INTRODUCTIONTop

Factors that promote variations in biodiversity are highly important considering the impact that diversity has on ecosystem functioning (Hooper et al. 2012Hooper D.U., Adair E.C., Cardinale B.J., et al. 2012. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486: 105-109.). While all species modify habitats, it is anthropogenic modifications that are frequently associated with diversity loss, resource exploitation, and habitat fragmentation (Chapin III et al. 2000Chapin III F., Zavaleta E., Eviner V., et al. 2000. Consequences of changing biodiversity. Nature 405: 234-242.). Indeed, oceans worldwide are facing increased threats, including resource overexploitation, habitat degradation and destruction, pollution, and climate change (Halpern et al. 2008Halpern B.S., Walbridge S., Selkoe K.A., et al. 2008. A global map of human impact on marine ecosytems. Nature 319: 948-952.). These stressors influence population declines of commercially/culturally important species, altered community structures and compromised ecosystem functioning.

The conservation and sustainable-use mechanisms for marine resources include Marine Protected Areas and no-take zones (Agardy 2003Agardy T. 2003. Dangerous targets? Unresolved issues and ideological clashes around marine protected areas. Aquat. Conserv. 13: 353-367.). In Chile, Management and Exploitation Areas for Benthic Resources (MEABRs) are another sustainable-use and nearshore marine resource management strategy (see references in Gelcich et al. 2008Gelcich S., Godoy N., Prado L., et al. 2008. Add-on conservation benefits of marine territorial user rights fishery policies in central Chile. Ecol. Appl. 18: 273-281.). Notably, MEABRs complement the biodiversity objectives of fully protected areas by providing important conservation add-on effects for species outside of management policies (Aldana et al. 2014Aldana M., Pulgar J.M., Orellana N., et al. 2014. Increased parasitism of limpets by a trematode metacercaria in fisheries management areas of central Chile: effects on host growth and reproduction. Ecohealth 11: 215-226., Molina et al. 2014Molina P., Ojeda P., Aldana M., et al. 2014. Spatial and temporal variability in subtidal macroinvertebrates diversity patterns in a management and exploitation area for benthic resources (MEABRs). Ocean. Coast. Manage. 93: 121-128.).

Due to dense, diverse organism assemblages, the rocky intertidal zone is an ideal “natural laboratory” for understanding the factors that govern intertidal community organization, a topic of numerous studies. Steep environmental gradients, rapid organism turnover, and abundant sessile and slow-moving organisms grant this zone experimental tractability (Paine 1994Paine R.T. 1994. Marine rocky shores and community ecology: An experimentalist’s perspective. Ecology Institute, Oldendorf, Luhe, Germany.). Furthermore, the physical gradients, spatial heterogeneity, competition, predation/grazing, disturbance, larval dynamics, and recruitment variability of the rocky shore system are ecological interactions and processes that influence community structure and species composition (see references in Paine 1994Paine R.T. 1994. Marine rocky shores and community ecology: An experimentalist’s perspective. Ecology Institute, Oldendorf, Luhe, Germany.).

Understanding community dynamics requires a basic knowledge of community interactions between member species, which define community structure and determine how effects are transmitted between species. For instance, predators can directly (e.g. by consumption) and indirectly (e.g. through the trophic cascade) affect community structure (Paine 1966Paine R.T. 1966. Food Web Complexity and Species Diversity. Am. Nat. 100: 65-75., Werner and Peacor 2003Werner E.E., Peacor S.D. 2003. A review of trait-mediated indirect interactions in ecological communities. Ecology 84: 1803-1100., García-Huidobro et al. 2015García-Huidobro M.R., Pulgar J., Pulgar V.M., et al. 2015. Impact of predators and resource abundance on the physiological traits of Fissurella crassa (Argeogastropoda). Hidrobiologica 25: 165-173.). Therefore, all ecological relationships in the community must be considered to gain full understanding. Likewise, marine resource exploitation can directly and indirectly modify rocky intertidal community structure and functioning (Steneck 1998Steneck R.S. 1998. Human influences on coastal ecosystems: Does overfishing create trophic cascades? Trends Ecol. Evol. 13: 429-430., see references in Castilla et al. 2007Castilla J.C., Gelcich S., Defeo O. 2007. Successes, lessons, and projections from experience in marine benthic invertebrate artisanal fisheries in Chile. In: McClanahan T., Castilla J.C. (eds), Fisheries Management: Progress toward Sustainability. Blackwell, Oxford, UK, pp. 25-42.). Consequently, in communities where predation is an important structuring process and some predator species are commercially exploited, appropriate conservation plans and resource management should be established by evaluating different predator species (Castilla and Durán 1985Castilla J.C., Durán L.R. 1985. Human exclusion from the rocky intertidal zone of central Chile: the effects on Concholepas concholepas (Gastropoda). Oikos 45: 391-399.).

Predator impacts on intertidal community structure have been studied for rocky platforms, but intertidal boulder fields—a habitat with a greater extension and heterogeneity—have not yet been considered (Bertness et al. 2001Bertness M.D., Gaines S.D., Hay M.E. 2001. Marine community ecology. Sinauer Associates.). Species living on and under boulders have greater small-scale spatial variabilities than rocky platform species due to discrete habitat patches separated from other boulders by distinct habit types, such as sand, mud, or smaller rocks (Chapman 2002aChapman M.G. 2002a. Patterns of spatial and temporal variation of macrofauna under boulders in a sheltered boulder field. Austral. Ecol. 27: 211-228., bChapman M.G. 2002b. Early colonization of shallow subtidal boulders in two habitats. J. Exp. Mar. Biol. Ecol. 275: 95-116.). Many species living under boulders do not inhabit the surrounding habitats. Furthermore, boulder-inhabiting animals and algae often vary between shorelines due to variations in boulder types and sizes (McGuinness and Underwood 1986McGuinness K.A., Underwood A.J. 1986. Habitat structure and the nature of communities on intertidal boulders. J. Exp. Mar. Biol. Ecol. 104: 97-123.) and/or to varied wave-actions and disturbances (Sousa 1979aSousa W.P. 1979a. Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecol. Monograph. 49: 227-254., bSousa W.P. 1979b. Disturbance in marine intertidal boulder fields: The nonequilibrium maintenance of species diversity. Ecology 60: 1225-1239., McGuinness 1987McGuinness K.A. 1987. Disturbance and organisms on boulders. I. Patterns in the environment and the community. Oecologia 71: 409-419.). Additionally, most intertidal boulder field studies focus on relatively exposed open-coast shores, where wave-actions and sand burial (processes that directly influence organisms) determine biological dynamics (Chapman and Underwood 1996Chapman M.G., Underwood A.J. 1996. Experiments on effects of sampling on biota under intertidal and shallow subtidal boulders. J. Exp. Mar. Biol. 207: 103-126., Smith and Otway 1997Smith K.A., Otway N.M. 1997. Spatial and temporal patterns in abundance and the effects of disturbance on under-boulder chitons. Molluscan. Res. 18: 43-57., Le Hir and Hily 2005Le Hir M., Hily C. 2005. Macrofaunal diversity and habitat structure in intertidal boulder fields. Biodivers. Conserv. 14: 233-250.).

Rocky platforms have decreased diversity due to space monopolization by highly competitive species (Lubchenco and Menge 1978Lubchenco J., Menge B.A. 1978. Community development and persistence in a low rocky intertidal zone. Ecol. Monograph. 48: 67-94., Sousa 1984Sousa W.P. 1984. Intertidal mosaics: Patch size, propagule availability, and spatial variable patterns of succession. Ecology 65: 1918-1935.). In contrast, boulder movements involve a frequent renewal of free space, thereby facilitating species coexistence (i.e. the intermediate perturbation hypothesis, Sousa 1979aSousa W.P. 1979a. Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecol. Monograph. 49: 227-254., bSousa W.P. 1979b. Disturbance in marine intertidal boulder fields: The nonequilibrium maintenance of species diversity. Ecology 60: 1225-1239.). High vulnerability to disturbances and habitat loss makes boulders analogous to habitat-forming biota, and, depending on the disturbance regime, boulders may be denuded (Lieberman et al. 1979Lieberman M., John D.M., Lieberman D. 1979. Ecology of subtidal algae on seasonally devastated cobble substrates off Ghana. Ecology 60: 1151-1161.), support few opportunistic species (Littler and Littler 1984Littler M.M., Littler D.S. 1984. Relationships between macroalgal functional form groups and substrata stability in a subtropical rocky-intertidal system. J. Exp. Mar. Biol. Ecol. 74: 13-34.) or support diverse assemblages (Sousa 1979aSousa W.P. 1979a. Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecol. Monograph. 49: 227-254., bSousa W.P. 1979b. Disturbance in marine intertidal boulder fields: The nonequilibrium maintenance of species diversity. Ecology 60: 1225-1239., McGuinness 1987McGuinness K.A. 1987. Disturbance and organisms on boulders. I. Patterns in the environment and the community. Oecologia 71: 409-419.). Boulder species are often patchily distributed among and within different fields, with variation mostly existing on individual boulders or among patches than between sites or locations (Chapman 2005Chapman M.G. 2005. Molluscs and echinoderms under boulders: Tests of generality of patterns of occurrence. J. Exp. Mar. Biol. Ecol. 325: 65-83., 2012Chapman M.G. 2012. Restoring intertidal boulder-fields as habitat for “specialist” and “generalist” animals. Restor. Ecol. 20: 277-285.). Considering this variability, in addition to the many characteristics that promote this variability (e.g. spatial heterogeneity, different rock types, wave exposure and boulder size) and the spatial coastal extension of boulder fields, evaluating the predation and anthropogenic impacts on community structure of this habitat becomes all the more important. This aspect has been poorly addressed in the literature, making the development of ecology-based resource management plans more difficult.

Therefore, the aims of this study were (1) to describe and quantify boulder field community structure; and (2) to assess boulder field community dynamics by proposing possible boulder field food webs, taking into consideration predatory and anthropogenic impacts. In the two zones were assessed, a MEABR and an open-access area (OAA), we expected to find notable differences in community structure and trophic web between the evaluated boulder fields.

MATERIALS AND METHODSTop

Sampling

Between the summers of 2008 and 2009, two intertidal zones from Quintay, Chile (33°11′S, 71°1′W) were sampled. The study zones were Playa Chica and Playa Grande, which are respectively a MEABR and an OAA. These study zones represent lower and higher anthropogenic impact scenarios, respectively (Castilla et al. 2007Castilla J.C., Gelcich S., Defeo O. 2007. Successes, lessons, and projections from experience in marine benthic invertebrate artisanal fisheries in Chile. In: McClanahan T., Castilla J.C. (eds), Fisheries Management: Progress toward Sustainability. Blackwell, Oxford, UK, pp. 25-42., Gelcich et al. 2008Gelcich S., Godoy N., Prado L., et al. 2008. Add-on conservation benefits of marine territorial user rights fishery policies in central Chile. Ecol. Appl. 18: 273-281., Molina et al. 2014Molina P., Ojeda P., Aldana M., et al. 2014. Spatial and temporal variability in subtidal macroinvertebrates diversity patterns in a management and exploitation area for benthic resources (MEABRs). Ocean. Coast. Manage. 93: 121-128.). Two sites that showed similar wave exposure and rock and boulder presence were selected per zone. The effect of predators on community structure was evaluated by comparing randomly collected rocks at the study site with treatment rocks maintained within cages that excluded predators (Menge 1976Menge B. 1976. Organization of the New England rocky intertidal communities: role of predation competition, and environmental heterogeneity. Ecol. Monogr. 46: 355-393.).

Specifically, three exclusion cages (20×30×30 cm) were installed at each site and at similar low-intertidal levels. All cages had an aluminium frame covered with wire mesh (10 mm) that was treated with anti-fouling and anti-oxidant paint (see Ojeda and Muñoz 1999Ojeda F.P., Muñoz A. 1999. Feeding selectivity of the herbivorous fish Scartichthys viridis: Effects on macroalgal community structure in a temperate rocky intertidal coastal zone. Mar. Ecol. Progr. Ser. 184: 219-229.). Six rocks (≈15 cm in diameter each) per cage were randomly selected from the same sampling site and placed within each cage. All exclusion cages were sampled monthly for one year, with the exception of some winter months due to adverse climatic conditions. For sampling, the six rocks within each exclusion cage, as well as six rocks outside each exclusion cage (controls), were collected. The collected rocks were placed in individual plastic bags, labelled with the sampling site and date, and transported to the laboratory for subsequent analysis. The rocks taken from inside the exclusion cages were replaced each month after sampling with similar rocks from each sampling site. A control cage was not used as it was impossible to anchor this structure in the boulder habitats.

In the laboratory, the sampled rocks were analysed using 5×5 cm quadrants divided into 25 sub-quadrants (1 cm each) (see Navarrete and Castilla 1990Navarrete S.A., Castilla J.C. 1990. Barnacle walls as mediators of intertidal mussel recruitment: effects of patch size on the utilization of space. Mar. Ecol. Prog. Ser. 68: 113-119.). Invertebrates and algae were classified and counted (number and coverage, respectively) under an Olympus CX31 stereomicroscope. Using the obtained data, the richness and diversity of each site were estimated. Specific richness (S) was established as the total number of species found for each rock sample, and diversity was estimated using the Shannon-Weaver Index.

Trophic web representation

The representation of trophic webs for the boulder fields of Quintay was supported by predator-prey relationships described in the literature (Paine 1966Paine R.T. 1966. Food Web Complexity and Species Diversity. Am. Nat. 100: 65-75., Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215., Angel and Ojeda 2001Angel A., Ojeda F.P. 2001. Structure and trophic organization of subtidal fish assemblages on the northern Chilean coast: the effect of habitat complexity. Mar. Ecol. Prog. Ser. 217: 81-91.). Using the collected data, species were grouped according to trophic status. This enabled an approximation of an overall trophic web (frames) that included all of the potential predators and respective prey in intertidal boulder fields, regardless of the sampling zone (see Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215., Angel and Ojeda 2001Angel A., Ojeda F.P. 2001. Structure and trophic organization of subtidal fish assemblages on the northern Chilean coast: the effect of habitat complexity. Mar. Ecol. Prog. Ser. 217: 81-91.).

Statistical analyses

Spatial variations in richness, density and diversity were assessed using two-way ANOVA (General Linear Models, GLM) to test for differences between study zones (MEABR and OAA) and between treatments (inside and outside exclusion cages). The study zone and treatment were considered fixed factors as interest was focused on the differences inside and outside exclusion cages and between the study zones. Insofar as these zones were inside and outside a MEABR, conclusions were limited to these levels (Bennington and Thayne 1994Bennington C.C., Thayne W.V. 1994. Use and misuse of mixed model analysis of variance in ecological studies. Ecology 75: 717-722.). Prior to GLM analysis, normal distribution was verified and an a posteriori Tukey analysis was performed to determine differences between factor levels.

Multivariate analysis was based on density data for collected mobile and sessile species. Density data were fourth-root-transformed and standardized (between 0 and 1) to ensure that all species, abundant or rare, contributed similarly to the analysis. The Bray-Curtis index of similarity was used. Nonmetric multidimensional scaling (MDS) was used to display the similarities of mobile and sessile species between study zones (MEABR and OAA) and between treatments (inside and outside exclusion cages). Differences in mobile and sessile community assemblages were tested a priori for significance with the ANOSIM procedure (randomized permutation test; Clarke and Warwick 2001Clarke K.R., Warwick R.M. 2001. A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar. Ecol. Prog. Ser. 216: 265-278.). Similarity analysis (SIMPER) identified those species that accounted for the largest differences between study zones (MEABR and OAA) and between treatments (inside and outside exclusion cages) (Clarke and Warwick 2001Clarke K.R., Warwick R.M. 2001. A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar. Ecol. Prog. Ser. 216: 265-278.).

Significance was established at P<0.05. For analyses concerning descriptors of community structure, the STATISTICA 7.0 (StatSoft.Inc. 2004) and PRIMER 5.0 (PRIMER-E Ltd) statistical software were used.

RESULTSTop

Recorded taxa

A total of 67 taxa were recorded, 27 of them corresponding to algae and 40 to invertebrates (Table 1). In the MEABR, 46 were recorded, 17 of them corresponding to algae and 29 to invertebrates (Table 1). In the OAA, 51 species were recorded, 24 of them corresponding to algae and 27 to invertebrates (Table 1). Mollusca and Rhodophyta were the most abundant taxonomic groups in both study zones.

Community structure of intertidal boulder fields

Analysis of invertebrates revealed greater species richness and density inside than outside exclusion cages (Table 2, Fig. 1A, B). Additionally, inside the exclusion cages, density was higher in the MEABR (posterior Tukey test P<0.05, Fig. 1B). However, invertebrate diversity was higher in the OAA (Table 2, Fig. 1C).

Algae analysis indicated that inside exclusion cages, richness and diversity were greater in the OAA than in the MEABR (Table 2, posterior Tukey test P<0.05; Fig. 2A, C). In terms of algal density, the MEABR showed higher density outside than inside exclusion cages (Table 2, posterior Tukey test P<0.05; Fig. 2B), whereas in the OAA no differences in density were found (posterior Tukey test P>0.05, Fig. 2B).

Regarding species composition, no differences were found between study zones (MEABR and OAA) or inside vs outside exclusion cages for either mobile or sessile species.

Trophic web for Playa Chica (MEABR)

The carnivorous predators registered in the MEABR were Actiniaria (Actinia spp., Phymactis clematis and Phymanthea pluvia) and Polycladida (Tythosoceros inca) (Table 1). Herbivorous species included amphipods (Amphipoda spp.), herbivorous decapods (Taliepus dentatus), isopods (Isopoda spp.), gastropods (Austrolittorina peruviana, Austrolittorina araucana, Fissurella spp., Mitrella spp., Prisogaster niger, Scurria ceciliana and Tegula euryomphala), and chitonids (Chiton cumingsi, Chiton spp. and Chiton latus). These herbivores prey on the benthic algae group found in the MEABR (Blidingia spp., Chaetomorpha spp., Codium dimorphum, Ulva spp., Colpomenia spp., Ahnfeltiopsis spp., Centroceras clavulatum, Corallina officinalis chilensis, Erythrotrichia spp., Lithothamnium spp., Mazzaella spp., Mazzaella membranacea, Mesophyllum spp., Polysiphonia mollis, Polysiphonia paniculata, Rhodymenia spp. and Rhodymenia coralline) (Fig. 3A, Table 1). Filter feeders recorded in the MEABR included mobile annelids (Pseudonereis gallapagensis), sessile annelids (Spirorbis spp.), bryozoa (Bryozoa spp.), cirripedes (Jehlius cirratus), copepods (Copepoda spp.), filtering decapods (Allopetrolisthes angulosus, Petrolisthes granulosus, Petrolisthes tuberculosus, Petrolisthes violaceus and Pisoides edwardsii) and Mytilidae (Perumytilus purpuratus and Semimytilus algosus) (Fig. 3A, Table 1).

Trophic web for Playa Grande (OAA)

Three carnivorous predator groups were recorded for the OAA: Asterozoa (Patiria chilensis and Ophiactis kroyeri), Actiniaria (Actinia spp. and Anemonia alicemartinae) and Polycladida (T. inca) (Fig. 3B, Table 1). Among herbivorous species were amphipods (Amphipoda spp.), isopods (Isopoda spp.), Echinoidea (Tetrapygus niger), gastropods (A. peruviana, Mitrella spp., P. niger, S. ceciliana, Tegula euryomphala, T. luctuosa and Turritella cingulata) and chitonids (Chiton cumingsi, Ch. latus and Tonicia disjuncta). The observed benthic algae group for the OAA included Blidingia spp., Chaetomorpha spp., C. dimorphum, Ulva spp., Adenocystis utricularis, Glossophora kunthii, Sphacelaria spp., Ahnfeltiopsis spp., Anisocladella pacifica, C. clavulatum, Chondria spp., C. officinalis chilensis, Erythrotrichia spp., Gelidium spp., Gelidium lingulatum, Lithothamnium spp., Mazzaella spp., M. membranacea, Mesophyllum spp., Nothogenia fastigiata, Porphyra spp., Rhodymenia spp., Rhodymenia corallina and Schottera nicaeensis (Fig. 3B, Table 1). Filter feeder species included Bryozoa (Bryozoa spp.), Veneroida (Protothaca thaca), Mytilidae (P. purpuratus and S. algosus), cirripedes (Balanus flosculus, Balanus laevis and J. cirratus) and sessile annelids (Phragmatopoma spp. and Spirorbis spp.).

DISCUSSIONTop

Species composition, richness, density and diversity

The species composition of the Quintay boulder fields showed patterns similar to those from other reported intertidal zones, such as platforms (Alveal 1971Alveal K. 1971. El ambiente costero de Montemar y su expresión biológica. Rev. Biol. Mar. Oceanogr. 14: 85–119., Santelices et al. 1977Santelices B., Cancino J., Montalva S., et al. 1977. Estudios ecológicos en la zona costera afectada por contaminación del “Northern Breeze”. II. Comunidades de playas de rocas. Medio Ambiente 2: 65-83., Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215., see Table 1). The study zones (MEABR and OAA) displayed taxonomic groups typical of the rocky intertidal zone (Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215.). However, important differences in community structure were recorded. Both boulder fields lacked top predators described for rocky platforms. Additionally, taxonomic groups that strongly attach to primary substrates were found, including benthic algae (e.g. Lithothamnium spp.), Mytilidae (e.g. P. purpuratus), Cirripedia (e.g. J. cirratus) and sessile annelids (e.g. Spirorbis spp.). Interestingly, intertidal boulder fields were a nursery habitat for all species, as evidenced by the presence of juveniles for all registered taxonomic groups (see Table 1). This finding highlights the importance of boulder fields for studying species development and the relationship of boulder fields with intertidal and subtidal diversity.

The differences in community structure between study sites are likely associated with coastal morphology and the environmental protection status of MEABRs. Moreover, the studied OAA is a well-described retention zone that, due to seawater circulation and coastal morphology, has increased phytoplankton abundance (Mace and Morgan 2006Mace A.J., Morgan S.G. 2006. Larval accumulation in the lee of the small headland: implications for the design of marine reserves. Mar. Ecol. Prog. Ser. 318: 19-29., Henríquez et al. 2007Henríquez L.A., Daner I.G., Muñoz C.A., et al. 2007. Primary production and phytoplanktonic biomass in shallow marine environments of central Chile: Effect of coastal geomorphology. Estuar. Coast. Shelf. 73: 137-147., Palma et al. 2009Palma A., Henriquez L.A., Ojeda F.P. 2009. Phytoplanktonic primary production modulated by coastal geomorphology in a highly dynamic environment of central Chile. Rev. Biol. Mar. Oceanogr. 44: 325-334.), which might help to explain the greater diversity of invertebrates in comparison with the MEABR (Fig. 1C). On the other hand, the Quintay MEABR may have had a differential impact on study zones.

General analyses of MEABRs have found greater species diversity and density than in OAAs, as well as different species composition (Durán and Castilla 1989Durán L.R., Castilla J.C. 1989. Variation and persistence of the middle rocky intertidal community of central Chile, with and without human harvesting. Mar. Biol. 103: 555-562., Gelcich et al. 2008Gelcich S., Godoy N., Prado L., et al. 2008. Add-on conservation benefits of marine territorial user rights fishery policies in central Chile. Ecol. Appl. 18: 273-281., Molina et al. 2014Molina P., Ojeda P., Aldana M., et al. 2014. Spatial and temporal variability in subtidal macroinvertebrates diversity patterns in a management and exploitation area for benthic resources (MEABRs). Ocean. Coast. Manage. 93: 121-128.). Similarly, greater benthic resource abundances in MEABRs than in OAAs could impact various species, even those not considered within management plans, through the direct and indirect effects of interspecific interactions such as competition and predation (for details see Castilla and Gelcich 2008Castilla J.C., Gelcich S. 2008. Management of the loco (Concholepas concholepas) as a driver for self-governance of small-scale benthic fisheries in Chile. In: Townsend R., Shotton R., Uchida H. (eds) Case studies in fisheries self-governance. FAO Fish. Tech., pp. 441-451., Gelcich et al. 2008Gelcich S., Godoy N., Prado L., et al. 2008. Add-on conservation benefits of marine territorial user rights fishery policies in central Chile. Ecol. Appl. 18: 273-281.). For example, some taxonomic groups, such as Arthropoda (e.g. crabs from the Petrolisthes genus) and Actiniaria (e.g. P. clematis and P. pluvia), may be favoured on the boulders of Quintay MEABR, (Fig. 3A, Table 1).

Studies evaluating the impacts of MEABRs on abundance and diversity have focussed on the subtidal system, a more stable habitat than boulder fields. Previous studies indicate significantly greater abundance and diversity in MEABRs than in OAAs (Gelcich et al. 2008Gelcich S., Godoy N., Prado L., et al. 2008. Add-on conservation benefits of marine territorial user rights fishery policies in central Chile. Ecol. Appl. 18: 273-281., Molina et al. 2014Molina P., Ojeda P., Aldana M., et al. 2014. Spatial and temporal variability in subtidal macroinvertebrates diversity patterns in a management and exploitation area for benthic resources (MEABRs). Ocean. Coast. Manage. 93: 121-128.). Additionally, the regular extraction of top predators (e.g. C. concholepas) (Molina et al. 2014Molina P., Ojeda P., Aldana M., et al. 2014. Spatial and temporal variability in subtidal macroinvertebrates diversity patterns in a management and exploitation area for benthic resources (MEABRs). Ocean. Coast. Manage. 93: 121-128.) may promote increased diversity by preventing the monopolization of major environmental resources by species with higher competitive capabilities (Paine 1966Paine R.T. 1966. Food Web Complexity and Species Diversity. Am. Nat. 100: 65-75.). This finding was supported by observations at the Quintay OAA, thus revealing a different functional dynamic related to the combined impact of top predator extraction and boulder field variability.

The greater richness and density of invertebrates within exclusion cages (Fig. 1A, B) suggests that the cage might have provided shelter against predators, thereby acting as an additional protective measure within the MEABR, which would explain the high density at this site (Fig. 1B). Echinodermata and Mollusca showed higher species diversity and density in the Quintay MEABR than in the OAA (see Table 1), an observation consistent with results obtained by Molina et al. (2014)Molina P., Ojeda P., Aldana M., et al. 2014. Spatial and temporal variability in subtidal macroinvertebrates diversity patterns in a management and exploitation area for benthic resources (MEABRs). Ocean. Coast. Manage. 93: 121-128.. Most molluscs and sea urchins are generalist grazers that scrape the substratum, thus removing spores, macroalgae plantlets, epiphytes and microalgae. The diet of these species is considerably similar (Aguilera 2011Aguilera M.A. 2011. The functional roles of herbivores in the rocky intertidal systems in Chile: A review of food preferences and consumptive effects. Rev. Chil. Hist. Nat. 84: 241-261.), with important impacts on benthic algae populations (Contreras and Castilla 1987Contreras S., Castilla J.C. 1987. Feeding behaviour and morphological adaptations in two sympatric sea urchins in central Chile. Mar. Ecol. Prog. Ser. 38: 217-224.). Therefore, the MEABR and exclusion cages promoted a protected area for mostly herbivorous invertebrate recruits (Fig. 3A). This protective status (i.e. MEABR regulations and exclusion cages) would differentially impact algae and invertebrates (Figs 1 and 2).

Indeed, the protection given to herbivorous invertebrates inside exclusion cages in the MEABR would increase foraging pressure, explaining the decreased algae density inside exclusion cages (Fig. 2B). This would additionally explain the lower richness and diversity of algae within the exclusion cages in the MEABR than in the OAA (Fig. 2A, C). Although there are no significant differences between zones (MEABR vs OAA), there was a tendency outside exclusion cages towards lower algae richness and diversity in the OAA, a zone where the Tetrapygus niger sea urchin was also recorded (see Table 1). The grazing activities of this species have been described as intense, generating large halos in the bed of intertidal benthic algae (Contreras and Castilla 1987Contreras S., Castilla J.C. 1987. Feeding behaviour and morphological adaptations in two sympatric sea urchins in central Chile. Mar. Ecol. Prog. Ser. 38: 217-224.).

In both study zones, the high abundance of red algae could be associated with the trophic morphology of the herbivores detected on boulders (Chiton spp. and Fissurella spp.) (Santelices and Correa 1985Santelices B., Correa J. 1985. Differential survival of macroalgae to digestion by intertidal herbivore molluscs. J. Exp. Mar. Biol. Ecol. 88: 183-191., Santelices et al. 1986Santelices B., Vasquez J., Meneses I. 1986. Patrones de distribución y dietas de un gremio de moluscos herbívoros en hábitats intermareales expuestos de Chile central. Monogr. Biol. 4: 147–171., Camus et al. 2008Camus P.A., Daroch K., Opazo F.L. 2008. Potential for omnivory and apparent intraguild predation in rocky intertidal herbivore assemblages from northern Chile. Mar. Ecol. Prog. Ser. 361: 35-45.) and of species that tolerate high habitat variability. Studies on intertidal rocky platforms have primarily addressed adult individuals with completely developed mouthparts, which prefer Calcarea algae species and other species resistant to grazing (Steneck and Dethier 1994Steneck R.S., Dethier M. 1994. A functional group approach to the structure of algal-dominated communities. Oikos 69: 476-498.). In boulder fields, only juveniles and invertebrate recruits were found (e.g. T. niger, C. cumingsi, C. latus; Fig. 1B), which may lead to the dominance of the Rhodophyta algae group in this habitat (Santelices 1990Santelices B. 1990. Patterns of organization of intertidal and shallow subtidal vegetation in wave exposed habitats in Central Chile. Hydrobiologia 192: 35-57., Muñoz and Ojeda 2000Muñoz A., Ojeda F.P. 2000. Ontogenetic changes in the diet of the herbivorous Scartichthys viridis in a rocky intertidal zone in central Chile. J. Fish. Biol. 56: 986-998., Aguilera 2011Aguilera M.A. 2011. The functional roles of herbivores in the rocky intertidal systems in Chile: A review of food preferences and consumptive effects. Rev. Chil. Hist. Nat. 84: 241-261.). On the other hand, species such as red crustose algae (e.g. Lithothamnium spp.) showed traits that would promote success in the highly variable boulder field habitat, which, in turn, would result in greater abundance.

Food webs

The OAA boulder field food web revealed the presence of Asterozoa predators such as the sea stars P. chilensis and O. kroyeri. Similar predator species were found for intertidal platforms (Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215.). Asterozoa species have a significant impact on community structure and dynamics since they prey on almost all of the sampled species (Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215., Navarrete et al. 2000Navarrete S.A., Menge B.A., Daily B. 2000. Species interactions at high trophic levels: intraguild predation or exploitation competition? Ecology 81: 2264-2277., Navarrete and Manzur 2008Navarrete S.A., Manzur T. 2008. Individual- and population- level responses of a keystone predator to geographic variation in prey. Ecology 89: 2005-2018., Fig. 3B). Sea stars are a determinant factor in species coexistence, with the predation of dominant community species by sea stars decreasing competitive impacts by preventing competitive exclusion, thereby increasing local diversity (Paine 1966Paine R.T. 1966. Food Web Complexity and Species Diversity. Am. Nat. 100: 65-75.). Moreover, the evidence obtained revealed the presence of other carnivorous groups such as anemones (Actinia spp. and A. alicemartinae) and planaria (T. inca), species with a broad trophic spectrum whose effects on boulder field communities are as yet unknown but should be considered (Sebens and Paine 1978Sebens K.P., Paine R.T. 1978. Biogeography of anthozoans along the west coast of South America: habitat, disturbance and prey availability. In: Proc. Int. Symp. Mar. Biogeogr. and Ecol. in the Southern Hemisphere. Vol. I., N. Zealand Dept. of Scientific and Industrial. Res. Inf. Ser. 137: 219-237., Zamponi 1979Zamponi M.O. 1979. Sobre la alimentación en Actiniaria (Coelenterata, Anthozoa). Neotropica 25: 195-202., Acuña and Zamponi 1996Acuña F.H., Zamponi M.O. 1996. Ecología trófica de las anemonas intermareales Phymactis clematis dana, 1849, Aulactinia marplatensis (Zamponi 1977) y A. reynaudi (Milne-Edwards 1857) (Actiniaria: Actiniidae): relaciones entre las anemonas y sus presas. Cienc. Mar. 22: 397-413.).

The MEABR boulder field trophic web revealed the presence of two carnivorous groups (Actiniaria and Polycladida) (Fig. 3A). In turn, the OAA showed three predator groups (Asterozoa, Actiniaria and Polycladida). The Asterozoa group was absent from the MEABR, which may be the result of an increased abundance of commercial predator species that would force Asterozoa to other intertidal or subtidal habitats; however, interactions between predators were not evaluated in this study. Interestingly, both boulder fields lacked the top predators described for rocky platforms, including C. concholepas and Sicyases sanguineus (Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215.). Moreover, species of the intertidal boulder fields that used primary substrates included benthic algae (e.g. C. dimorphum, G. lingulatum, Lithothamnium spp. and Ulva spp), Mytilidae (e.g. P. purpuratus and S. algosus), Cirripedia (e.g. B. flosculus, B. laevis and J. cirratus) and sessile annelids (e.g. Spirorbis spp.). In turn, the rocky platforms of central Chile only contain benthic algae and invertebrates such as Mytilidae and Cirripedia (Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215.).

In conclusion, rocks sampled from both Quintay zones showed similar invertebrate compositions and algae patterns to those of other intertidal habitats (e.g. Alveal 1971Alveal K. 1971. El ambiente costero de Montemar y su expresión biológica. Rev. Biol. Mar. Oceanogr. 14: 85–119., Santelices et al. 1977Santelices B., Cancino J., Montalva S., et al. 1977. Estudios ecológicos en la zona costera afectada por contaminación del “Northern Breeze”. II. Comunidades de playas de rocas. Medio Ambiente 2: 65-83., Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215.). The most abundant taxonomic group was Mollusca, as was found for rocky platforms, and a comparable result was obtained for algae species (Otaíza and Santelices 1985Otaíza R.D., Santelices B. 1985. Vertical distribution of chitons (Mollusca: Polyplacophora) in the rocky intertidal zone of central Chile. J. Exp. Mar. Biol. Ecol. 86: 229-240., Santelices et al. 1986Santelices B., Vasquez J., Meneses I. 1986. Patrones de distribución y dietas de un gremio de moluscos herbívoros en hábitats intermareales expuestos de Chile central. Monogr. Biol. 4: 147–171., Aguilera 2011Aguilera M.A. 2011. The functional roles of herbivores in the rocky intertidal systems in Chile: A review of food preferences and consumptive effects. Rev. Chil. Hist. Nat. 84: 241-261.). The analysed boulders of the MEABR and OAA showed taxonomic groups characteristic of intertidal zones (Castilla 1981Castilla J.C. 1981. Perspectivas de investigación en estructura y dinámica de comunidades intermareales rocosas de Chile Central. II. Depredadores de alto nivel trófico. Medio ambiente 5: 190-215.). Evidence of diversity and food web structure variability likely associated with MEABR protection was detected. Moreover, the high diversity observed in the OAA revealed a different functional dynamic that is likely associated with the combined impact of top predator extraction and boulder field variability. Finally, boulder fields are a necessary habitat for the recruitment of, and as a nursery for, all intertidal species, as is supported by the present findings of only juvenile invertebrate individuals. Therefore, the functional impact of boulder fields on the structural dynamics of intertidal communities should be considered in any management plans.

ACKNOWLEDGEMENTSTop

This study was funded by Universidad Andres Bello grants DI 0508/R, DI 17-10R, DI 16-12/R, and DI-495-14/R awarded to JP, and Universidad Andres Bello grant DI-02-11/I awarded to MRG-H.

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