Abundance and Diversity of Crypto- and Necto-Benthic Coastal Fish Are Higher in Marine Forests than in Structurally Less Complex Macroalgal Assemblages

PLOS ONE, Oct 2016

In Mediterranean subtidal rocky reefs, Cystoseira spp. (Phaeophyceae) form dense canopies up to 1 m high. Such habitats, called ‘Cystoseira forests’, are regressing across the entire Mediterranean Sea due to multiple anthropogenic stressors, as are other large brown algae forests worldwide. Cystoseira forests are being replaced by structurally less complex habitats, but little information is available regarding the potential difference in the structure and composition of fish assemblages between these habitats. To fill this void, we compared necto-benthic (NB) and crypto-benthic (CB) fish assemblage structures between Cystoseira forests and two habitats usually replacing the forests (turf and barren), in two sampling regions (Corsica and Menorca). We sampled NB fish using Underwater Visual Census (UVC) and CB fish using Enclosed Anaesthetic Station Vacuuming (EASV), since UVC is known to underestimate the diversity and density of the ‘hard to spot’ CB fish. We found that both taxonomic diversity and total density of NB and CB fish were highest in Cystoseira forests and lowest in barrens, while turfs, that could be sampled only at Menorca, showed intermediate values. Conversely, total biomass of NB and CB fish did not differ between habitats because the larger average size of fish in barrens (and turfs) compensated for their lower densities. The NB families Labridae and Serranidae, and the CB families Blenniidae, Cliniidae, Gobiidae, Trypterigiidae and Scorpaenidae, were more abundant in forests. The NB taxa Diplodus spp. and Thalassoma pavo were more abundant in barrens. Our study highlights the importance of using EASV for sampling CB fish, and shows that Cystoseira forests support rich and diversified fish assemblages. This evidence suggests that the ongoing loss of Cystoseira forests may impair coastal fish assemblages and related goods and services to humans, and stresses the need to implement strategies for the successful conservation and/or recovery of marine forests.

Abundance and Diversity of Crypto- and Necto-Benthic Coastal Fish Are Higher in Marine Forests than in Structurally Less Complex Macroalgal Assemblages

RESEARCH ARTICLE Abundance and Diversity of Crypto- and Necto-Benthic Coastal Fish Are Higher in Marine Forests than in Structurally Less Complex Macroalgal Assemblages Pierre D. Thiriet1,2*, Antonio Di Franco1,3, Adrien Cheminée1,4, Paolo Guidetti1, Olivier Bianchimani5, Solène Basthard-Bogain5, Jean-Michel Cottalorda1, Hazel Arceo1,6, Joan Moranta7,8, Pierre Lejeune9, Patrice Francour1, Luisa Mangialajo1,10 a11111 OPEN ACCESS Citation: Thiriet PD, Di Franco A, Cheminée A, Guidetti P, Bianchimani O, Basthard-Bogain S, et al. (2016) Abundance and Diversity of Crypto- and Necto-Benthic Coastal Fish Are Higher in Marine Forests than in Structurally Less Complex Macroalgal Assemblages. PLoS ONE 11(10): e0164121. doi:10.1371/journal.pone.0164121 Editor: Heather M. Patterson, Department of Agriculture and Water Resources, AUSTRALIA Received: May 23, 2016 Accepted: September 19, 2016 Published: October 19, 2016 Copyright: © 2016 Thiriet et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: PT Phd thesis was funded by the University Nice Sophia Antipolis; the work was partially realized in the framework of (and funded by) the Coconet European project (grant number 287844) and FOREFISH project funded by Total Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. 1 Université Nice Sophia Antipolis, CNRS, FRE 3729 ECOMERS, Parc Valrose 28, Nice, France, 2 Muséum National d’Histoire Naturelle, UMR 7208 BOREA, Station Marine de Dinard—CRESCO, Dinard, France, 3 CRIOBE, USR 3278 CNRS-EPHE-UPVD, Perpignan, France, 4 UMR 5110 CNRS/UPVD— CEFREM, Université de Perpignan Via Domitia, Perpignan, France, 5 Septentrion Environnement, Marseille, France, 6 Marine Science Institute, University of the Philippines, Diliman, Quezon City, Philippines, 7 Estación de Investigación Jaume Ferrer, Maó, Menorca, Illes Balears, España, 8 Instituto Español de Ocenografı́a (IEO), Centre Oceanogràfic de les Balears, Moll de Ponent s/n, Palma de Mallorca, Spain, 9 STARESO, Station de Recherches Océanographiques et Sous-Marines, Calvi, France, 10 Sorbonne Universités, UPMC Univ. Paris 06, INSU-CNRS, UMR 7093, Laboratoire d’Océanographie de Villefranche, Villefranche sur mer, France * Abstract In Mediterranean subtidal rocky reefs, Cystoseira spp. (Phaeophyceae) form dense canopies up to 1 m high. Such habitats, called ‘Cystoseira forests’, are regressing across the entire Mediterranean Sea due to multiple anthropogenic stressors, as are other large brown algae forests worldwide. Cystoseira forests are being replaced by structurally less complex habitats, but little information is available regarding the potential difference in the structure and composition of fish assemblages between these habitats. To fill this void, we compared necto-benthic (NB) and crypto-benthic (CB) fish assemblage structures between Cystoseira forests and two habitats usually replacing the forests (turf and barren), in two sampling regions (Corsica and Menorca). We sampled NB fish using Underwater Visual Census (UVC) and CB fish using Enclosed Anaesthetic Station Vacuuming (EASV), since UVC is known to underestimate the diversity and density of the ‘hard to spot’ CB fish. We found that both taxonomic diversity and total density of NB and CB fish were highest in Cystoseira forests and lowest in barrens, while turfs, that could be sampled only at Menorca, showed intermediate values. Conversely, total biomass of NB and CB fish did not differ between habitats because the larger average size of fish in barrens (and turfs) compensated for their lower densities. The NB families Labridae and Serranidae, and the CB families Blenniidae, Cliniidae, Gobiidae, Trypterigiidae and Scorpaenidae, were more abundant in forests. The NB taxa Diplodus spp. and Thalassoma pavo were more abundant in barrens. Our study highlights the importance of using EASV for sampling CB fish, and shows that Cystoseira forests support rich and diversified fish assemblages. This evidence PLOS ONE | DOI:10.1371/journal.pone.0164121 October 19, 2016 1 / 24 Crypto- and Necto-Benthic Fish in Mediterranean Macroalgal Assemblages Competing Interests: The authors have declared that no competing interests exist. suggests that the ongoing loss of Cystoseira forests may impair coastal fish assemblages and related goods and services to humans, and stresses the need to implement strategies for the successful conservation and/or recovery of marine forests. Introduction Habitat degradation, including the loss of structural complexity (e.g. loss of structural components such as boulders, trees or corals) [1], is recognized as a major threat to terrestrial, aquatic and marine ecosystems [2, 3]. This may affect ecological processes underlying abundances and distributions of organisms, community structures, ecosystem functions and ecosystem resistance and resilience. Ultimately, this may reduce the potential of the ecosystem to sustainably provide goods and services to humans [3–5]. In temperate subtidal seascapes worldwide, some macrophytes (seaweeds and seagrasses) may form structurally complex benthic habitats, such as kelp forests on hard bottoms and seagrass meadows on soft bottoms. These macrophyte-formed habitats are usually characterized by high biodiversity and high production rates [6]. However, these habitats are being degraded or lost worldwide due to a broad spectrum of anthropogenic and natural causes [7, 8]. This process has negative impacts on associated communities [9], including species that are of ecological and socio-economic importance, such as some fish [10, 11]. Mediterranean algal forests are formed in subtidal rocky reefs by Cystoseira (and some Sargassum) species (Phaeophyceae), forming a dense canopy up to 1 m high (depending on the species, site and season, e.g. [12, 13–15]). These habitats are suffering degradation as well [16], and past and ongoing losses of Cystoseira forests have been recorded throughout the Mediterranean Sea [17, 18–21]. Depending on the identity and intensity of natural and/or anthropogenic stressors, Cystoseira forests can be replaced by structurally less complex macroalgal habitats. For instance, in some areas with degraded water quality (e.g. eutrophication, increased turbidity, waste water discharge, other pollutants), Cystoseira forests can be replaced by turfs [22, 23] or shrubland-like habitats (hereafter ‘shrubs’), formed by Dictyotales, Sphacelariales and/or articulated Corallinales [24, 25]. In addition, herbivory can be a major cause of Cystoseira forest loss. For example, in areas where sea urchins are abundant (due to natur (...truncated)


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Pierre D. Thiriet, Antonio Di Franco, Adrien Cheminée, Paolo Guidetti, Olivier Bianchimani, Solène Basthard-Bogain, Jean-Michel Cottalorda, Hazel Arceo, Joan Moranta, Pierre Lejeune, Patrice Francour, Luisa Mangialajo. Abundance and Diversity of Crypto- and Necto-Benthic Coastal Fish Are Higher in Marine Forests than in Structurally Less Complex Macroalgal Assemblages, PLOS ONE, 2016, Volume 11, Issue 10, DOI: 10.1371/journal.pone.0164121