The Structure of Mediterranean Rocky Reef Ecosystems across Environmental and Human Gradients, and Conservation Implications

and Conservation Implications. PLoS ONE 7(2): e32742. doi:10.1371/journal.pone.0032742 The Structure of Mediterranean Rocky Reef Ecosystems across Environmental and Human Gradients, and Conservation Implications Enric Sala 0 Enric Ballesteros 0 Panagiotis Dendrinos 0 Antonio Di Franco 0 Francesco Ferretti 0 David Foley 0 Simonetta Fraschetti 0 Alan Friedlander 0 Joaquim Garrabou 0 Harun Gu c lu soy 0 Paolo 0 Guidetti 0 Benjamin S. Halpern 0 Bernat Hereu 0 Alexandros A. Karamanlidis 0 Zafer Kizilkaya 0 Enrique Macpherson 0 Luisa Mangialajo 0 Simone Mariani 0 Fiorenza Micheli 0 Antonio Pais 0 Kristin 0 Riser 0 Andrew A. Rosenberg 0 Marta Sales 0 Kimberly A. Selkoe 0 Rick Starr 0 Fiona Tomas 0 Mikel 0 Zabala 0 Tamara Natasha Romanuk, Dalhousie University, Canada 0 1 National Geographic Society , Washington, D.C. , United States of America, 2 Centre d'Estudis Avanc ats de Blanes , CEAB-CSIC, Blanes , Spain , 3 MOm/Hellenic Society for the Study and Protection of the Monk Seal , Athens, Greece, 4 DiSTeBA , Universita` del Salento , Lecce , Italy , 5 Hopkins Marine Station, Stanford University , Pacific Grove , California, United States of America, 6 NOAA Southwest Fisheries Science Center, Pacific Grove, California, United States of America, 7 Joint Institute for Marine and Atmospheric Research, University of Hawaii, Honolulu, Hawaii, United States of America, 8 U.S. Geological Survey, Hawaii Cooperative Fishery Research Unit and University of Hawaii at Manoa, Honolulu, Hawaii, United States of America, 9 Centre Mediterrani d'Investigacions Marines i Ambientals , ICM-CSIC, Barcelona , Spain , 10 Dokuz Eylu l University - Institute of Marine Sciences and Technology , Inciralti, Izmir, Turkey, 11 SAD-EKOG, Maltepe, Ankara , Turkey , 12 National Center for Ecological Analysis and Synthesis, University of California Santa Barbara, Santa Barbara, California, United States of America, 13 Departament d'Ecologia, Facultat de Biologia, Universitat de Barcelona , Barcelona , Spain , 14 Universite de Nice-Sophia Antipolis , Nice, France, 15 Dipartimento di Scienze Zootecniche , Universita` di Sassari , Sassari , Italy , 16 Scripps Institution of Oceanography, La Jolla, California, United States of America , 17 Conservation International, Arlington , Virginia, United States of America, 18 Estacio d'Investigacio Jaume Ferrer, IEO-Centre Oceanogra`fic de Balears , Mao , Spain, 19 Moss Landing Marine Laboratories, Moss Landing, California , United States of America Historical exploitation of the Mediterranean Sea and the absence of rigorous baselines makes it difficult to evaluate the current health of the marine ecosystems and the efficacy of conservation actions at the ecosystem level. Here we establish the first current baseline and gradient of ecosystem structure of nearshore rocky reefs at the Mediterranean scale. We conducted underwater surveys in 14 marine protected areas and 18 open access sites across the Mediterranean, and across a 31-fold range of fish biomass (from 3.8 to 118 g m22). Our data showed remarkable variation in the structure of rocky reef ecosystems. Multivariate analysis showed three alternative community states: (1) large fish biomass and reefs dominated by non-canopy algae, (2) lower fish biomass but abundant native algal canopies and suspension feeders, and (3) low fish biomass and extensive barrens, with areas covered by turf algae. Our results suggest that the healthiest shallow rocky reef ecosystems in the Mediterranean have both large fish and algal biomass. Protection level and primary production were the only variables significantly correlated to community biomass structure. Fish biomass was significantly larger in well-enforced no-take marine reserves, but there were no significant differences between multi-use marine protected areas (which allow some fishing) and open access areas at the regional scale. The gradients reported here represent a trajectory of degradation that can be used to assess the health of any similar habitat in the Mediterranean, and to evaluate the efficacy of marine protected areas. - Funding: This study was funded by the Oak Foundation, the Pew Charitable Trusts, Spains National Council for Scientific Research (CSIC) and the Lenfest Ocean Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Intense exploitation over millennia has depleted Mediterranean species from the large to the small, including the Mediterranean monk seal, sea turtles, bluefin tuna, groupers, red coral, lobsters, and limpets (e.g., [1,2,3]). Habitat destruction, pollution, introduced species and climate change have also taken a toll on Mediterranean species and ecosystems [4,5]. Although these impacts have been significant, based on qualitative observations over the millennia, it is difficult to evaluate their magnitude because there is no rigorous historical baseline for the abundance of marine species or the structure of marine ecosystems in the Mediterranean [6,7], except for a few taxa and local time series of fishery dependent and independent data [3]. Most of the quantitative data on the structure of Mediterranean ecosystems originates from field studies in the last 30 years. Therefore, our attempts to evaluate the health of the marine ecosystem and the efficacy of recent conservation actions at the ecosystem level are constrained by a limited sense of what is possible or natural [8]. Here we establish the first current comparable baseline of ecosystem structure at the Mediterranean scale, focusing on nearshore rocky reefs. What would a healthy Mediterranean rocky bottom look like? There are no pristine sites (i.e. undisturbed by humans, with historical ecosystem structure and carrying capacity) left in the Mediterranean that allow us to set a baseline against which to compare the health of current ecosystems. Research on pristine, historically unfished sites in the central Pacific show that intact, complex reef ecosystems harbor large biomass of fishes, with inverted biomass pyramids, and high coral cover [9,10]. Fishing pressure has been a major stressor on Mediterranean reef systems. Thus, in the Mediterranean, we would expect total fish biomass to be also the single most important indicator of the health of fish populations, with biomass increasing with decreased fishing pressure, as Mediterranean no-take marine reserves demonstrate [11,12,13,14]. Therefore, marine reserves are the best proxies for the trajectory of recovery of fish assemblages towards a pristine state, possibly including cascading effects leading to a wider recovery of the protected ecosystems. However, we expect these current baselines to be still far from historical baselines with an intact ecosystem likely including all apex predators such as sharks and monk seals. Predatory fishes can have a major role (...truncated)