used as biofilters, were placed into a 50 x 50-cm mesh bag. Three samplers were placed simultaneously at each study site between 5- and 10-m deep during the annual settlement peak of this species in the Canary Islands (September–October; Hernández, 2006), then recovered after 1 month. The organisms were washed from the samplers (Hernández, 2006), and all newly settled D. aff. antillarum were identified using the method described in Hernández et al. (2005b) and counted under a stereomicroscope (20x).
Diadema aff. antillarum recruitment rates
We define recruitment as the appearance of individuals of <20 mm test diameter (Hernández, 2006) on 25 x 25 cm quadrats over natural substratum, a method previously used to quantify recruitment of several echinoid species (Tegner and Dayton, 1981; Rowley, 1989; Tomas et al., 2004; Hernández, 2006). Within 1 month of settlement, ten quadrats per site were randomly deployed during the recruitment peak of D. aff. antillarum in the Canary Islands (November–December; Hernández, 2006).
Diadema aff. antillarum adult densities
At each site, the belt transect method was used to estimate D. aff. antillarum adult densities (>20 mm in test diameter), a technique frequently used with echinoids (Turón et al., 1995; Sala and Zabala, 1996). In all, eight 10 x 2-m transects were surveyed parallel to the coastline between 5- and 15-m deep.
Predation level upon Diadema aff. antillarum
We evaluated predation levels by tethering experiments (Clemente et al., 2007a). This technique has also been used to test predation intensity on sea urchins in tropical (McClanahan and Muthiga, 1989; McClanahan et al., 1999) and temperate systems (Sala and Zabala, 1996; Shears and Babcock, 2002; Guidetti, 2006). D. aff. antillarum individuals of three different size classes (Class 1, 20–30 mm; Class 2, 30–40 mm; Class 3, 40–50 mm) were tethered to lines fixed to the substratum (McClanahan and Muthiga, 1989). As handling this species becomes difficult because of its morphological characteristics, a modified tagging technique that used external tags, which were anchored through holes drilled in the urchin tests, was employed. This method was previously tested for artefacts with enclosure cages and successfully applied in situ to D. aff. antillarum (Clemente et al., 2007b).
Ten tagged individuals of each size class were attached at 1-m intervals along 11-m transect lines laid over rocky reefs at depths between 4 and 10 m at each site. Each individual was threaded with 40 cm of nylon monofilament, which allowed urchins to roam an area of 0.785 m2 and usually find holes or crevices to occupy in the substratum. The experiments were visited every 24 h over 5 d to determine the number of individuals that died during each daily interval. Urchins that appeared to be dying as a result of the piercing procedure, characterized by intact bleached tests with spines missing around the hole through which they were pierced (Clemente et al., 2007b), were identified during daily monitoring. Individuals that lost their tag in the period 1–4 h before the beginning of the experiment were also detected. To minimize these effects, these individuals were replaced and removed from the data analysis.
Survival rate (S) was calculated as the number of days each individual survived in the experiment, and predation rate as the total length of the experiment (5 d) minus the survival rate. Finally, a relative predation intensity index (PI) was calculated for each site and size class, dividing predation rate by the length of the experiment [PI = (5 – S)/5]. The index produces a value between 0 and 1, where 0 corresponds to no urchins eaten over the whole experiment and 1 to all individuals eaten during the first experimental day.
Diadema aff. antillarum fish predator populations
Based on Clemente (2007), densities of the main fish predators of D. aff. antillarum, two balistid species (Balistes capriscus and Canthidermis sufflamen), one diodontid (Chilomycterus reticulata), one labrid (Bodianus scrofa), and two sparids (Diplodus cervinus and Diplodus sargus) were estimated using an in situ stationary visual-census method. We followed the point-count method in which the observer takes a position at the centre of a circle with a radius of 5.6 m (100 m2), recording the number and size (±1 cm) of the individuals of each species for 5 min (Bortone et al., 1989). Six replicates of this procedure were conducted at each site. As in previous studies evaluating populations of urchin predatory fish (Guidetti, 2006), juvenile stages were excluded from the assessments, because their numerical contribution may strongly influence average densities while having no predatory effect on urchins (Clemente, 2007). For the same reason, only large D. sargus, approximately larger than two-thirds of the maximum size (TL; >30 cm) and medium-large D. cervinus (>30 cm) were considered in the analysis, because they are the only sizes able to prey effectively on D. aff. antillarum (Clemente, 2007).
Data analyses
Diadema aff. antillarum settlement and recruitment rates, adult urchin densities, as well as relative predation index, and total fish predator abundances were compared with distance-based permutational ANOVAs (Anderson, 2001). A two-way design was conducted when analysing settlement, recruitment, adult urchin abundances, and total fish predator densities, in which Area was treated as a fixed factor with three levels (MPA, FA, HFA) and Site as a random factor nested within Area, with six levels. A three-way design was performed when analysing relative predation index, in which urchin Size was also included as a fixed factor with three levels (20–30, 30–40, >40 mm). All analyses were based on Euclidean distances of raw data, with p-values obtained using 4999 permutations of the appropriate exchangeable units (Anderson, 2001). Significant terms in the full model were examined individually using appropriate a posteriori pairwise comparisons, also conducted by permutations (Anderson, 2001). The software PRIMER 6 & PERMANOVA+ (www.primer-e.com) was used to perform all procedures.
Linear relationships between settlement and recruitment rates, between relative predation index and densities of adult D. aff. antillarum, and the potential relationship between total abundance of predatory fish and densities of adult urchins were assessed using the SPSS-14 statistical package.
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Results |
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Settlement, recruitment, and adult densities of Diadema aff. antillarum
Settlement of D. aff. antillarum was observed at all sites within the three surveyed areas of the Canarian Archipelago (Figure 2a) and permutational ANOVA revealed no differences in the number of newly settled urchins per sampler between areas and sites (Table 1). Conversely, recruits were not observed at all studied sites and areas (Figure 2b), but no significant effect of Area on recruitment rate was found in the analysis (Table 2). However, the ANOVA revealed significant differences in the density of new recruits between sites within each studied area [Site (Area); Table 2]. Adult urchin densities were highly variable; the analysis revealed a significant effect of Area as well as highly significant differences at the local level (Table 3). A posteriori pairwise analyses revealed that densities of adult D. aff. antillarum in the MPA and nearby FA of El Hierro were significantly lower than those recorded in the Tenerife HFA (Table 3; Figure 2c).
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Predation level on Diadema aff. antillarum and fish predator populations
We recorded predation events on D. aff. antillarum in all studied areas and sites (Figure 2d). Comparison of relative predation intensity indices by ANOVA demonstrated a significant interaction of Area x Size (Table 4), meaning that predation intensity differed between urchin sizes in relation to the area considered (Figure 3). A posteriori analyses for this interaction revealed a significantly higher predation index for the smallest urchins (20–30 mm) compared with larger urchins in the Tenerife HFA (Table 4; Figure 3). However, the highest predation levels recorded in El Hierro, both in the MPA and FA, did not differ between studied urchin sizes (Table 4; Figure 3). In fact, predation pressure in both areas of El Hierro was not significantly different when considering small- and medium-sized urchins (20–30 and 30–40 mm), but they differed from values obtained in the Tenerife HFA (Table 4; Figure 3). Only in the largest urchin size class were there differences between the MPA, which supported higher predation, and the FA of El Hierro (Table 4; Figure 3).
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There were significant differences between study areas in the densities of D. aff. antillarum fish predators (Table 5; Figure 2e). Predatory fish abundances were significantly higher in the Mar de Las Calmas MPA than in the Tenerife HFA, although no differences were obtained between the MPA and FA of El Hierro Island (Table 5; Figure 2e). Moreover, there was no effect of Site within each study area (Table 5).
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Relationships between the measured variables
No significant relationship was detected between the D. aff. antillarum settlement rate (number of newly settled individuals per sampler) and the density of adult urchins (Figure 4a). However, a significant positive linear relationship was found between sea urchin recruitment rate (number of new recruits m–2) and adult urchin density (Figure 4b).
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There was a significant negative and linear relationship between the relative predation intensity index and the density of adult D. aff. antillarum (Figure 5a). The density of adult urchins also varied inversely with the total abundance of urchin fish predators (number of individuals 100 m–2; Figure 5b). The scatterplots show higher variability in the data at the lowest levels of both predation index and total abundance of predators (Figure 5a and b), whereas variability decreases at the highest levels of the variables, and the data appear to be much more adjusted to the models.
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Discussion |
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The three areas studied can be considered as different phases of benthic rocky ecosystems in the Canary Islands, with different structures and functioning in which D. aff. antillarum appears as a key species (Hernández et al., 2008b). The progressive development of fisheries has led to a clear overexploitation of marine ecosystems in the archipelago as a direct consequence of the expanding population (Hernández et al., 2008b). This situation has contributed to the deterioration of littoral fish communities, especially in the most developed island of Tenerife, in agreement with the worldwide trend in declining fishery resources in the past few decades (Pauly et al., 1998; Worm et al., 2006). However, El Hierro Island, the smallest (287 km2) and most isolated of the archipelago, has a less perturbed inshore fishery (Bortone et al., 1991; Falcón et al., 1996; Tuya et al., 2004) associated with its delayed development and sustainability policies (Bortone et al., 1991), including the establishment of an MPA.
Previous studies have related human pressure and the overexploitation of urchin fish predators to the increasing development of D. aff. antillarum populations and the subsequent depletion of algal stands (Clemente, 2007; Hernández et al., 2008a, 2008b). However, the simultaneous evaluation conducted in this study of the ecological variables involved in this phenomenon, such as urchin settlement, recruitment, and predation, is the key to understanding the transition between different states of the system. Our results support the hypothesis that reduced fish predator populations as a result of overfishing can explain extremely high urchin abundances. In fact, none of the study areas appeared to differ in successful urchin settlement, so larval supply does not seem to be limiting urchin populations. However, knowing the limited temporal replication of the present study, we have to be cautious when interpreting the results. We found some site variability in urchin recruitment and, despite non-significant effects, no recruits were observed in the Mar de Las Calmas MPA, so the area-related pattern of recruitment was similar to the pattern of adult D. aff. antillarum abundance. The pronounced differences in urchin abundances between El Hierro, both within the MPA and FA, and Tenerife seem to be caused by differences in post-settlement and post-recruitment mortality events, of which fish predation upon juvenile and adult urchins appears to be most important. However, substantial mortalities in the early stages may be caused by other factors related to less-altered ecosystems, such as predation by other invertebrates that commonly inhabit algal assemblages (Sala and Zabala, 1996; Hereu et al., 2005); the availability of suitable substrate or habitat, which in El Hierro is mainly constituted by brown algae Lobophora variegata stands (Sangil, et al., 2006); or the lack of conspecifics. Other studies have already demonstrated the relevance of post-settlement processes, especially mortality events that can sometimes be very high (Rowley, 1989) and structure urchin populations (Cameron and Schroeter, 1980; Rowley, 1989).
Fish predator populations seem to have a major influence on urchin populations, as demonstrated in other systems (Hay, 1984; McClanahan and Muthiga, 1989; Sala and Zabala, 1996). However, the effects of protection from fishing activities were not clear in El Hierro, which seems to retain a high conservation status all around its littoral (Hernández et al., 2008a). Instead, observed differences in the role of top–down forces may be associated with intrinsic between-island variability. Biogeographical differences in fish communities are widely known throughout the Canary Islands, where urchin fish predators, such as B. capriscus, C. sufflamen, and Ch. reticulata, are more common in the western islands (Bortone et al., 1991; Falcón et al., 1996; Tuya et al., 2004). Our findings are consistent with this spatial pattern and provide evidence of a critical threshold in the abundance of fish predators and in predator intensity to keep D. aff. antillarum at low densities. Higher densities of major urchin fish predators and increased predation were obtained in El Hierro, and very low predation upon all urchin sizes in Tenerife, as a result of the abundance and composition of the predatory guild, in which only certain sparid species, mainly predators of juveniles, are locally abundant (Clemente, 2007; Clemente et al., 2007a). However, there was a heavy predation pressure in the Mar de Las Calmas MPA upon the largest urchins (>40 mm), probably an effect of protection that increases the mean size of specific predators that provide more control over large individuals.
Urchin populations in El Hierro encompass individuals that were able to escape the existing high levels of fish predation, probably by utilizing the substratum for refuge (Clemente, 2007), because structural complexity of habitat is known to reduce predation of early settled individuals (Andrew, 1993; Sala and Zabala, 1996; Hereu et al., 2004). In Tenerife, where barren grounds are commonly extensive (Hernández et al., 2008b), the high urchin densities recorded appear to be determined by increased levels of urchin recruitment and low predation levels. When urchins grow to a certain size, they are no longer under the same predation pressure (Tegner and Dayton, 1981; McClanahan and Muthiga, 1989; Sala and Zabala, 1996), which in Tenerife occurs at relatively smaller urchin size, because fish mean size has been reduced by overfishing. Therefore, differences in system functioning have been verified. Whereas in El Hierro, we demonstrated a top–down control of communities, in which predation limits the survival of recently settled and adult D. aff. antillarum, in Tenerife, the magnitude of recruitment appears to control local variability in urchin abundance, as has been suggested with other echinoids (Sala and Zabala, 1996; Hereu et al., 2005).
In recent years, D. aff. antillarum populations have increased greatly in the Canary Islands (Hernández et al., 2008b). This study suggests that recruit abundance along with the lack of fish predators, especially of those effective in targeting a wide urchin size spectrum in overfished areas of the archipelago, is an important factor in this degradation process. The reduction of fish predators by severe overfishing in most areas of the archipelago have led to an urchin population outbreak driven by settlement and recruitment processes (Hernández, 2006; Clemente, 2007), with dramatic consequences to the entire benthic community.
This study confirms that there are positive effects of MPAs or reduced fishing efforts in enhancing and maintaining trophic cascades that control urchin populations and reduce the establishment of barren grounds (Sala and Zabala, 1996; Sala et al., 1998a; Shears and Babcock, 2002; Hereu et al., 2005; Guidetti, 2006). Increased fish predator populations, even in unprotected areas that are remote and have a low human population or fishing effort, may have important implications for the structure and functioning of benthic communities, as reported in El Hierro island and other regions (Hay, 1984; McClanahan, 1994; McClanahan and Muthiga, 1989; Sala and Zabala, 1996). In El Hierro, algae stands are widely distributed (Hernández et al., 2008a), there are healthy fish predator populations, and there is a high resilience that maintains this state. Conversely, the HFA of the archipelago, where the urchin population appears to be driven mainly by settlement and recruitment events, demonstrate a great resistance to the reversal of barren grounds into more complex algal systems (Hernández et al., 2008b). Therefore, the establishment of fishery policies to restore populations of urchin fish predators and the trophic structure of the system is urgently needed. Management should focus on the exclusion of urchin predatory fish from fisheries in the Canary Islands and on creating new protection categories, which should include functionally important species. Considering the ecological importance of predators and the dramatic barren situation of the Canary Islands, more studies are needed to define D. aff. antillarum predatory guilds accurately. Additionally, more protected areas all around the archipelago should be created to enhance predator fish populations and maintain or recover the desirable conservation status of the marine ecosystem through trophic cascade processes.
In conclusion, this study reveals the importance of reduced fishing intensity in promoting cascading effects on benthic communities, suggesting that transitions between algal beds and barren grounds could be driven by thresholds in predatory fish abundance. However, the importance of predation control depends greatly on the incidence of other ecological variables such as urchin recruitment rate. Moreover, we demonstrate the need to consider different fishing levels among "non-protected treatments", within a framework of increasing marine ecosystem degradation gradient, to interpret ecological results accurately.
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Acknowledgements |
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A. Rodríguez, D. Girard, and K. Toledo helped during field and laboratory procedures. We are indebted to N. Aguilar and M. Johnson for accommodating us in the new Marine Laboratory of El Hierro, and to Capt. O. Monterroso, who skippered the research vessel. L. Rodriguez greatly improved first drafts of this paper. SC and JCH benefited from a postgraduate fellowship provided by the Spanish Ministerio de Educación y Ciencia within the FPU programme.
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