Spatial and Temporal Variability in Subtidal Macroinvertebrates Diversity Patterns in a Management and Exploitation Area for Benthic Resources (Meabrs)

Ocean & Coastal Management 93 (2014) 121e128

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Ocean & Coastal Management

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Spatial and temporal variability in subtidal macroinvertebrates diversity patterns in a management and exploitation area for benthic resources (MEABRs)

Pilar Molina a, F. Patricio Ojeda a, Marcela Aldana a,b,c, V.M. Pulgar d, * M. Roberto García-Huidobro c, José Pulgar b, a Pontiﬁcia Universidad Católica, Alameda 340, Santiago, Chile b Universidad Andres Bello, Departamento de Ecología & Biodiversidad, República 470, Santiago, Chile c Escuela de Pedagogía en Biología y Ciencias, Facultad de Ciencias de la Educación, Universidad Central de Chile, Santa Isabel 1278, Santiago, Chile d Center for Research in Obstetrics & Gynecology, Wake Forest School of Medicine and Biomedical Research Infrastructure Center, Winston-Salem State University, Winston-Salem, NC, USA article info abstract

Article history: Diversity and biological variability are key attributes to maintain a viable life system in the marine Available online 12 April 2014 benthic zone and this balance is heavily affected by human activities. In Chile, Management and Exploitation Areas for Benthic Resources (MEABRs) are coastal areas administrated by local ﬁshermen, which regulate the extraction of species of commercial of commercial importance (e.g. Concholepas concholepas, Fissurella spp. Loxechinus albus), key components of food webs. Both spatial and temporal impacts these species have on the structure and dynamics of the subtidal community are poorly un- derstood. In one of the oldest MEABRs of Chile we evaluated spatial and temporal effects of controlled extraction of commercial species on subtidal macro invertebrate’s diversity. Our results indicate that in a spatial scale MEABRs showed increased species richness, and important temporal changes in diversity and species composition from bivalves, ascidians and gastropods to cnidarians, sponges and bryozoans. We discuss possible mechanisms associated with the combined effects of ﬁshery management and predation by key species on temporal composition variation in the subtidal macro invertebrate assemblage in this regulated area. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction Botsford et al., 1997; Castilla, 1999, 2000; Dayton et al., 1995; Hockey and Bosman, 1986; Siegfried et al., 1985). Predation is one of the key processes governing structure of Marine Protected Areas (MPAs) have gained worldwide recog- natural communities (Duffy, 2002; Hairston et al., 1960). In recent nition as an important tool for biodiversity conservation and years, the threat of human activities as a top-down perturbation resource management (Allison et al., 1998; Fernández et al., 2000; that affects populations of large predators in natural ecosystems Lauck et al., 1998; Roberts, 1997), including protection of spawning has been fully recognized. Thus fishing has been demonstrated to stock, increase of recruitment rates, maintenance of the age and severely impact target species that in most cases are represented by size structures of stocks, and preservation of biodiversity. MPAs high trophic level predators (Fernández and Castilla, 2005; Jackson showed ability to protect habitats, conserve biodiversity and et al., 2001; Pauly et al., 1998; Myers and Worm, 2003; Sala et al., defend endangered stocks from overexploitation (Gell and Roberts, 1998; Steneck, 1998; Tegner and Dayton, 2000). The evidence in- 2003; Halpern and Warner, 2002; Halpern, 2003; Lubchenco et al., dicates that harvesting by humans can have dramatic effects on the 2003; Manríquez and Castilla, 2001; Shears and Babcock, 2003). structure and function of marine communities (Agardy, 1994; In this context, field evidence obtained from experimental ecological studies in Chile has been essential to demonstrate human impacts on inshore coastal ecosystems (e.g. Castilla and Durán, 1985; Castilla and Bustamante, 1989; Castilla, 1999, 2000; Moreno * Corresponding author. Tel.: þ56 2 6618416. et al., 1984). In MPAs of southern Chile, an increase in the density E-mail address: [email protected] (V.M. Pulgar). of keyhole limpets (Fissurella spp.) was detected during the first five http://dx.doi.org/10.1016/j.ocecoaman.2014.03.005 0964-5691/Ó 2014 Elsevier Ltd. All rights reserved. 122 P. Molina et al. / Ocean & Coastal Management 93 (2014) 121e128 years as consequence of human gatherers exclusion. This change Table 1 was coupled with a decline in the abundance of mid-intertidal Results of General Linear Model (Two-Way ANOVA) comparing the time spent filming the different types of subtidal habitats (boulders, crevices, walls, algae, and macroalgae (Moreno et al., 1984). In central Chile, human exclu- sand) in MEABRs and open-access area (sampled sector). df ¼ degrees of freedom, sion resulted in higher density of muricid gastropod Concholepas MS ¼ mean square, F ¼ F value, p ¼ probability value. concholepas, which in turn resulted in stronger predation of the Effect df MS Fp dominant intertidal mussel Perumytilus purpuratus. Primary space liberated by predation was colonized by barnacles, such as Sampled sector (SS) 1 0.76 0.012 0.91 Notochthamalus scabrosus and Jehlius cirratus, and several species of Habitat (H) 4 400.02 6.57 0.0001 SSxH 4 152.65 2.50 0.041 macroalgae (Castilla, 1999; Navarrete et al., 2010). Error 506 60.83 Management and Exploitation Areas for Benthic Resource (MEABRs) represent a tool for management and diversity protection developed in Chile (Castilla and Fernández, 1998; Gelcich et al., 2008; Manríquez and Castilla, 2001). The Chilean Under- comparisons were developed in the same sector, nearest to secretary of Fisheries assigns temporary permits quotes to legally CIMARQ (Center for Marine Investigation Quintay, Universidad registered artisanal fishing associations in defined geographical Andres Bello). In spatial evaluation, open-access area corresponds coastal areas, ranging from 50 to 300 ha of seabed. MEABRs are to a zone adjacent to MEABRs; and the temporal evaluation was created and assessed considering economically important benthic performed by comparing data obtained in 1989e1990 (just before species such as the carnivorous muricid gastropod Concholepas the establishment of MEABRs) under tenure of project FONDECYT concholepas (evaluated in w80% of MEABRs), key-hole limpets, 0349/1989 (F. P. Ojeda) with those obtained during 2008e2009 Fissurella spp. (w70%), and the red sea urchin Loxechinus albus (about 20 years after the establishment of MEABRs). In each of (w30%) (Castilla et al., 2007). The biological and economic suc- these areas, habitat characterization, density and richness of cesses of MEABRs policies have been proclaimed based on sub- macro-invertebrates were surveyed by SCUBA divers along subtidal stantial increases in abundances and sizes of managed species transects perpendicular to the coast. All diving activities were within MEABRs in comparison to open-access areas (Castilla and performed from a fisherman boat. Fernández, 1998; Castilla et al., 1998; Gelcich et al., 2008; Manríquez and Castilla, 2001; SUBPESCA, 2002). However, this 2.1. Habitat characterization economic success is associated to important dynamic and struc- tural changes in the marine ecosystem (Castilla, 2000; Gelcich Frequency of different habitats was estimated by filming for one et al., 2008), which would be even more relevant when the minute in 360 , every 10 m of depth in six subtidal transects within extent of MEABRs is considered. The 479 MEABRs in full operation of MEABRs and three subtidal transects in open-access area, at are spread over w1100km2 along the coast of Chile (SERNAPESCA, depths from 2 to 32 m. Habitat considered were: boulders, crevices, 2011), which exceeds the total area covered by no-take marine walls, algae, and sand. Data are expressed as habitat type by second. reserves, marine concessions with conservation purposes, multiple This methodology is a modification of nondestructive visual sam- use MPAs, and marine park (Fernández and Castilla, 2005). pling methods (Gelcich et al., 2008). MEABRs spread across the w4 000 km of coastal Chile and thus have the potential to scale-up the sustainable use of benthic re- 2.2. Spatial comparisons sources and also enhance marine conservation initiatives (Castilla, 2000; Castilla et al., 2007). The macro-invertebrates density and richness were recorded Despite MEABRs economic success, some objections have been along seven transects within of MEABRs and four transects in open- risen due to: a) the lack of baseline studies or information pre- access area, at depths from 2 to 30 m. They were set perpendicular vious to MEABRs started operation (Parnell et al., 2005; Sale et al., to the coast and were surveyed by autonomous divers. In each 2005), and specifically because b) only economically benthic transect and every 2 m, on average four quadrats (0.5 0.5 m) were species are included in the biological evaluation. These are surveyed. The position of transect and quadrants were randomly fundamental and critical points to validate MEABRs as manage- allocated. ment and biological conservation tools and finally determine the ecological change associated to protection (Castilla, 2000; Folke et al., 2005; Huitric, 2005). The aim of our study was: a) to compare community structure in a MEABRs versus an open- access area (non protected marine belt, with free access to marine resources), and b) to evaluate temporal ecological variations in community structure before versus twenty years after that the MEABRs started operation. We tested the hypothesis that MEABRs represents an important biological conservation tool, however dramatic changes in density, richness and species composition have occurred when comparing: a) temporal variability in diversity before versus after the establishment of MEABRs, and b) spatial variability between MEABRs versus open- access area.

2. Methods

This study was developed in the subtidal zone of a MEABRs located in central Chile (MEABR Quintay, 3311 0 S, 71410 W), one the oldest Chilean MEABRs (started operation in 1989). This Fig. 1. Average time spent ﬁlming the different habitat types registered in the subtidal MEABRs includes two sectors and both spatial and temporal of MEABRs and open-access area, at Quintay. Vertical bars indicate 1 standard error. P. Molina et al. / Ocean & Coastal Management 93 (2014) 121e128 123

2.3. Temporal comparisons respectively. Statistical significance was establishes at the 0.05 level. Density data was fourth-root-transformed and standardized This evaluation included the macro-invertebrates density and (between 0 and 1) to ensure that all species, abundant or rare, richness recorded along of subtidal transects at depths from 2 to contributed to similar way to the analysis. Additionally, multivar- 12 m of the same sector. Data from two transects sampled in 1989e iate analysis was performed based on gathered species’ presence 1990 and from eight transects sampled in 2008e2009 were versus absence data. We used the BrayeCurtis index of similarity. considered. In each transect and every two meters two quadrants Nonmetric Multidimensional Scaling (MDS) was used to display (0.5 0.5 m) was surveyed. invertebrate’s similarities between MEABRs and open-access area. For all evaluations (temporal and spatial), species richness and Differences in invertebrate community assemblages were tested a density were estimated from total number of species and in- priori for significance with the ANOSIM procedure (randomized dividuals per quadrant respectively. From these data, we estimated permutation test, Clarke and Warwick, 2001). Similarity analysis the macro-invertebrates diversity within quadrants with the (SIMPER) identified those species that accounted for the largest Shannon index. differences between MEABR and open-access area (Clarke and Warwick, 2001). 2.4. Data analysis 3. Results One-way and two-way ANOVAs (GLM) were used to compare the macro-invertebrates density, richness and species diversity 3.1. Habitat characterization variations, at spatial and temporal scale, inside and outside of MEABRs Quintay. Prior to all statistical analyses, data were The most common habitat registered in the subtidal Quintay examined for assumptions of normality and homogeneity of (either inside or outside the MEABRs) was algae. Boulders and variance using KolmogoroveSmirnov and Levene tests, walls were more frequent in the MEABRs, while that sand was

Table 2 Presence-absence of macro-invertebrates in MEABRs vs. open-access area, at Quintay. X ¼ presence.

Phyllum Clase Specie MEABRs Open-access area

Porifera Demospongiae Clionopsis platei (Thiele, 1905) X X Unidentified sponge 1 (Brown) X X Unidentified sponge 2 (Purple) X X Unidentified sponge 3 (Black) X Unidentified sponge 4 (White) X X Bryozoa Gymnolaemata Cellaria malvinensis (Busk, 1852) X Cnidaria Anthozoa Anthothoe chilensis (Lesson, 1830) X Phymactis papillosa (Lesson, 1830) X X Phymantea pluvia (Drayton, 1846) X X Anemonia alicemartinae (Sebens and Paine, 1979) X X Asteroidea Poraniopsis echinaster (Perrier, 1891) X Meyenaster gelatinosus (Meyen, 1834) X X Odontaster penicillatus (Philippi, 1870) X X Patiria chilensis (Lütken, 1859) X X Patiria obesa (Clark, 1910) X X Heliaster helianthus (Lamarck 1816) X X Stichaster striatus (Müller & Troschel, 1840) X X Holothuroidea Athyonidium chilensis (Semper, 1868) X Echinoidea Loxechinus albus (Molina, 1782) X Tetrapygus niger (Molina, 1782) X X Arthropoda Crustacea Taliepus dentatus (H. Milne Edwards, 1834) X X Taliepus marginatus (Bell, 1835) X X Rhynchocinetes typus (H. Milne Edwards, 1837) X X Pagurus edwardsi (Dana, 1852) X X Pagurus villosus (Nicolet, 1849) X Austromegabalnus psittacus (Molina 788) X X Homalaspis plana (H. Milne Edwards , 1834) X Cancer setosus (Molina, 1782) X Pygnogonida indet X Anisodoris fontaini (d’Orbigny, 1837) X X Mollusca Gastropoda Anisodoris rudberghi (Marcus & Marcus, 1967) X X Mitrella unifasciata (Sowerby 1832) X Prisogaster niger (Wood 1828) X Tegula atra (Lesson, 1830) X X Tegula quadricostata (Wood, 1828) X X Xanthochorus cassidiformis (Blainville 1832) X X Scurria spp. (Lesson 1830) X X Concholepas concholepas (Bruguiere, 1789) X Fissurella costata (Lesson 1830) X Fissurella cummingi (Reeve, 1849) X Fissurella latimarginata (Sowerby, 1835) X Acanthopleura echinata (Barnes 1824) X Polyplacophora Chiton magnificus (King & Broderip, 1832) X Chaetopleura peruviana (Lamarck 1819) X Tonicia chilensis (Frembly, 1827) X Total species 44 27 124 P. Molina et al. / Ocean & Coastal Management 93 (2014) 121e128 more common in open-access area. Crevices and algae were not Echinodermata (13.4%), 16 Crustacea (23.9%), 23 Gastropoda different between open-access area and MEABRs (Table 1 and (34.3%), 4 Bivalvia (5.9%) and 1 Urochordata (1.5%). Fig. 1). 3.3. Spatial comparisons: MEABRs vs. open-access area 3.2. Invertebrate taxonomic groups from the subtidal community of MEABRs Quintay Our results indicate higher diversity in MEABRs compared with open-access area (One way-anova F(1, 140) ¼ 6.88; p < 0.05, Fig. 2), We found a total of 67 invertebrate species (Tables 2 and 3). The moreover, MEABRs showed an increase of 63% in species as breakdown of these species is as follows: 5 Poryfera (7.5%), 1 compared with open-access areas (Chi-square test c2 ¼ 4.98, gl ¼ 1; Bryozoa (1.5%), 3 Cnidaria (4.5%), 5 Polyplacophora (7.5%), 9 p ¼ 0.02; Table 2). However, this increase in richness is not

Table 3 Presence-absence of macro-invertebrates before and after of MEABRs at Quintay. X ¼ presence.

Phyllum Class Specie Before MEABRs After MEABRs

Porifera Demospongiae Clionopsis platei (Thiele, 1905) X Unidentified sponge 1 (Brown) X Unidentified sponge 2 (Purple) X Unidentified sponge 3 (Black) X Bryozoa Gymnolaemata Cellaria malvinensis (Busk, 1852) X Cnidaria Cnidaria Anemonia alicemartinae (Sebens and Paine, 1979) X Phymactis papillosa (Lesson, 1830) X Anthothoe chilensis (Lesson, 1830) X Odontaster penicillatus (Philippi, 1870) X Echinodermata Asteroidea Stichaster striatus (Müller & Troschel, 1840) X Heliaster helianthus (Lamarck, 1816) X X Echinodermata Loxechinus albus (Molina, 1782) X X Tetrapygus niger (Molina, 1782) X X Holothuroidea Athyonidium chilensis (Semper, 1868) X Arthropoda Crustacea Taliepus dentatus (H. Milne Edwards , 1834) X Taliepus marginatus (Bell, 1835) X Anfipoda spp. X Cancer setosus (Molina 1782) X Homalaspis plana (H. Milne Edward, 1834) X Isopoda spp. X Liopetrolisthes mitra (Dana, 1852) X Rhynchocinetes typus (H. Milne Edwards , 1837) X Pagurus edwardsi (Dana, 1852) X Pagurus villosus (Nicolet, 1849) X Pagurus spp. X Austromegabalnus psittacus (Molina, 1788) X Balanus laevis (Bruguière, 1789) X Pisoides edwardsi (Fagetti, 1969) X Mollusca Gastropoda Collisella zebrina (Lesson, 1830) X Collisella atrata (Carpenter, 1857) X Concholepas concholepas (Bruguiere, 1789) X Crepipatella dilatata (Lamark, 1822) X Crassilabrum crassilabrum (Sowerby, 1834) X Fissurella costata (Lesson, 1830) X Fissurella cumingi (Reeve, 1849) X X Fissurella latimarginata (Sowerby, 1835) X X Fissurella máxima (Sowerby, 1835) X Fissurella crassa (Lamarck, 1822) X Fissurella oriens (Sowerby, 1835) X Mitrella unifasciata (Sowerby 1832) X X Prisogaster niger (Wood 1828) X X Tegula atra (Lesson, 1830) X X tegula quadricostata (Wood, 1828) X Xanthochorus cassidiformis (Blainville 1832) X Scurria spp. (Lesson, 1830) X Turritella spp. (Lamark, 1799) X Nassaria spp. (Röding, PF 1798) X Nucula spp. (Cuvier 1798) X Hiatella albus (Hunter, 1949) X Endodesma spp. (Ulrich, 1894) X Polyplacophora Acanthopleura echinata (Barnes, 1824) X Chiton magnificus (King and Broderip, 1832) X Chaetopleura peruviana (Lamarck, 1819) X Tonicia chilensis (Frembly, 1827) X Chiton commingsi (Frembly, 1827) X Bivalvia Brachidontes granulata (Hanley, 1843) X Semimytilus algosus (Gould, 1850) X Chordata Ascidiacea Pyura chilensis (Molina, 1782) X Total species 34 36 P. Molina et al. / Ocean & Coastal Management 93 (2014) 121e128 125

Fig. 3. Average density of sessile macroinvertebrates in MEABRs and open-access area, at Quintay. Vertical bars indicate 1 standard error.

(e.g. Brachidontes granulata and Semimytilus algosus) and barnacles (as Balanus laevis) before MEABRs was observed, whereas Porifera and Cnidaria species were predominant after MEABRs (Fig. 7A, Table 3). Analyses of mobile animals indicate a 96% of dissimilitude (ANOSIM R ¼ 0.85; p ¼ 0.001) with a greater contribution of Pri- sogaster niger and Tetrapygus niger before of MEABR and Tegula atra after of MEABRs (Fig. 7B).

3.5. Spatial and temporal comparisons Fig. 2. A) Diversity, and B) Richness per quadrant of marine macroinvertebrates species in MEABRs and open-access area, at Quintay. Vertical bars indicate 1 standard Comparisons that include spatial and temporal evaluation error. indicate a greater diversity in 1989e1990 than in 2008e2009, regardless of the protection of the area (whether open-access or protected area) (One-way anova F(2, 90) ¼ 16.44; p < 0.05, Fig. 8). sufficient to determine composition differences between open- access area versus MEABRs (sessile invertebrates stress ¼ 0.17, 4. Discussion mobile invertebrates stress ¼ 0.14). In general, in the subtidal of Quintay, sessile animals such as Our results support the hypothesis that important ecological Porifera and Bryozoa were the most abundant taxonomic groups changes have occurred at both spatial and temporal scales in (Table 4, Fig. 3). In MEABRs, mobile taxa such as Gastropoda and MEABRs Quintay. Diversity, total richness and density of main Echinodermata, showed higher density compared with open- taxonomic groups and commercial species, were higher in MEABRs, access area (Table 5, Fig. 4). Moreover, in MEABRs we found whereas a greater diversity of sessile species was found before the higher density of commercial species (e.g. Fissurella spp., Con- establishment of MEABRs. cholepas concholepas y Loxechinus albus) compared with open- The complexity of habitat structure has been largely recognized access areas (Table 6, Fig. 5). as one of the factors affecting diversity, distribution as well as abundance of several taxa including rocky reef fishes (Bodkin,1988; 3.4. Temporal comparisons: before vs after of MEABRs Dayton, 1985; Ebeling et al., 1980; Ebeling and Hixon, 1991; Quast, 1968). In general, more structured habitats (i.e. presence of artificial A similar total number of species was found when comparing reef, kelp forest) show higher density and species richness (Carr, before vs. after the establishment of MEABRs (Table 3). However, 1991, 1994; Carr and Hixon, 1995; Rojas and Ojeda, 2010). In higher species richness and diversity of macro-invertebrates at temperate zones, such as the coast of Chile, habitat complexity has depths of 6e12 m, was observed before the establishment of been associated with Lessonia trabeculta kelp forest, because MEABRs (Table 7 and Fig. 6A, B). Composition analysis for sessile greater invertebrates density and greater richness of reef-fish animals, showed a 99% of temporal dissimilitude (ANOSIM R ¼ 0.68, determine high levels of prey availability, particularly to species p < 0.05), with two distinct predominant groups when comparing inhabiting the kelp understory, and apparently support a more before vs. after MEABRs. A higher contribution of Bivalve species complex trophic organization (Angel and Ojeda, 2001; Choat and Ayling, 1987). Our results indicate similar frequencies of Lessonia

Table 4 Results of General Linear Model (two-way ANOVA) comparing the density of Table 5 different taxa of sessile macroinvertebrates in MEABRs and open access area Results of General Linear Model (Two-Way ANOVA) comparing the density of (sampled sector). df ¼ degrees of freedom, MS ¼ mean square F ¼ F value, different taxa of mobile macroinvertebrates in MEABRs and open-access area. p ¼ probability value. df ¼ degrees of freedom, MS ¼ mean square, F ¼ F value, p ¼ probability value.

Effect df MS FP Effect df MS Fp

Sampled sector (SS) 1 1.69 0.014 0.90 Sampled sector (SS) 1 13.53 3.90 0.048 Taxa (T) 4 2 489.97 20.67 0.0001 Taxa (T) 3 17.68 4.27 0.005 SSxT 4 73.53 0.61 0.65 SSxT 3 7.43 1.79 0.14 Error 2 612 120.4 Error 9 855 4.14 126 P. Molina et al. / Ocean & Coastal Management 93 (2014) 121e128

Table 7 Results of General Linear Model (two-way ANOVA) comparing richness and diversity of macroinvertebrates, between different sampled depth (0e5m,6e8 m, and 9e12 m) and times (before vs after MEABRs installation). df ¼ degrees of freedom, MS ¼ mean square, F ¼ F value, p ¼ probability value.

Effect df MS Fp

Richness Sampled Time (ST) 1 987.67 411.12 0.0001 Depth (D) 2 95.08 39.57 0.0001 STxD 2 89.65 37.32 0.0001 Error 143 2.40 Diversity Sampled Time (ST) 1 4.14 45.69 0.0001 Depth (D) 2 0.52 5.83 0.006 STxD 2 0.92 10.17 0.0001 Error 36 0.09

Fig. 4. Average density of mobile macroinvertebrates in MEABRs and open access areas, at Quintay. Vertical bars indicate 1 standard error. evidence is in agreement with other studies showing population enhancement of target-managed invertebrates inside MEABRs (Fernández and Castilla et al., 1998; Gelcich et al., 2008). Table 6 Scarce information exists regarding the biodiversity quantifi- Results of General Linear Model (Two-Way ANOVA) comparing the density of in- cation prior to the operation of any conservation tool (MPAs or vertebrates commercial species (Loxechunus albus, Concholepas concholepas, Fissur- MEABRs). Our results showed greater diversity before MEABRs ella spp) in MEABRs and open-access area. df ¼ degrees of freedom, MS ¼ mean square, F ¼ F value, p ¼ probability value. Quintay, associated with important temporal changes in invertebrate’s composition. In other localities in Chile, temporal axis Effect df MS Fp is a relevant factor to consider when MEABRs success is evaluated Sampled sector (SS) 1 39.54 4.57 0.036 (Moreno, 1986; Stotz and Pérez, 1992; Stotz, 1997). Our evidences Species (S) 2 6.31 0.73 0.48 indicate that complete taxonomic groups as bivalves, ascidians and SSxS 2 6.65 0.77 0.46 Error 53 8.63 some gastropoda species have disappeared from the subtidal of Quintay. These taxonomic groups are indicated as food items of highly mobile subtidal predators such as fishes (Angel and Ojeda, 2001), echinoderms belonging to the Asteroidea class such as trabeculata kelp forest in MEABRs compared with open-access area. Meyenaster gelatinosus (Dayton et al., 1977) and Heliaster heliantus Thus, if habitat structure is important in explaining the greater (Paine et al., 1985), and finally C. concholepas (Castilla, 1999; macro-invertebrate diversity in MEABRs, it should be associated Moreno et al., 1986), the principal protected species in all with the presence of boulders and walls. MEABRs (see Castilla et al., 2007). Interestingly, the released habitat Boulders and walls would be especially important for sessile or those who need substrate, but the abundance of sessile species was similar between MEABRs and the open access area. Our study shows that Echinodermata and Gastropoda were the taxa that showed higher species diversity and density in the MEABRs compared to the open access area, suggesting the effect of protection on commercial species such as echinoderm Loxechinus albus, and gastropods Concholepas concholepas and Fissurrella spp. Our

Fig. 5. Average density of commercial species of macroinvertebrates in MEABRs and open access areas, at Quintay. Vertical bars indicate 1 standard error. L. albus ¼ Loxechinus albus; F. latimarginata ¼ Fissurella latimarginata, F. cummingi ¼ Fissurella cummingi, F. maxima ¼ Fissurella maxima, Fig. 6. A) Diversity, and B) Richness per quadrant of marine macroinvertebrates spe- C. concholepas ¼ Concholepas concholepas. cies before vs. after of MEABRs Quintay. Vertical bars indicate 1 standard error. P. Molina et al. / Ocean & Coastal Management 93 (2014) 121e128 127

add-on effects for species that are not the focus of current management policies (Castilla, 1999; Gelcich et al., 2008; Moreno et al., 1984). Moreover, although a decrease in richness and diversity per quadrant in the last twenty years has been observed in the area, our data suggest that MEABRs strengthened total species richness. Our evidence represents the ﬁrst comparison of temporal changes in diversity (before vesus after) of any conservation or management tool. We propose that temporal changes in species composition and density, ideally from data bases obtained before to operation of MEABRs, must be considered in the analysis of MEABRs success. In addition, periodic quantiﬁcations in MEABRs should include not only target-managed species but the whole coastal community.

5. Conclusions

We reported important temporal and spatial ecological changes mediated by the installation of MEABRs Quintay. A greater species diversity before MEABRs was associated with temporal changes in invertebrate’s composition. Complete taxonomic groups such as bivalves, ascidians and some gastropoda species have disappeared from the subtidal of Quintay. These taxonomic groups are indicated as food items of highly mobile subtidal predators such as fishes, Asteroidea species and C. concholepas, the main protected species in all MEABRs. Other important findings indicated that MEABRs showed almost Fig. 7. Results of multidimensional scaling analysis (MDS) for A) mobile, and B) sessile twice as many species than open-access areas, supporting the macroinvertebrates before and after of MEABRs Quintay as indicated. MEABRs key role in providing conservation add-on effects for species that are not the focus of current management policies. has been occupied by cnidarians, sponges, and bryozoans, revealing a successional change mediated by the protection of commercial Acknowledgments species in MEABRs (Table 3). The temporal changes in species composition observed in the subtidal zone of Quintay, from bi- This study was funded by grants DI0508, DI1710R, DI-16-12/R to valves, ascidians and gastropods to cnidarians, sponges and bryo- J. Pulgar, Universidad Andres Bello. We thank to J. Espinoza, S. zoans (Table 3 and Fig. 7), may well be explained by the fact that Benitez and A. Delgadillo for their help in the field. these latter groups are not prey of the most important predators of these systems such as fishes (Angel and Ojeda, 2001; Aldana et al., References 2002). The high density of predatory fishes observed within marine reserves (Micheli et al., 2004), as well as in other Chilean MEABRs Agardy, T., 1994. The Science of Conservation in the Coastal Zone: new Insight on how to Design, Implement, and Monitor Marine Protected Areas. A marine (Gelcich et al., 2008) clearly support our contention. conservation and development report. IUCN, Gland, Switzerland, VIII 72 pp. Understanding how the protection of key species in food webs Aldana, M., Pulgar, J., Ogalde, F., Ojeda, F.P., 2002. Morphometric and parasitogical may affect community’s dynamic and structure is fundamental for evidence for ontogenetic and geographic dietary shifts in intertidal fishes. Bull. e the maintenance and success of MEABRs. At Quintay, MEABRs Mar. Sci. 70 (1), 55 74. Allison, G., Lubchenco, J., Carr, M., 1998. Marine reserves are necessary but not showed almost twice as many species than open-access area sufficient for marine conservation. Ecol. Appl. 8, S79eS92. (Table 2), with open-access area species representing a composi- Angel, A., Ojeda, F.P., 2001. Structure and trophic organization of subtidal fish as- tional subset of those found in MEABR. In this sense, our evidence semblages on the northern Chilean coast: the effect of habitat complexity. Mar. Ecol. Prog. Ser. 217, 81e91. supports MEABRs in terms of providing important conservation Bodkin, J.L., 1988. Effects of kelp forest removal on associated fish assemblages in central California. J. Exp. Mar. Biol. Ecol. 117, 227e238. Botsford, L.W., Castilla, J.C., Peterson, C.H., 1997. The management of fisheries and marine ecosystems. Science 277, 509e515. Carr, M.H., 1991. Habitat selection and recruitment of an assemblage of temperate zone reef fishes. J. Exp. Mar. Biol. Ecol. 146, 113e137. Carr, M.H., 1994. Effects of macroalgal dynamics on recruitment of a temperate reef fish. Ecology 75, 1320e1333. Carr, M.H., Hixon, M., 1995. Predation effects on early post-settlement survivorship of coral reef fishes. Mar. Ecol. Prog. Ser. 124, 31e42. Castilla, J.C., Durán, L., 1985. Human exclusion from the rocky intertidal zone of Central Chile: the effects on Concholepas concholepas (Gastropoda). Oikos 45, 391e399. Castilla, J.C., Bustamante, R.H., 1989. Human exclusion from rocky intertidal of Las Cruces, Central Chile: effects on Durvillaea Antarctica (Phaeophyta, Durvil- leales). Mar. Ecol. Prog. Ser. 50, 203e214. Castilla, J.C., Fernández, M., 1998. Small-scale benthic fisheries in Chile: on comanagement and sustainable use of benthic invertebrates. Ecol. Appl. 8 (1), S124eS132. Castilla, J.C., Manríquez, P., Alvarado, J., Rosson, A., Pino, C., Espóz, C., Soto, R., Oliva, D., Defeo, O., 1998. Artisanal Caletas: as units of production and co- managers of benthic invertebrates in Chile. Can. J. Fish. Aquat. Sci. 125, 407e Fig. 8. Diversity of macroinvertebrates per quadrant in samples taken before and after 413 (special publication). of MEABRs, and open-access area, at Quintay as indicated. Bars indicate 1 standard Castilla, J.C., 1999. Coastal marine communities: trends and perspectives from hu- error. man exclusion experiments. Trends. Ecol. Evol. 14, 280e283. 128 P. Molina et al. / Ocean & Coastal Management 93 (2014) 121e128

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