Mar Biol (2007) 151:1153–1161 DOI 10.1007/s00227-006-0557-0
R E SEARCH ART I CLE
Detecting conservation beneWts in spatially protected Wsh populations with meta-analysis of long-term monitoring data C. Ojeda-Martinez · J. T. Bayle-Sempere · P. Sánchez-Jerez · A. Forcada · C. Valle
Received: 2 August 2006 / Accepted: 10 November 2006 / Published online: 14 December 2006 © Springer-Verlag 2006
Abstract Marine protected areas (MPA) produce a positive eVect on Wsh populations, but this may be diYcult to identify due to the high temporal variability of populations. Meta-analysis is an option for analysing data from diVerent sources and sampling designs and it can address problems related to temporal and spatial variability in Wsh populations. We analysed Wsh abundance data from visual counts conducted in summer, from 1996 to 2002, in the MPA of Tabarca (Alicante, Spain). The results showed an overall positive eVect of protection at the species and family levels. Overall abundance of Wshes inside the reserve was, on average, 1.22 times higher than outside the reserve boundaries. Positive eVect of protection was found for Boops boops, Diplodus annularis, Diplodus cervinus, Epinephelus marginatus, Epinephelus costae and Epinephelus aenus. Species of Labrids were not aVected by protection, except for Thalassoma pavo and Symphodus ocellatus. Meta-analysis of temporal data allows evaluation of the protection MPA provide and is particularly useful when data sources have diVerent experimental designs or sampling programs. The Tabarca MPA has beneWted Wsh populations by increasing their abundance and we suggest that meta-analysis is a complementary tool for the management of MPAs.
Communicated by S.A. Poulet, RoscoV. C. Ojeda-Martinez (&) · J. T. Bayle-Sempere · P. Sánchez-Jerez · A. Forcada · C. Valle Departamento de Ciencias del Mar y Biología Aplicada, Unidad de Biología Marina, Universidad de Alicante, Apdo. 99, 03080 Alicante, Spain e-mail:
[email protected]
Introduction Marine protected areas (MPA) are being established worldwide at a rapid rate. Locations with important ecological and socio-economic beneWts are being managed to protect habitats and biological richness and restore Wshing stocks and degraded areas. (Allison et al. 1998; Bohnsack 1998; Lauck et al. 1998; Hastings and Botsford 1999; Murray et al. 1999; Agardy 2000) As a result, biological diversity, population structures and community conWgurations return, in time, to states that existed prior to human alterations (Ramos-Esplá et al. 2004). Conservation beneWts of MPA can be predicted by estimating the reductions in Wshing mortality that result from protection and assessing how that aVects the abundance and dynamics of resident Wsh populations (Beverton and Holt 1957; Buxton and Smale 1989; Ciriaco et al. 1998; Cadoret 1999). It is becoming apparent that these beneWts do not apply to all species all of the time (Mosquera et al. 2000), and therefore quantifying the conservation beneWts of MPA is complex (Guenette et al. 1998). However, identifying general patterns for deWning the eVects of protection on Wsh assemblages are crucial for correct management of MPAs. The existence of strong temporal variability in ichthyofauna abundance is usual (Holbrook et al. 1994). This temporal variability, especially interannual, must be considered to understand the eVect of protection on Wsh abundance because the reserve eVect could vary among years according to annual or pluriannual cycles (Francour 1994). Meta-analysis (deWned as the quantitative analysis of data that originated from several independent studies) provides major advantages over more traditional
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synthesis and reviews (Hedges and Olkin 1985; Gurevitch and Hedges 1993). The underlying approach and objectives are to quantify emergent patterns by applying speciWc statistical procedures (Hughes et al. 2002). Following advances in the social sciences (Glass et al. 1981) and medicine (Sachs et al. 1987), applications of meta-analysis to ecological data are becoming increasingly common (Arnqvist and Wooster 1995; Osenberg et al. 1999). Meta-analysis methods represent a complementary tool for monitoring and management in MPA. Nevertheless, studies using meta-analysis that test and quantify if MPA are working correctly are scarce (Mosquera et al. 2000; Coté et al. 2001). In this work, we use meta-analysis to deWne, to compare the general eVects of 16 years of protection. We have used a long-term data set of Wsh assemblages (6 years from 1996 to 2002), of the marine Protected Area of Tabarca Island (Alicante, Spain) and unprotected locations. By using a meta-analysis statistical methodology, we tried to assess the hypothesis that Wsh abundance is positively aVected due to protection, in spite of the inherent temporal variability of Wsh populations. The objectives were (1) to detect the overall eVects of 16 years of protection on Wsh assemblage parameters using two taxonomic levels, family and species, and (2) to assess the protection eVect for each family and species independently.
Materials and methods Study site The study area was Tabarca Island Marine Protected Area, (Alicante, SE Spain; 38° 09⬘ 30⬙N; 00° 28⬘30⬙W). The studied MPA was created in 1986, with an area of 1,400 ha and is patrolled at full time during all the year. Cabo San Martín–Cabo Negro (with Portichol island) and Altea Bay (Morro de Toix, Cabo Mascarat and Olla de Altea islands) were chosen as control areas, as they had similar topography to the MPA and all three areas exhibited alike habitat structure (Forcada 2005), and were located 88 and 67 km away and therefore were unlikely to be inXuenced by the reserve (Fig. 1). The sampling habitat was rocky substrate, composed primarily of boulders of diverse sizes interspersed with patches of sand and Posidonia oceanica seagrass meadow, between 10 and 20 m depth. Sampling design Data were obtained from the monitoring studies carried out for the University of Alicante on the MPA and
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control locations (Bayle-Sempere 1999; Forcada 2005), using visual censuses. These sampling methods have been used extensively in MPAs because they are nondestructive and guarantee that the Wsh community is not aVected by sampling, avoiding interference with previous evaluations of the eVects of protection, and maintain a high degree of consistency of gathered data among observers over time (i.e., performance to survey the most visually observable fraction of the Wsh with the same eYciency) (Harmelin-Vivien et al. 1985; Harmelin-Vivien and Francour 1992). No similar biological data are available from the period prior to the establishment of the MPA. However, it was obvious from technical reports (Ramos Esplá 1985) and interviews of persons living in and knowing the area that there had been substantial anthropogenic changes in the area prior to the establishment of the reserve, mostly overWshing that cause the depletion of Wsh assemblages. In these studies, nine sites (separated by 100s of meters) in each location (MPA and two control locations) were randomly selected. Three replicate transects of 50 £ 5 m were used to count Wsh abundance. The monitoring was carried out in summer, June to August, in 6 years from 1996 to 2002. Meta-analysis procedure Fish abundance (number of individuals per 250 m2) was estimated for each transect at the species and family levels. The eVect that protection generates on Wsh assemblage structure was quantiWed with the mean abundance and standard deviation of all data from inside the MPA and from the two control locations. We used the arithmetic mean for Wsh species abundance for the data from the two control areas. Finally, we worked with two treatments: MPA and control. Meta-analysis was carried out for the six sets of data from 1996 to 2002 (Bayle-Sempere 1999; Forcada 2005). We removed several species from the data set because they could produce an error eVect in the interpretation of the results (García-Charton et al. 2004). Small-sized, cryptic species (belonging to the Bleniidae, Gobiidae, Syngathidae and Tripterygidae families) were excluded from the censuses to avoid biases. Reduced total abundance and eVects of protection was estimated by excluding all pelagic and highly patchy species (Atherinidae, Engraulidae and Sphyraenidae), including shoaling species occupying the water column (Pomacentridae) and those species that were particularly cryptic (Apogonidae, Phycidae and Gadidae). Several authors (Bayle-Sempere 1999; García-Charton
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et al. 2004) have used this species reduction in single and multi-variant techniques to analyze the eVects of MPA, and the same appears to be useful for meta-analysis. Meta-analysis is a set of quantitative methods designed to synthesize the results of disparate studies (Hedges and Olkin 1985). It oVers several advantages over traditional, quantitative reviews of the literature. In particular, it allows the computation of both the magnitude and signiWcance of an overall eVect shared among studies. This overall eVect size is based on the calculation of eVect sizes for each contributing study, and these eVect sizes do not depend on sample size (FernándezDuque 1997). However, the meta-analysis approach also acknowledges that studies with large sample sizes, temporal and spatial, may be more reliable, and the technique oVers the possibility of weighting studies by their sample size or similar measure of reliability (Cooper and Hedges 1994; Arnquist and Wooster 1995). Mean number and standard deviation of Wsh for the MPA and the control sites were sampled in equal areas (250 m2) in the diVerent years. For this reason, data obtained for the MPA and the control sites could be directly compared. So, meta-analysis could be performed by the “eVect size” metric by Cohen’s coeYcient (Hedges and Olkin 1985; Lajeunesse and Forbes 2003). Means and variances for control data were made using the mean abundance for each species. Following this procedure, global eVect of protection was estimated by means of species and family abundances, as well as the eVect of protection for each independent species and family.
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EVect on species In total, 31 species were aVected positively by protection, while 17 showed the opposite pattern (Table 1). For example, we obtained a positive and signiWcant response to protection for Diplodus annularis, Diplodus sargus, Diplodus vulgaris, Epinephelus marginatus (E = 3.842, P < 0.01), Oblada melanura, Spicara maena, Symphodus ocellatus (E = 2.727, P < 0.001), Sciaena umbra (E = 4.18, P < 0.001) and Thalassoma pavo (E = 5.727, P < 0.001). Some species exhibited a positive response to protection, although this was not statistically signiWcant, such as Muraena helena and Diplodus cervinus (Fig. 2). In contrast, some species showed a higher negative response to protection (e.g., Mullus surmuletus: E = ¡3.125, P < 0.01; Symphodus roissali: E = ¡1.743, P < 0.01; and Coris julis: E = ¡1.8, P < 0.001; Fig. 2). EVect on families Nine families responded positively to protection (Table 2). Centracanthidae (E = 1.94, P < 0.001), Labridae (E = 0.687, P < 0.001), Sciaenidae (E = 4.18, P < 0.001), Sparidae (E = 1.536, P < 0.001) and Serranidae (E = 1.259, P < 0.01) were statistically signiWcant (Fig. 3). Other families such as the Belonidae, Haemulidae and Moronidae did not respond signiWcantly to protection. Mullidae (E = ¡3.12, P < 0.01), Scorpaenidae (E = ¡0.17, ns) and Congridae (E = ¡0.8, ns) showed a negative eVect to protection.
Discussion Results A total of 59 Wsh species (belonging to 23 families) were observed during the six summer censuses at Tabarca MPA and the control areas (Bayle-Sempere 1999; Forcada 2005). Sparidae (15 species), Labridae (13 species) and Serranidae (6 species) were the families most represented. Overall eVect at diVerent taxonomic levels When all species were considered, Wsh abundance was higher in the MPA. The eVects of protection [eVect (E): E = 1.22, P < 0.001] indicates that Wsh were on average 1.2 times higher in the MPA than in controls, being statistically signiWcant. When meta-analysis was analyzed at family level, protection eVect was higher (E = 17.14, P < 0.001)
Our meta-analysis oVers the Wrst large quantitative estimation of the magnitude of the protection eVects on Wsh abundance in a MPA in the Mediterranean Sea. We found that Wshes were on average 1.2 times more abundant inside than outside the MPA. In general, species and families were more abundant within the MPA. Targeted species were more abundant within the reserve; however, non-target species showed similar abundances inside and outside the MPA or were in higher abundances outside the reserve boundaries. Increased abundances of target species, and of total abundance and biomass, is to be expected within MPAs due to reduced Wshing mortality. These results conWrm the widely held opinion that marine reserves are beneWcial to Wsh populations (Roberts and Polunin 1991; Bohnsack 1998; García-Charton et al. 2000; Halpern 2003).
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Fig. 1 Control areas and MPA location, including limits and zonation of Tabarca Marine Reserve (I integral reserve area, II damping area, III transitional area)
In our study, mean abundances increased due to rises in the frequency and density of target species like Epinephelus marginatus, Sciaena umbra and Diplodus sp. This occurs visibly in other studies done in MPA when comparing protected and unprotected locations (e.g., García-Rubiés and Zabala 1990; Rakitin and Kramer 1996; Willis et al. 2003) and also this trend was shown in studies with temporal replication scales ranging from 2 to 3 years (e.g., Harmelin et al. 1995; Edgar and Barrett 1997). These species have low natural mortality, late maturity, slow growth rates and/or low rates of recruitment and are the most targeted by Wshermen (Russ 1991). Populations of the species outside of MPAs are Wshed down, by both commercial and recreational Wshing. A similar response should be expected of Sparus aurata, Conger conger, Scorpaena sp., Mullus surmuletus, Serranus cabrilla, Pagrus pagrus, Pagellus
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sp., and Spondyliosoma cantharus, which are also aVected by Wshing, but they did not respond positively to protection. This result could be due to the intrinsic characteristics of the studied MPA in that it was unable to promote increased stocks of all species. However, the greater abundance recorded in the studied MPA may be associated with better quality habitats more suitable to certain life history stages of some species and/or more heterogeneous habitats (García Charton and Pérez Ruzafa 1998). In this sense, habitat structure is an important factor structuring Wsh assemblages at diVerent spatial scales (García Charton et al. 2004), oVering resources such as food and/or shelter, and should be taken in account when a MPA is going to be located or designed. Mixed results were also obtained for species not targeted by Wshing which were, frequently small-bodied,
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Table 1 Values of protection eVect and signiWcance for each species meta-analysed Families
Species
EVect
Status
Belonidae Centracanthidae
Belone belone Spicara Xexuosa Spicara maena Spicara smaris Conger conger Pomadasys incisus Coris julis Labrus bergylta Labrus merula Labrus viridis Symphodus cinereu Symphodus doderleini Symphodus mediterraneus Symphodus ocellatus Symphodus roissali Symphodus rostratus Symphodus tinca Thalassoma pavo Dicentrarchus labrax Mugil sp. Mullus surmuletus Muraena helena Chromis chromis Sciaena umbra Scorpaena notata Scorpaena porcus Epinephelus aeneus Epinephelus costae Epinephelus marginatus Mycteroperca rubra Serranus cabrilla Serranus scriba Boops boops Dentex dentex Diplodus annularis Diplodus cervinus Diplodus puntazzo Diplodus sargus Diplodus vulgaris Lithognathus mormyrus Oblada melanura Pagellus acarne Pagellus erythrinus Pagrus pagrus Sarpa salpa Sparus aurata Spondyliosoma cantharus
1.087ns 2.83ns 4.19** 4.186** ¡0.808ns ¡1.26ns ¡1.8*** 1.12ns 2.64ns 0.04ns ¡0.23ns ¡0.07ns
By-catch Non target Non target Non target By-catch By-catch Non target By-catch By-catch By-catch Non target Non target
¡0.18ns
Non target
2.73*** ¡1.74** 0.09ns 0.29ns 5.73*** 2.54ns 0.085ns ¡3.13** 2.55ns 2.21*** 4.18*** ¡0.03ns ¡1.50ns 0.95ns 1.05ns 3.84**
Non target Non target Non target Non target Non target Target Target Target By-catch Non target By-catch Target Target Target Target Target
1.17ns ¡0.34ns 1.69ns 2.90*** 0.59ns 2.65*** 3.69ns 0.60ns 1.91*** 1.92*** ¡1.80ns
Target Target Target Non target Target Target Target Target Target Target Target
2.59*** ¡1.55ns ¡1.60ns ¡1.62ns 0.24ns ¡0.59ns ¡1.42ns
Non target Target Target Target Non target Target Target
Congridae Haemulidae Labridae
Moronidae Mugilidae Mullidae Muraenidae Pomacentridae Sciaenidae Scorpaenidae Serranidae
Sparidae
ns not signiWcant **P < 0.01, ***P < 0.001
fast-growing and highly fecund species. Spicara sp., Symphodus ocellatus, Thalassoma pavo, Chromis chromis, Boops boops and Oblada melanura would not be
expected to beneWt strongly from protection. However, they did indeed and were more abundant within the MPA since they could have found suitable habitat (Roberts and Ormond 1987; Jennings et al. 1996a, b; Chapman and Kramer 1999) or could obtain more trophic resources (Babcock et al. 1999; see Pinnegar et al. 2000 for a review). Furthermore, species like Coris julis and some Symphodus sp. responded negatively to protection, probably due to the increase of predatory species or negative interactions with other species as suggested Mosquera et al. (2000). The implementation of MPAs is not always successful in boosting Wsh populations. Some studies have reported failed or ambiguous eVects of protection, either by comparing only no-take areas versus open Wshed controls (e.g., Bell 1983; Roberts and Polunin 1993; Letourneur 1996; Tuya et al. 2006) or monitoring the protected Wsh assemblage over diVerent periods at both MPAs and control localities (e.g., Buxton and Smale 1989; Dufour et al. 1995; Edgar and Barrett 1999; LaMesa and Vacchi 1999; Francour 2000; Guidetti et al. 2005). We obtained a similar result with our data when the two only 3 year sampling periods were considered separately (Bayle-Sempere 1999; Forcada 2005), despite the fact that these studies applied the same kind of stratiWed, highly replicated experimental design. These negative Wndings can be due to diVerent causes. Firstly, data gathered by visual census on Wsh assemblages generally have very high variability, low precision, low power, (Samoilys and Carlos 2000) and usually lack the parametric assumptions such as normality. For this reason, detecting the eVects of protection in Wsh abundances is a complex problem. In addition, Wsh assemblages, like other ecological communities, are patchy, often simultaneously at several spatial and temporal scales (Dayton and Tegner 1984; Kotliar and Wiens 1990). This patchiness is the eVect of physical (e.g., habitat, climatic diVerences; Holbrook et al. 1997; García-Charton et al. 2004 and/or ecological factors (e.g., recruitment, competition, predation; Sale 1978; Hixon 1991; Booth and Brosnan 1995) that generate the above-mentioned high variability (Holbrook et al. 1994). Therefore, it is necessary to determine the suitable spatial and temporal scales (Levin 1992), to deWne proper sampling designs (García Charton and Pérez Ruzafa 1999) and eVort (Mouillot and Culioli 2002) to have suYcient ability to detect real changes due to protection in MPAs. However, the extent of variability is usually unknown prior to sampling and as such it is not considered in many studies (Rowley 1994). Other causes of the failure of MPAs to boost Wsh stocks could be ineVective enforcement (Jennings et al. 1996a, b) or incorrect selection of indicator parameters
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Fig. 2 Protection eVect on diVerent species. Reserve eVect value and bootstrapgenerated conWdence intervals are shown. See Table 1 for further details
(Pelletier et al. 2005). All of these factors can mask that eVect of protection make diYcult the task of distinguishing its eVect from other changes linked to indirect eVects, ecological variability or global changes (Menge 1997).
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It is remarkable that few studies assessing the eVects of protection are based on long-term sampling data; most studies include sampling results from 2 to 3 years. At short-term temporal scales (diurnal, daily and
Mar Biol (2007) 151:1153–1161 Table 2 Values of protection eVect and signiWcance for each family meta-analysed
ns not signiWcant **P < 0.01, ***P < 0.001
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Family
EVect
Belonidae Centracanthidae Congridae Haemulidae Labridae Moronidae Mugilidae Mullidae Sciaenidae Scorpaenidae Serranidae Sparidae
1.08ns 1.94*** ¡0.80ns 1.26ns 0.69*** 2.54ns 0.08ns ¡3.12** 4.18*** ¡0.17ns 1.259** 1.536***
Usually, monitoring programmes in MPAs are not carried out over long periods in a regular way (e.g., same temporal replication) and by the same observer. These constraints make data analyses diYcult, for example by ANOVA, due to the lack of balanced designs. Meta-analysis could be useful as a complementary technique to evaluate changes in MPAs, and can help solve the lack of suitable statistical power obtained in independent, short-term sampling programmes. We therefore conclude that species such as Boops boops, Diplodus annularis, Diplodus cervinus, Epinephelus marginatus, Epinephelus costae and Epinephelus aenus and families of Sciaenidae, Sparidae, Serranidae and Labridae can be used to detect the eVect of protection in Mediterranean MPAs. Our results reinforce the need for Wnancing long-term monitoring programmes in MPAs. Acknowledgments We wish to thank Club Náutico Santa Pola, Club Náutico de Altea and Club Náutico Javea for their facilities. Thanks are due to Dra. S. Revenga and The General Secretary of Marine Fisheries for providing facilities at the Tabarca Marine Reserve. The authors are very grateful to Dr. Julio Sánchez Meca, Universidad de Murcia, for his helpful advice on metaanalysis method. Thanks are due to Dr. Tim Dempster, SINTEF Norway, for reviewing the English version.
References
Fig. 3 Protection eVect on diVerent families. Reserve eVect value and bootstrap-generated conWdence intervals are shown. See Table 2 for further details
monthly), Wsh assemblage variability is higher than interannual variations (Thompson and Mapstone 2002). Most probably, changes due to protection were not detected due to the lack of long-term studies. Given the high variability of Wsh assemblages at multiple spatial and temporal scales, sampling programmes should include suitable spatial ranges and duration over time to obtain enough statistical power and minimize the noise in the ecological data. Our results show that a suitable period for monitoring programmes for MPAs in the Mediterranean Sea could be a minimum of 5–6 years, with sampling designs that consider replicated units of space and time in an hierarchical structure. This sampling procedure facilitates establishment of the best scales for monitoring (García-Charton and Pérez Ruzafa 1998). The data gathered in this manner will allow changes due to protection to be distinguished from those due to physical and/or ecological variations.
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