Vol. 567: 1–16, 2017 MARINE ECOLOGY PROGRESS SERIES Published March 13 https://doi.org/10.3354/meps12057 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Temperate rocky subtidal reef community reveals human impacts across the entire food web Alejandro Pérez-Matus1,*, Andres Ospina-Alvarez2, Patricio A. Camus3, Sergio A. Carrasco1, Miriam Fernandez2,4, Stefan Gelcich2,4,5, Natalio Godoy5,6, F. Patricio Ojeda6, Luis Miguel Pardo7,8, Nicolás Rozbaczylo6, Maria Dulce Subida2, Martin Thiel9,10,11, Evie A. Wieters2, Sergio A. Navarrete2,6 1Subtidal Ecology Laboratory & Center for Marine Conservation, Estación Costera de Investigaciones Marinas, Pontificia Universidad Católica de Chile, Casilla 114-D, 2690931 Santiago, Chile 2–11Full list of author addresses is provided in the Supplement at www.int-res.com/articles/suppl/m567p001_supp.pdf ABSTRACT: Food webs as representations of who eats whom are at the core of community ecology. Incorporation of tools from network theory enables assessment of how complex systems respond to natural and human-induced stressors, revealing how harvesting may degrade the properties and resili- ence of food webs. We present a comprehensive, coastal marine food web that includes 147 taxa co- occurring on shallow subtidal reefs along the highly productive and exploited Humboldt Current System of central Chile. This food web has connectance of 0.06, link density of 1204 and mean chain length of 4.3. The fractions of intermediate (76%), omnivorous (49%) and cannibalistic (8%) nodes are slightly Simplified food web with top/fishery (T, F; orange), interme- lower than those observed in other marine food webs. diate (I; red, blue = invertebrates, fishes, respectively) and Of the 147 nodes, 34 are harvested. Links to har- basal (B; green) nodes of the subtidal rocky shores of central vested nodes represented 50 to 100% of all trophic Chile. Characteristic species shown include sea urchins, sea links of non-harvested nodes, illustrating the great stars, kelp and reef fishes impact that fishery pressure can have on the food Image: Alejandro Pérez-Matus web. The food web was compartmentalized into 5 sub-webs with high representation of harvested taxa. KEY WORDS: Network structure · Marine ecosystems This structure changes if the fishery node is removed. · Fishery · Resilience · Chile Similarity analyses identified groups of harvested species with non-harvested nodes, suggesting that these tropho-equivalents could be sentinel species INTRODUCTION for the community-wide impacts of coastal fisheries. We conclude that fishing effects can be transmitted The advent of network theory and other recent throughout the food web, with no compartments theoretical and computational advances (Miele et al. completely unaffected by harvesting. It is urgent to establish monitoring programs for community-wide 2012, Kéfi et al. 2015, Kéfi et al. 2016) have revitalized effects of fisheries and assess whether resilience of food web ecology as an area of empirical and theoreti- these highly productive subtidal food webs has al - cal research that promises to provide a robust frame- ready been compromised, thereby identifying essen- work to evaluate fundamental and applied questions tial nodes that require stronger fisheries regulation. through embracing, instead of simplifying or decon- structing, the inherently complex nature of ecological © The authors 2017. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Mar Ecol Prog Ser 567: 1–16, 2017 systems (Thompson et al. 2012). Indeed, a community reported terrestrial, estuarine and freshwater food food web describes the feeding relationships among webs (see also Riede et al. 2010), and that given the all co-occurring taxa comprising a ‘local’ community. short average path between species, the impact of dis- Beyond the limitations inherent to representing spe- turbances could rapidly propagate throughout the en- cies interaction strengths as simple binary links (but tire ecosystem. This result is in good agreement with see Berlow et al. 2009, Carscallen et al. 2012) and the the recent historical compilation of food webs reported fact that important non-trophic interactions are not by Sala (2004) for the Mediterranean Sea. Therefore, captured in these representations (Ings et al. 2009, there are still comparatively few marine food web Mougi & Kondoh 2012, Kéfi et al. 2015), these trophic representations that can capture a sig nificant fraction link webs can provide firsthand information on of the species that co-occur in local communities. species relationships within a community and how di- Here, we present the results of an effort to assemble verse stressors are expected to propagate and degrade the first food web for shallow subtidal benthic habitats ecosystem resilience. Moreover, they offer a glimpse of the highly productive Humboldt Current System into the processes and species (nodes) that are most (HCS) (Thiel et al. 2007). This is a community-based likely to push the system towards alternative states approach, in which we included a large fraction of all or whole-sale extinctions (Dell et al. 2005, Lotze et species known to coexist and interact within a defined al. 2011b, Thompson et al. 2012). When combined geographic area and type of habitat (i.e. kelp beds) of with traditional experimental and observational ap- subtidal rocky shores of central Chile. The list of proaches, which typically focus on a small subset of species included in the food web encompasses, to the species (Martinez 1993, Bascompte & Pedro 2006), best of our knowledge, the species richness commonly food web analyses can be a very powerful approach to found in these habitats. The web was constructed fol- investigate natural and anthropogenic impacts, while lowing a comprehensive literature review, interviews allowing for nature’s complexity. with experts and direct ecological observations con- Unfortunately, assembling realistic food web repre- ducted by the authors for more than 40 yr of cumula- sentations of natural communities is not an easy task. tive field research in central Chile. The classic paper by Martinez (1993) clearly shows Noteworthy attributes of the productive waters of how incompleteness of food web depictions can alter the HCS (Chavez & Messié 2009) is the economic most food web patterns; that is, most attributes change importance of artisanal fisheries in coastal habitats of with species richness and the number of true links the inner shelf and the high diversity of targeted spe- (see also Dunne et al. 2004, Riede et al. 2010). In the cies, including numerous species of macroalgae, case of marine coastal ecosystems, probably the most invertebrates and fishes (Bustamante & Castilla 1987, common approach to food webs is to focus on and rep- Defeo & Castilla 2005, Thiel et al. 2007). This is the resent strongly interacting subsets of species (e.g. situation in central Chile, where most of the dive fish- Menge & Sutherland 1976, Paine 1980, Bustamante & eries are located predominantly on rocky bottoms Branch 1996, Navarrete & Menge 1996, Castilla 1999, within a depth of 10 to 30 m. Beyond studies docu- Fariña et al. 2008), rather than to encompass local spe- menting the effects of human harvesting on subsets cies richness. Consequently, far fewer comprehensive of exploited and unexploited species (e.g. Godoy et marine food webs have been reported than their ter- al. 2010), there is still no synthetic knowledge about restrial counterparts (Link 2002, Dunne et al. 2004), how these impacts propagate and affect the rest of and their initial represen tations (e.g. Cohen 1994) the shallow subtidal community. The study by Sala were poorly resolved and grossly undersampled, gen- (2004) for the highly diverse marine food webs of the erating a number of spurious patterns (Gauzens et al. Mediterranean Sea (>1000 species), although admit- 2013). Thus, completeness of food web representa- tedly incomplete in link density, vividly shows how tions is important, whether they are used to explore the long history of human harvesting that led to the existence of regularities and scaling properties in extinction of most megafauna may have also pro- nature (e.g. Riede et al. 2010) or to investigate the im- foundly altered the topology and structure of those pact of disturbances in multi-species systems (Boit et food webs. Further simulation studies using stochas- al. 2012, Thompson et al. 2012). For instance, Dunne tic structural and mass balance food web models et al. (2004) analyzed the attributes of 3 published show that a number of attributes of Mediterranean marine food webs with ‘relatively detailed species food webs evidence an advanced state of degrada- and trophic interactions’. Their conclusions suggest tion in comparison to those food webs reported for that, contrary to previous claims (Cohen 1994, Link the Caribbean, Ben guela and continental USA (Coll 2002), marine food webs are not too distinct from well- et al. 2008)—greatly due to fisheries, but also due to Pérez-Matus et al.: Subtidal food web of rocky shores 3 species introductions (Lotze et al. 2011a). To what waters (if any) were not considered. Similarly, sandy extent the structural simplification of the Mediterran- and other soft-sediment habitats were not included. ean food web, which is progressively becoming less Additionally, we did not include invertebrate species connected and more dominated by small-body-size such as meiofauna (interstitial organisms <1 mm) and components (Lotze & Milewski 2004), is also ob - parasites in this food web. The species list and trophic served in other large marine ecosystems must be links were initially assembled from published records urgently investigated. Therefore, a first step is to im- that included qualitative, quantitative and experi- prove our knowledge of the structural properties of mental studies conducted in this region over the past the diverse and complex system of the HCS, which 30 yr (see Supplement 1 at www.int-res.com/ articles/ provides essential eco system services for humans.