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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Mar. Sci.</journal-id>
<journal-title>Frontiers in Marine Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Mar. Sci.</abbrev-journal-title>
<issn pub-type="epub">2296-7745</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fmars.2017.00054</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Marine Science</subject>
<subj-group>
<subject>Perspective</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Seagrass Meadows Provide 3D Habitat for Reef Fish</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name><surname>Serrano</surname> <given-names>Oscar</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="author-notes" rid="fn001"><sup>&#x0002A;</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/302076/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Serrano</surname> <given-names>Eduard</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/398724/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Inostroza</surname> <given-names>Karina</given-names></name>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref>
</contrib>
<contrib contrib-type="author">
<name><surname>Lavery</surname> <given-names>Paul S.</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/336754/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Mateo</surname> <given-names>Miguel A.</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/336211/overview"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Ballesteros</surname> <given-names>Enric</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<uri xlink:href="http://loop.frontiersin.org/people/337312/overview"/>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup><institution>Centre for Marine Ecosystems Research, School of Science, Edith Cowan University</institution> <country>Joondalup, WA, Australia</country></aff>
<aff id="aff2"><sup>2</sup><institution>Centre d&#x00027;Estudis Avan&#x000E7;ats de Blanes-CSIC</institution> <country>Blanes, Spain</country></aff>
<aff id="aff3"><sup>3</sup><institution>BMT Oceanica Pty Ltd.</institution> <country>Wembley, WA, Australia</country></aff>
<author-notes>
<fn fn-type="edited-by"><p>Edited by: Angel Borja, AZTI, Spain</p></fn>
<fn fn-type="edited-by"><p>Reviewed by: Susana Enr&#x000ED;quez, National Autonomous University of Mexico, Mexico; Jos&#x000E9; Lino Vieira De Oliveira Costa, Universidade de Lisboa, Portugal</p></fn>
<fn fn-type="corresp" id="fn001"><p>&#x0002A;Correspondence: Oscar Serrano <email>o.serranogras&#x00040;ecu.edu.au</email></p></fn>
<fn fn-type="other" id="fn002"><p>This article was submitted to Marine Ecosystem Ecology, a section of the journal Frontiers in Marine Science</p></fn></author-notes>
<pub-date pub-type="epub">
<day>28</day>
<month>02</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<year>2017</year>
</pub-date>
<volume>4</volume>
<elocation-id>54</elocation-id>
<history>
<date date-type="received">
<day>11</day>
<month>12</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>15</day>
<month>02</month>
<year>2017</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#x000A9; 2017 Serrano, Serrano, Inostroza, Lavery, Mateo and Ballesteros.</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>Serrano, Serrano, Inostroza, Lavery, Mateo and Ballesteros</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p></license>
</permissions>
<abstract>
<p>For large fishes, seagrass canopies typically provide a relatively flat habitat on seabeds, but seagrasses in the genus <italic>Posidonia</italic> can provide additional habitat complexity by forming organic-rich deposits known as mats. Erosional processes can scour channels through the mats, resulting in the formation of escarpments with caves. Here we report that reef fishes, such as groupers, inhabit the caves found within mat escarpments. The characteristics of the cavities are highly variable, ranging from small-elongated holes to deep caves with large entrances. The origin of these caves (biological and/or geological) is unknown, but it is possible that fish behavior enhance their formation. <italic>Posidonia</italic> seagrass escarpments provide a complex 3D habitat for reef fish that is not provided by typical canopy structure of seagrass. Further studies are required to gain insights into the natural history of seagrass escarpments and their ecological importance.</p>
</abstract>
<kwd-group>
<kwd><italic>Posidonia</italic></kwd>
<kwd>biodiversity</kwd>
<kwd>fish ecology</kwd>
<kwd>behavior</kwd>
<kwd>Mediterranean Sea</kwd>
<kwd>Indian Ocean</kwd>
</kwd-group>
<contract-num rid="cn001">DE170101524</contract-num>
<contract-sponsor id="cn001">Australian Research Council<named-content content-type="fundref-id">10.13039/501100000923</named-content></contract-sponsor>
<counts>
<fig-count count="2"/>
<table-count count="0"/>
<equation-count count="0"/>
<ref-count count="13"/>
<page-count count="3"/>
<word-count count="1657"/>
</counts>
</article-meta>
</front>
<body>
<p>Seagrass canopies typically provide a relatively uniform habitat on the seabed, which is not suitable for large reef fishes. However, seagrasses in the genus <italic>Posidonia</italic> can modify bottom bathymetry through vertical plant growth and sediment accumulation, resulting in organic-rich deposits known as mats (P&#x000E9;r&#x000E8;s and Picard, <xref ref-type="bibr" rid="B9">1964</xref>; Mateo et al., <xref ref-type="bibr" rid="B6">1997</xref>). Erosional processes can scour channels through the mats, resulting in the formation of 1&#x02013;3 m high and up to 500 m long escarpments (Serrano et al., <xref ref-type="bibr" rid="B11">2016</xref>; Figure <xref ref-type="fig" rid="F1">1</xref>). Previous studies also reported the presence of blowouts in <italic>Thalassia testudinum</italic> meadows, consisting of bare areas with an eroding edge that forms a vertical wall with overhanging seagrass roots and rhizomes (Patriquin, <xref ref-type="bibr" rid="B8">1975</xref>; Wanless, <xref ref-type="bibr" rid="B12">1981</xref>; Maci&#x000E1; and Robinson, <xref ref-type="bibr" rid="B5">2005</xref>).</p>
<fig id="F1" position="float">
<label>Figure 1</label>
<caption><p><bold>Erosional mat escarpments in seagrass <italic><bold>Posidonia</bold></italic> meadows. (a)</bold> <italic>Posidonia australis</italic> mat escarpment in Shark Bay, Western Australia (&#x02212;25.796563&#x000B0;, 113.460218&#x000B0;; Indian Ocean). <bold>(b)</bold> <italic>Posidonia oceanica</italic> mat escarpment in Es Pujols Cove, Balearic Islands (38.727964&#x000B0;, 1.456189&#x000B0;; Mediterranean Sea).</p></caption>
<graphic xlink:href="fmars-04-00054-g0001.tif"/>
</fig>
<p>The mechanisms behind escarpment formation can be related to natural processes (e.g., wave action, tidal flow, and hurricanes) or to anthropogenic activities, such as dredging, vessel groundings, and propeller scars (Whitfield et al., <xref ref-type="bibr" rid="B13">2002</xref>). Mat escarpments have been described in shallow and highly productive <italic>P. oceanica</italic> meadows from the Mediterranean Sea, <italic>P. australis</italic> meadows from the Indian Ocean (Serrano et al., <xref ref-type="bibr" rid="B11">2016</xref>), and in <italic>T. testudinum</italic> meadows from the Caribbean exposed to strong wave action (Patriquin, <xref ref-type="bibr" rid="B8">1975</xref>; Wanless, <xref ref-type="bibr" rid="B12">1981</xref>). In <italic>Posidonia</italic> meadows, the inter-twined remains of seagrass tissues consolidate the sandy substrate, holding together the exposed face of the seagrass escarpment and maintaining a semi-rigid, 3D structure, in which caves are found. This phenomenon is unusual but of ecological importance due to its role as habitat for exclusively reef fish species (Figure <xref ref-type="fig" rid="F2">2</xref>).</p>
<fig id="F2" position="float">
<label>Figure 2</label>
<caption><p><bold>Reef-associated fish inhabiting caves within seagrass mat escarpments</bold>. <bold>(a&#x02013;c)</bold> <italic>Epinephelus coioides, Apogon angustatus</italic>, and <italic>Abudefduf bengalensis</italic> inhabiting caves within <italic>Posidonia australis</italic> mat escarpment in the Indian Ocean (Shark Bay, Western Australia). <bold>(d)</bold> <italic>Apogon imberbis</italic> inhabiting caves within <italic>Posidonia oceanica</italic> mat escarpment in the Mediterranean Sea (Balearic Islands).</p></caption>
<graphic xlink:href="fmars-04-00054-g0002.tif"/>
</fig>
<p>During a routine field trip to monitor seagrass meadows at Shark Bay (Western Australia), we discovered that escarpments supported abundant reef fish assemblages. Caves (up to &#x0007E;1 m<sup>3</sup>) found throughout mat escarpments were occupied primarily by groupers (<italic>Epinephelus coioides</italic>, Serranidae), with up to 10 individuals (30&#x02013;100 cm in length) observed in a single cave (Figure <xref ref-type="fig" rid="F2">2</xref> and Supplementary Video <xref ref-type="supplementary-material" rid="SM1">1</xref>). Other reef-associated fish found within the escarpment included sea perches (<italic>Psammoperca waigiensis</italic>, Latidae), cardinalfishes (<italic>Apogon angustatus</italic> and <italic>A. cavitensis</italic>, Apogonidae), bengal sergeants (<italic>Abudefduf bengalensis</italic>, Pomacentridae), and sea chubs (<italic>Microcanthus strigatus</italic>, Kyphosidae) (Figure <xref ref-type="fig" rid="F2">2</xref> and Supplementary Video <xref ref-type="supplementary-material" rid="SM1">1</xref>). A similar fish assemblage was observed in reef habitat but not in seagrass canopies nor in unvegetated sand at Shark Bay. Life-time observations made by the authors revealed that mat escarpments in <italic>P. oceanica</italic> meadows are also occupied by reef-associated fish such as scorpionfishes (<italic>Scorpaena porcus</italic> and <italic>S. scrofa</italic>, Scorpaenidae), groupers (<italic>Epinephelus marginatus</italic> and <italic>E. costae</italic>, Serranidae), cardinalfishes (<italic>Apogon imberbis</italic>, Apogonidae), brown meagres (<italic>Sciaena umbra</italic>, Sciaenidae), seabreams (<italic>Diplodus sargus</italic>, Sparidae), and wrasses (<italic>Labrus viridis, L. merula, Symphodus tinca</italic>, Labridae<italic>)</italic> (Figure <xref ref-type="fig" rid="F2">2</xref> and Supplementary Video <xref ref-type="supplementary-material" rid="SM1">1</xref>).</p>
<p>In both <italic>P. oceanica</italic> and <italic>P. australis</italic> mat escarpments we found several burrows in the form of cavities inhabited by reef fish. The form, shape, and dimension of the cavities were highly variable, ranging from small-elongated holes to deep caves with large entrances. The process(es) forming these caves (biological and/or geological origin) is unknown, but it is possible that displacement of sediment by fish (i.e., swimming action and/or deliberate digging or burrowing) leads to, or enhances, their formation, as described in other unconsolidated sandy substrates (Mueller, <xref ref-type="bibr" rid="B7">2015</xref>).</p>
<p>Seagrass meadows provide valuable ecosystem services (Green and Short, <xref ref-type="bibr" rid="B3">2003</xref>) and are ecologically important as they provide habitat and shelter for juvenile fish and larval recruitment (Hemminga and Duarte, <xref ref-type="bibr" rid="B4">2000</xref>; Borg et al., <xref ref-type="bibr" rid="B1">2006</xref>; Prado et al., <xref ref-type="bibr" rid="B10">2009</xref>), maintaining high biodiversity, while providing shoreline protection against erosion (Green and Short, <xref ref-type="bibr" rid="B3">2003</xref>), and sequestering carbon (Fourqurean et al., <xref ref-type="bibr" rid="B2">2012</xref>), among others. The ecosystem services provided by seagrass meadows greatly vary among habitats due to biotic and abiotic factors, and in this study we provide evidence of a novel function of <italic>Posidonia</italic> escarpments, through provision of complex 3D habitat for reef fish that is not provided by typical canopy structure of seagrass.</p>
<p>Further studies are required to gain insights into the natural history of seagrass escarpments and their ecological importance. Firstly, there is need to report and map additional seagrass escarpments within <italic>Posidonia</italic> meadows (Serrano et al., <xref ref-type="bibr" rid="B11">2016</xref>) and other seagrass ecosystems worldwide, including <italic>T. testudinum</italic> meadows in the Caribbean region. Secondly, further research is required to understand the mechanisms of escarpment and cave formation, including testing the hypothesis of cavities within the escarpment originated by fish behavior, and describe their size and dimension. Finally, there is a need to demonstrate the ecological importance of seagrass escarpments as reef fish habitat, enhancing fish biodiversity and biomass, and their importance for reproduction, predator avoidance and feeding areas, among others.</p>
<sec id="s1">
<title>Ethics statement</title>
<p>The Ethics Committee of Edith Cowan University has approved this study &#x02013; Project 17297.</p>
</sec>
<sec id="s2">
<title>Author contributions</title>
<p>OS: Conceived the manuscript. All authors critically revised and approved the final manuscript.</p>
<sec>
<title>Conflict of interest statement</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
</sec>
</body>
<back>
<ack><p>This work was supported by the ECU Early Career Research Grant Scheme. OS was supported by an ARC DECRA DE170101524. This is a contribution of the Benthic Ecology Group, 2014SGR120.</p>
</ack>
<sec sec-type="supplementary-material" id="s3">
<title>Supplementary material</title>
<p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="http://journal.frontiersin.org/article/10.3389/fmars.2017.00054/full#supplementary-material">http://journal.frontiersin.org/article/10.3389/fmars.2017.00054/full#supplementary-material</ext-link></p>
<supplementary-material xlink:href="Video1.MP4" id="SM1" mimetype="video/mp4" xmlns:xlink="http://www.w3.org/1999/xlink"/>
</sec>
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</article>