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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.2023.1243153</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Marine Science</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Learning from <italic>Caretta caretta</italic> (Linnaeus, 1758) epibionts: a study from the Adriatic Sea</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Baruffaldi</surname>
<given-names>Matilde</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rubini</surname>
<given-names>Silva</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2525804"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ignoto</surname>
<given-names>Sara</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2237813"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Angelini</surname>
<given-names>Valeria</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1052258"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Tiralongo</surname>
<given-names>Francesco</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/297981"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Experimental Zooprophylactic Institute of Lombardy and Emilia Romagna</institution>, <addr-line>Ferrara</addr-line>, <country>Italy</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Biological, Geological and Environmental Sciences, University of Catania</institution>, <addr-line>Catania</addr-line>, <country>Italy</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Ente Fauna Marina Mediterranea, Scientific Organization for Research and Conservation of Marine Biodiversity</institution>, <addr-line>Avola</addr-line>, <country>Italy</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Fondazione Cetacea Onlus</institution>, <addr-line>Riccione</addr-line>, <country>Italy</country>
</aff>
<aff id="aff5">
<sup>5</sup>
<institution>National Research Council, Institute of Biological Resources and Marine Biotechnologies</institution>, <addr-line>Ancona</addr-line>, <country>Italy</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Suncica Bosak, University of Zagreb, Croatia</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Carlos Jimenez, Enalia Physis Environmental Research Centre (ENALIA), Cyprus; Ana Rita Patr&#xed;cio, MARE-ISPA, Portugal</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Francesco Tiralongo, <email xlink:href="mailto:francesco.tiralongo@unict.it">francesco.tiralongo@unict.it</email>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>19</day>
<month>10</month>
<year>2023</year>
</pub-date>
<pub-date pub-type="collection">
<year>2023</year>
</pub-date>
<volume>10</volume>
<elocation-id>1243153</elocation-id>
<history>
<date date-type="received">
<day>20</day>
<month>06</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>03</day>
<month>10</month>
<year>2023</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2023 Baruffaldi, Rubini, Ignoto, Angelini and Tiralongo</copyright-statement>
<copyright-year>2023</copyright-year>
<copyright-holder>Baruffaldi, Rubini, Ignoto, Angelini and Tiralongo</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) and the copyright owner(s) 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>Epibiont communities can be used as useful ecological indicators, providing information on the ecology and health conditions of their hosts. In this study, we analyzed the cirriped community from a total of 117 dead specimens of <italic>Caretta caretta</italic> (Linnaeus, 1758) collected in the north Adriatic between the years 2020 and 2022. We recorded a total of six different species distributed in five genera of cirripeds. The two most abundant species were <italic>Chelonibia testudinaria</italic> (Linnaeus, 1758) and <italic>Platylepas hexastylos</italic> (Linnaeus, 1758), located in different areas of the body; the former mainly on the carapace, while the latter mainly on the skin. We analyzed their abundance and distribution pattern on the sea turtle&#x2019;s body and used the findings to deduce the health conditions and ecological aspects of stranded specimens of <italic>C. caretta</italic>, providing new data on this threatened and vulnerable species and its epibionts. A total of 11 specimens of <italic>C. caretta</italic> were affected by DTS (Debilitative Turtle Syndrome), these specimens exhibited a significant barnacle infestation on all body parts, markedly higher than the specimens of <italic>C. caretta</italic> not affected by DTS. Studies of associated barnacles in sea turtles should be encouraged among researchers as complementary tool to infer habitat use and health status of sea turtle species.</p>
</abstract>
<kwd-group>
<kwd>loggerhead sea turtle</kwd>
<kwd>cirripeds</kwd>
<kwd>barnacles</kwd>
<kwd>Mediterranean Sea</kwd>
<kwd>threatened species</kwd>
<kwd>fishery</kwd>
</kwd-group>
<counts>
<fig-count count="10"/>
<table-count count="2"/>
<equation-count count="0"/>
<ref-count count="93"/>
<page-count count="12"/>
<word-count count="5632"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Marine Biology</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<title>Introduction</title>
<p>Sea turtles are one of several examples of a broadly distributed group that has historically suffered population declines caused by fishing bycatch and hunting of adult turtles and harvesting of eggs (<xref ref-type="bibr" rid="B28">Dodd, 1988</xref>; <xref ref-type="bibr" rid="B47">Jackson et&#xa0;al., 2001</xref>; <xref ref-type="bibr" rid="B31">Ernst and Lovich, 2009</xref>). These declines have led to worldwide conservation efforts since the 1950s (<xref ref-type="bibr" rid="B42">Hamann et&#xa0;al., 2010</xref>). In the Mediterranean Sea, the only common and widely distributed species of sea turtle is <italic>Caretta caretta</italic> (Linnaeus, 1758), commonly known as the &#x201c;loggerhead sea turtle&#x201d; (<xref ref-type="bibr" rid="B71">Prato et&#xa0;al., 2022</xref>). The other two species recorded in the basin are <italic>Chelonia mydas</italic> (Linnaeus, 1758) and <italic>Dermochelys coriacea</italic> (Vandelli, 1761). While the former nests in some areas of the Mediterranean, the latter is an occasional visitor (<xref ref-type="bibr" rid="B14">Casale et&#xa0;al., 2018</xref>). The Adriatic Sea represents an important marine sector of the Mediterranean basin with regard to <italic>C. caretta</italic> ecology. While the southern part of the Adriatic Sea has been identified as a significant growth habitat (<xref ref-type="bibr" rid="B18">Casale et&#xa0;al., 2007</xref>), the shallow waters of the central and northern Adriatic are recognized as some of the most crucial neritic feeding grounds in the region for specific populations (<xref ref-type="bibr" rid="B58">Margaritoulis et&#xa0;al., 2003</xref>; <xref ref-type="bibr" rid="B52">Lazar et&#xa0;al., 2004</xref>; <xref ref-type="bibr" rid="B92">Zbinden et&#xa0;al., 2008</xref>).</p>
<p>A large variety of marine organisms have the ability to colonize surfaces and develop encrusting communities (<xref ref-type="bibr" rid="B80">Sch&#xe4;rer, 2003</xref>). These organisms are called epibiotic if they live or grow attached to other living organisms (called &#x201c;basibionts&#x201d;), such as corals, shelled mollusks, decapod crustaceans, sea turtles and cetaceans (<xref ref-type="bibr" rid="B89">Wahl, 1989</xref>; <xref ref-type="bibr" rid="B72">Ramos-Rivera et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B87">Ten et&#xa0;al., 2022</xref>). The most common epibionts include cirripedes (Crustacea, Cirripedia), which exhibit high diversity (<xref ref-type="bibr" rid="B5">Bille and Spitzner, 2021</xref>) and live in a great variety of natural (and also artificial) substrates, including rocky shores, mangroves, deep-sea hydrothermal vents and cold seeps (<xref ref-type="bibr" rid="B24">Darwin, 1854</xref>; <xref ref-type="bibr" rid="B3">Anderson and Underwood, 1994</xref>; <xref ref-type="bibr" rid="B20">Chan et&#xa0;al., 2021</xref>). Cirripedes are also often the dominant component of biofouling on hard substrates (both natural and artificial), as they are perfectly adapted to sessile life. This high degree of adaptability is due to their peculiar larval stage (cypris). Indeed, <xref ref-type="bibr" rid="B23">Crisp (1984)</xref> stated that they are &#x201c;<italic>the top of the evolution of sessile organisms.</italic>&#x201d; The members of the superfamily Coronuloidea Leach, 1817 are currently divided into five families, namely, Austrobalanidae Newman &amp; Ross, 1976, Bathylasmatidae Newman &amp; Ross, 1971, Chelonibiidae Pilsbry, 1916, Coronulidae Leach, 1817 and Tetraclitidae Gruvel, 1903. Some of these species are obligate commensals of sea turtles and cetaceans, while other are more generalist species. The so called &#x201c;turtle barnacles&#x201d; indicate barnacle species that exclusively or preferentially live on carapace, plastron or skin of chelonians (<xref ref-type="bibr" rid="B77">Ross and Newman, 1967</xref>; <xref ref-type="bibr" rid="B76">Ross and Frick, 2011</xref>; <xref ref-type="bibr" rid="B43">Hayashi et&#xa0;al., 2013</xref>). It has been demonstrated that chelonibiids have been turtle-dwelling species for more than 30 million years (<xref ref-type="bibr" rid="B22">Collareta et&#xa0;al., 2023</xref>).</p>
<p>Sea turtles host a considerable variety of epibiont communities (including ectoparasites) of algae and invertebrates (<xref ref-type="bibr" rid="B8">Caine, 1986</xref>; <xref ref-type="bibr" rid="B50">Kitsos et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B75">Robinson et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B82">Serio et&#xa0;al., 2020</xref>). The qualitative and quantitative composition of epibionts can offer indications on the ecology, behavior and health status of their hosts (<xref ref-type="bibr" rid="B49">Killingley and Lutcavage, 1983</xref>; <xref ref-type="bibr" rid="B33">Flint et&#xa0;al., 2009</xref>; <xref ref-type="bibr" rid="B67">Pfaller et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B29">Doell et&#xa0;al., 2017</xref>). For example, one recent study suggested that epibionts can be an indication of the foraging regions used by <italic>C. caretta</italic> and specialized habitat use (<xref ref-type="bibr" rid="B83">Silver-Gorges et&#xa0;al., 2021</xref>). Furthermore, quali-quantitative composition of barnacle species found on the body, as well as the chemical analysis of their shells, may provide useful information on different biological and ecological aspects of sea turtles (<xref ref-type="bibr" rid="B44">Hayashi and Tsuji, 2008</xref>). However, the paucity of knowledge about different life aspects of barnacles, such as growth rates and age determination, limit the utilization of barnacles as ecological indicators. Some studies have demonstrated that barnacles serve as effective environmental indicators, capturing variations such as water flow strength in estuaries &#x2013; where they display phenotypic plasticity in response to flow (<xref ref-type="bibr" rid="B74">Reustle et&#xa0;al., 2023</xref>) - and the prevalence of microplastics in their environment (<xref ref-type="bibr" rid="B93">Zhang et&#xa0;al., 2022</xref>). Moreover, it was demonstrated, for example, that data on spatio-temporal patterns of sea turtles can be inferred through analyses of chemical composition of the barnacle shells. This happens because the chemical composition varies according to different chemical-physical parameters, such as salinity and temperature of the different water body masses that the sea turtle has gone through during its life and the barnacles were exposed to (<xref ref-type="bibr" rid="B49">Killingley and Lutcavage, 1983</xref>). Sea turtles are used by barnacles as an attachment substrate that can optimize, thanks to the swimming movements of the sea turtle, the suspension and filter feeding strategies (<xref ref-type="bibr" rid="B37">Frick et&#xa0;al., 2002</xref>; <xref ref-type="bibr" rid="B36">Frick et&#xa0;al., 2004</xref>). More than 15 species of corolunoid were recorded as epibionts on sea turtles, with members of the genera <italic>Chelonibia</italic> Leach, 1817, <italic>Platylepas</italic> Gray, 1825, <italic>Chelolepas</italic> Ross &amp; Frick, 2007, <italic>Cylindrolepas</italic> Pilsbry, 1916, <italic>Stomatolepas</italic> Pilsbry, 1910, <italic>Stephanolepas</italic> Fischer, 1886, and <italic>Calyptolepas</italic> Frick, Zardus &amp; Lazo-Wasem, 2010. Furthermore, of all the genera mentioned above, the last five were found only on sea turtles (<xref ref-type="bibr" rid="B10">Carriol and Vader, 2002</xref>; <xref ref-type="bibr" rid="B38">Frick et&#xa0;al., 2010a</xref>; <xref ref-type="bibr" rid="B39">Frick et&#xa0;al., 2010b</xref>; <xref ref-type="bibr" rid="B40">Frick et&#xa0;al., 2011</xref>). A study showed that stranded turtles were in bad health conditions with epibiont loads significantly higher than those of nesting or foraging turtles (<xref ref-type="bibr" rid="B26">Deem et&#xa0;al., 2009</xref>). Previous reports have suggested an increased occurrence of <italic>Chelonibia testudinaria</italic> (Linnaeus, 1758) on turtles found in benthic habitats of the continental shelf, where turtle density is usually high (<xref ref-type="bibr" rid="B17">Casale et&#xa0;al., 2004a</xref>; <xref ref-type="bibr" rid="B19">Casale et al., 2004b</xref>; <xref ref-type="bibr" rid="B21">Collareta and Bianucci, 2021</xref>). Barnacle&#x2013;turtle associations has been considered a borderline symbiotic relationship between mutualism and parasitism. This association is not considered a phoresis, where an organism (phoretic) attaches itself to another (host) for the purpose of travel (<xref ref-type="bibr" rid="B90">White et&#xa0;al., 2018</xref>). Rather, this association is usually considered a case of commensalism, which literally means &#x201c;feeding at a common table&#x201d; (<xref ref-type="bibr" rid="B88">Van Beneden, 1878</xref>). In this association, the commensal (barnacles) benefits and the other (turtle) remains unaffected. However, this relationship can assume other nuances depending on the health status of the sea turtle and of the barnacle species involved. Different factors, such as environmental, physiological and behavioral ones, determine the recruitment of barnacle species and their survival on sea turtles; while the relationship between barnacles&#x2019; density, spatial distribution and size and sea turtle health condition has only rarely been demonstrated (<xref ref-type="bibr" rid="B63">N&#xe1;jera-Hillman et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B78">Rubin et&#xa0;al., 2016</xref>). In all cases, commensalism is rarely reported as obligate and specific (<xref ref-type="bibr" rid="B89">Wahl, 1989</xref>) and no benefits to sea turtles have been demonstrated by the association with barnacles, though some authors have suggested that barnacle coverage may provide a disruptive camouflage (<xref ref-type="bibr" rid="B89">Wahl, 1989</xref>; <xref ref-type="bibr" rid="B51">Kobayashi, 2000</xref>). In most cases of association, the presence of barnacles on the body of sea turtles is benign under normal conditions and chemical signaling from host to commensal may be a key element (<xref ref-type="bibr" rid="B91">Zardus and Hadfield, 2004</xref>). In other cases, chronically debilitated specimens of <italic>C. caretta</italic> showed a heavy barnacle&#x2019;s coverage (<xref ref-type="bibr" rid="B26">Deem et&#xa0;al., 2009</xref>; <xref ref-type="bibr" rid="B85">Stacy et&#xa0;al., 2018</xref>). These specimens are characterized by lethargy and emaciation, and often show various injuries and trauma caused by hooks and other fishing gears and by collision with boats (<xref ref-type="bibr" rid="B11">Casal and Or&#xf3;s, 2009</xref>). Unlike specimens not affected by Debilitative Turtle Syndrome (DTS) the ones ill-affected have significantly lower body condition index, with altered parameters in total white blood cell (WBC) count, glucose (Glc), total protein, calcium (Ca), respiratory burst, etc. (<xref ref-type="bibr" rid="B85">Stacy et&#xa0;al., 2018</xref>).</p>
<p>It is still unclear if massive barnacle aggregations occurring in some debilitated or sick sea turtles are responsible for the death of their host. In this regard, some authors suggested that such specimens were already in poor health conditions due to other factors prior to the massive colonization of epibionts (<xref ref-type="bibr" rid="B26">Deem et&#xa0;al., 2009</xref>; <xref ref-type="bibr" rid="B65">Novarini et&#xa0;al., 2009</xref>). In fact, when in good health conditions, sea turtles regularly participate in symbiotic cleaning associations with shrimps, crabs and fishes (<xref ref-type="bibr" rid="B25">Davenport, 1994</xref>; <xref ref-type="bibr" rid="B57">Losey et&#xa0;al., 1994</xref>; <xref ref-type="bibr" rid="B27">Dellinger et&#xa0;al., 1997</xref>; <xref ref-type="bibr" rid="B35">Frick and Slay, 2000</xref>; <xref ref-type="bibr" rid="B36">Frick et&#xa0;al., 2004</xref>; <xref ref-type="bibr" rid="B79">Sazima et&#xa0;al., 2010</xref>) and scrape off epibionts by rubbing the body underwater against hard structures (<xref ref-type="bibr" rid="B34">Frick and McFall, 2007</xref>). This behavior helps to control epibiont colonization (<xref ref-type="bibr" rid="B81">Schofield et&#xa0;al., 2006</xref>). Extensive seasonal migrations may also affect the quali-quantitative composition of the epibiotic community in healthy turtles (<xref ref-type="bibr" rid="B73">Reich et&#xa0;al., 2010</xref>). Many of the factors that affect barnacle colonization on sea turtles are environmental, including water flow rate, which has a major influence on settlement variability. Furthermore, the competition and hence the distribution among barnacle species can be affected by the different hydrodynamic areas on the carapace, characterized by different flow patterns and drag (<xref ref-type="bibr" rid="B55">Logan and Morreale, 1994</xref>; <xref ref-type="bibr" rid="B63">N&#xe1;jera-Hillman et&#xa0;al., 2012</xref>). The presence of different barnacle species in different microhabitats represented by different body parts of the sea turtles indicated their niche partitioning (<xref ref-type="bibr" rid="B61">Motlagh et&#xa0;al., 2020</xref>). A large number of epibionts were recorded on sea turtles, and especially on <italic>C. caretta</italic>. However, despite the important information that they can provide on sea turtles&#x2019; life aspects, the relationships between barnacles, and between them and their host, are still poorly known. <xref ref-type="bibr" rid="B16">Casale et&#xa0;al. (2012a)</xref> demonstrated that barnacle&#x2019;s species composition on sea turtles collected at Lampedusa (central Mediterranean Sea, Italy) varies not only among different geographic areas, but also among different habitats within the same geographic area. Indeed, it was demonstrated for some barnacle&#x2019;s species their presence in association with different habitats frequented by sea turtles: e.g. pelagic vs. benthic ones (<xref ref-type="bibr" rid="B17">Casale et&#xa0;al., 2004a</xref>).</p>
<p>With the present study on the epibiotic community of cirripeds associated with loggerhead sea turtles in the Adriatic Sea, we aim to provide important new data on the localization and abundance of barnacles that can be useful to infer on health condition and biological and ecological aspects of <italic>C. caretta</italic> specimens. Data here provide baseline information that is important for the development of conservation strategies and management of endangered sea turtles species. Indeed, epibionts can be used to better understand geographical distribution, migration routes, habitat preferences, as well as health status of sea turtles.</p>
</sec>
<sec id="s2" sec-type="materials|methods">
<title>Material and methods</title>
<p>A total of 117 dead loggerhead sea turtles (<italic>Caretta caretta</italic>) found stranded in varying conditions and states of preservation were analyzed from 2020 to 2022 to assess barnacle loads. Specimens were found beached along the North Adriatic coast (along the stretch of coast that extends from the mouth of the river Po to the mouth of the Reno, for a total length of about 28 km) and transported to the Istituto Zooprofilattico Sperimentale della Lombardia e dell&#x2019;Emilia Romagna (IZSLER) for routinary necropsy analyses. Before conducting the necropsy, we assessed the condition of the carcasses. Ideally, necropsies were carried out on fresher carcasses. Our study is based on carcasses categorized as code 1 (fresh carcass, less than 24 hours <italic>post mortem</italic>) or code 2 (moderate decomposition), following the standardized necropsy protocols NETCET (<xref ref-type="bibr" rid="B70">Poppi and Marchiori, 2013</xref>).</p>
<p>Sampling for epibionts was conducted by collecting barnacles from the dorsal and ventral area of each turtle, recording position on the body and the area occupied for each barnacle. Barnacles were collected by scraping the carapace and skin with a bistoury and were immediately preserved in 70% ethanol. A total of 26,498 cirripeds were collected on the 117 dead specimens of <italic>C. caretta</italic>; of this, a total of 3,464 (13.1%) specimens were randomly selected for measurement (width and length in mm) and identification to species level, following the identification key provided by <xref ref-type="bibr" rid="B46">Igi&#x107; (2007)</xref>. This percentage of barnacles is hence representative of the total number of barnacles present on sea turtles analyzed. These data were used to calculate species composition, abundance and determine position of barnacles for each sea turtle.</p>
<p>Photographs of barnacles on different body parts of <italic>C. caretta</italic> were analyzed before removal using ImageJ, a java-based analysis software, that allowed us to identify the specific position of each barnacle on carapace, plastron and other parts of turtle bodies, and size of each barnacle. The initial step involved establishing the measurement scale. To achieve this, an ABFO scale was added to each photograph. Using the &#x201c;line&#x201d; tool, a straight line was drawn between two points of known distance on the ABFO scale. The line was then selected, and the &#x201c;Analyze&#x201d; &gt; &#x201c;Set Scale&#x201d; option was chosen. In the &#x201c;Set Scale&#x201d; window, the length of the line in pixels was displayed. Subsequently, the known distance and units of measurement were entered into the appropriate fields. From that point on, measurements were displayed using these settings. If the pixel-to-length relationship was previously determined through another measurement, this information could be directly inputted into the &#x201c;Set Scale&#x201d; window. Following this procedure for each barnacle, both length and width were measured. To take measurements, the &#x201c;line&#x201d; tool was selected, and a single click was made to specify the starting point on the edge of the barnacle. Then, the mouse was dragged to the opposite edge of the barnacle to determine the endpoint.</p>
<p>Each specimen of <italic>C. caretta</italic> was measured to the nearest 0.1 cm using a soft tape considering its curved carapace length (CCL) and assigned to a specific life stage: juveniles (CCL 15&#x2013;50 cm), subadults (CCL 51&#x2013;77 cm) and adults (CCL&gt;77 cm) (<xref ref-type="bibr" rid="B66">Peckham et&#xa0;al., 2007</xref>).</p>
<p>Two-way ANOVA (&#x3b1; = 0.05) was used to compare the abundance of barnacles in relation to body size of <italic>C. caretta</italic> (CCL in cm).</p>
<p>One-sample Wilcoxon test (&#x3b1; = 0.05) was used to compare the overall barnacle&#x2019;s abundance in different body parts of <italic>C. caretta</italic>: head-neck, carapace, plastron, forelimbs, hindlimbs and tail.</p>
<p>A two-way ANOVA (&#x3b1; = 0.05) was performed to compare barnacle&#x2019;s abundance in different body parts of <italic>C. caretta</italic> per each species.</p>
<p>A paired t-test (&#x3b1; = 0.05) was used to compare the barnacle load of <italic>C. caretta</italic> affected by DTS (Debilitative Turtle Syndrome) versus unaffected specimens. To assess if the turtles were affected by the DTS, the recovery center, where the individuals were hospitalized, conducted a clinical examination. Animals with severely damaged skin, anemic, hyporeactive, and completely colonized by barnacles were considered to have DTS.</p>
</sec>
<sec id="s3" sec-type="results">
<title>Results</title>
<p>The total number of <italic>C. caretta</italic> specimens analyzed was 117. Most of these were juveniles (55.6% of 117, equivalent to 65 turtles), followed by subadults (35.9% of 117, equivalent to 42 turtles), with only a small proportion being adults (8.5% of 117, equivalent to 10 turtles). We identified six different species and five genera of cirripeds, namely: <italic>Amphibalanus eburneus</italic> (Gould, 1841), <italic>Chelonibia caretta</italic> (Spengler, 1790), <italic>Chelonibia testudinaria</italic> (Linnaeus, 1758), <italic>Lepas anatifera Linnaeus</italic>, 1758, <italic>Platylepas hexastylos</italic> (Fabricius, 1798) and <italic>Stomatolepas elegans</italic> (Costa, 1838). Eleven out of one hundred seventeen specimens examined showed DTS (Debilitative Turtle Syndrome). All these DTS specimens were juveniles with a CCL ranging from 17.5 to 24.5 cm.</p>
<p>There was no correlation between the size of the sea turtles and the number of Cirripedia they carried [F (2, 4) = 3.903, p = 0.1148)] (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). On the contrary, the overall barnacle abundance was statistically different depending on the body part (W = 21.00, p = 0.0312), with most barnacles (52,9%) concentrated on the carapace (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>). The majority of barnacles was specifically located on the costal (41,7%) and vertebral scutes (31,4%). Another aspect highlighted during barnacle inspection was the marked aggregation behavior of barnacles (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref>).</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Distribution of barnacles found on dead loggerhead turtles stranded in the North Adriatic coast from 2020-2022, across different turtle curved carapace lengths (CCL in cm).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g001.tif"/>
</fig>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>
<bold>(A, B)</bold> Total barnacle distribution (all species) on <italic>Caretta caretta</italic>, dorsal and ventral body surface; <bold>(C, D)</bold> barnacle distribution on <italic>C. caretta</italic> carapace and plastron.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g002.tif"/>
</fig>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>Barnacle aggregation (all species, with prevalence of <italic>C. testudinaria</italic>) on the carapace of <italic>C. caretta</italic> <bold>(A)</bold> detail of posterior <bold>(B)</bold> and anterior <bold>(C)</bold> part of the body.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g003.tif"/>
</fig>
<p>The most abundant cirriped was <italic>C. testudinaria</italic> (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>). This barnacle was present in 90.6% of specimens of sea turtle studied, and was the most abundant on the carapace (~59%), followed by the fore limbs (~15%), plastron (~13%), hind limbs (~9%), head/neck (~4%) and tail (&lt;1%). Furthermore, some specimens of <italic>C. caretta</italic> also carried <italic>C. testudinaria</italic> complemental males (<xref ref-type="bibr" rid="B91">Zardus and Hadfield, 2004</xref>) (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5</bold>
</xref>). The second most abundant cirriped was <italic>Platylepas hexastylos</italic> (Fabricius, 1798), found in 45.3% of specimens of <italic>C. caretta</italic> analyzed. Unlike <italic>C. testudinaria</italic>, it was found to be more abundant in the soft parts of the turtle represented by the skin (e.g., head, neck, fore- and hind limbs, tail) (<xref ref-type="fig" rid="f6">
<bold>Figure&#xa0;6</bold>
</xref>) than hard parts (carapace and plastron). Similar to <italic>C. testudinaria</italic>, <italic>Chelonibia caretta</italic> was also primarily found on the carapace, albeit in lower abundance and less common compared to its congeneric species (it was found only in 13.7% of specimens studied). On the other hand, <italic>Stomatolepas elegans</italic> was found exclusively on soft parts (<xref ref-type="fig" rid="f7">
<bold>Figure&#xa0;7</bold>
</xref>), and only in 5.1% of studied specimens of <italic>C. caretta</italic>. <italic>Lepas anatifera</italic> (order Scalpellomorpha) was also identified (in 0.85% of studied specimens); this species was found on the carapace only in low abundance. Finally, similarly to <italic>L. anatifera</italic>, <italic>Amphibalanus eburneus</italic> (Gould, 1841) was recorded in low abundance and on the carapace only, in 0.85% of investigated specimens. The abundance/preference of the different barnacle species per body part was statistically significant (F (5, 25) = 3.537, p = 0.0149). <italic>Chelonibia testudinaria</italic> exhibited a well-distributed abundance across all the size classes examined, as shown in <xref ref-type="fig" rid="f8">
<bold>Figure&#xa0;8</bold>
</xref>.</p>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>Abundance of barnacles collected on <italic>C. caretta</italic> specimens.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g004.tif"/>
</fig>
<fig id="f5" position="float">
<label>Figure&#xa0;5</label>
<caption>
<p>Complemental males on <italic>Chelonibia testudinaria</italic> indicated by red arrows.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g005.tif"/>
</fig>
<fig id="f6" position="float">
<label>Figure&#xa0;6</label>
<caption>
<p>Aggregation of <italic>Platylepas</italic> hexastylos on the skin of <italic>C. caretta</italic>. Anterior part of the body.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g006.tif"/>
</fig>
<fig id="f7" position="float">
<label>Figure&#xa0;7</label>
<caption>
<p>Aggregation of <italic>Stomatolepas elegans</italic> on the skin of <italic>C. caretta</italic>.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g007.tif"/>
</fig>
<fig id="f8" position="float">
<label>Figure&#xa0;8</label>
<caption>
<p>Barnacles size per species found on <italic>C. caretta</italic>; only the three most abundant species are showed.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g008.tif"/>
</fig>
<p>Finally, evidence (t = 3.767, df = 5, p = 0.0131) does show a link between turtles affected by DTS&#x2013; so small individuals &#x2013; and the prevalence of epibionts (<xref ref-type="fig" rid="f9">
<bold>Figure&#xa0;9</bold>
</xref>). In terms of the size, the largest cirriped species recorded was <italic>Chelonibia testudinaria</italic> (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>). Indeed, specimens affected by DTS exhibited a significant barnacle infestation on all body parts, markedly higher than the specimens of <italic>C. caretta</italic> not affected by DTS (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>).</p>
<fig id="f9" position="float">
<label>Figure&#xa0;9</label>
<caption>
<p>
<bold>(A)</bold> <italic>C. caretta</italic> affected by Debilitative Turtle Syndrome (DTS), dorsal (A1) and ventral (A2) view; <bold>(B)</bold> another specimen of <italic>C. caretta</italic> affected by DTS, dorsal (B1) and ventral (B2) view.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g009.tif"/>
</fig>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Sizes of barnacles collected on <italic>C. caretta</italic> specimens; AL, average length; AW, average width; LR, length range; WR, width range.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" align="center">
Species
</th>
<th valign="middle" align="center">
AL (cm)
</th>
<th valign="middle" align="center">
AW (cm)
</th>
<th valign="middle" align="center">
LR (cm)
</th>
<th valign="middle" align="center">
WR (cm)
</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="middle" align="left">
<italic>Chelonibia testudinaria</italic> (Linnaeus, 1758)</td>
<td valign="middle" align="center">1.54</td>
<td valign="middle" align="center">1.3</td>
<td valign="middle" align="center">0.1&#x2013;5.16</td>
<td valign="middle" align="center">0.07&#x2013;4.85</td>
</tr>
<tr>
<td valign="middle" align="left">
<italic>Chelonibia caretta</italic> (Spengler, 1790)</td>
<td valign="middle" align="center">1.07</td>
<td valign="middle" align="center">0.92</td>
<td valign="middle" align="center">0.12&#x2013;2.92</td>
<td valign="middle" align="center">0.16&#x2013;2.63</td>
</tr>
<tr>
<td valign="middle" align="left">
<italic>Platylepas hexastylos</italic> (Fabricius, 1798)</td>
<td valign="middle" align="center">0.78</td>
<td valign="middle" align="center">0.71</td>
<td valign="middle" align="center">0.1&#x2013;2.37</td>
<td valign="middle" align="center">0.1&#x2013;2.29</td>
</tr>
<tr>
<td valign="middle" align="left">
<italic>Amphibalanus eburneus</italic> (Gould, 1841)</td>
<td valign="middle" align="center">0.92</td>
<td valign="middle" align="center">0.76</td>
<td valign="middle" align="center">0.44&#x2013;1.75</td>
<td valign="middle" align="center">0.34&#x2013;0.96</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="T2" position="float">
<label>Table&#xa0;2</label>
<caption>
<p>Barnacle abundance on different body parts between <italic>C. caretta</italic> specimens affected by DTS (Debilitative Turtle Syndrome) versus unaffected specimens.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="bottom" align="center"/>
<th valign="middle" colspan="2" align="center">DTS</th>
<th valign="middle" colspan="2" align="center">Unaffected</th>
</tr>
<tr>
<th valign="bottom" align="center"/>
<th valign="middle" align="center">Mean</th>
<th valign="middle" align="center">SD</th>
<th valign="middle" align="center">Mean</th>
<th valign="middle" align="center">SD</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="bottom" align="left">Head-neck</td>
<td valign="middle" align="center">92.27</td>
<td valign="middle" align="center">72.79</td>
<td valign="middle" align="center">6.78</td>
<td valign="middle" align="center">20.38</td>
</tr>
<tr>
<td valign="bottom" align="left">Forelimbs</td>
<td valign="middle" align="center">321.19</td>
<td valign="middle" align="center">198.18</td>
<td valign="middle" align="center">8.19</td>
<td valign="middle" align="center">27.41</td>
</tr>
<tr>
<td valign="bottom" align="left">Carapace</td>
<td valign="middle" align="center">288.27</td>
<td valign="middle" align="center">212.19</td>
<td valign="middle" align="center">102.41</td>
<td valign="middle" align="center">142.58</td>
</tr>
<tr>
<td valign="bottom" align="left">Plastron</td>
<td valign="middle" align="center">232.00</td>
<td valign="middle" align="center">148.51</td>
<td valign="middle" align="center">10.97</td>
<td valign="middle" align="center">27.22</td>
</tr>
<tr>
<td valign="bottom" align="left">Hindlimbs</td>
<td valign="middle" align="center">141.09</td>
<td valign="middle" align="center">122.65</td>
<td valign="middle" align="center">7.08</td>
<td valign="middle" align="center">16.39</td>
</tr>
<tr>
<td valign="bottom" align="left">Tail</td>
<td valign="middle" align="center">17.27</td>
<td valign="middle" align="center">19.49</td>
<td valign="middle" align="center">0.80</td>
<td valign="middle" align="center">2.66</td>
</tr>
<tr>
<td valign="bottom" align="left">Total</td>
<td valign="middle" align="center">1,092.09</td>
<td valign="middle" align="center">539.53</td>
<td valign="middle" align="center">139.23</td>
<td valign="middle" align="center">189.34</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn id="fnT1_1">
<p>DTS, 11 specimens; Unaffected, 106 specimens.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<p>Necropsies conducted on <italic>C. caretta</italic> specimens in 2020 revealed signs of drowning, such as swallowing seawater and having a red neck, as well as the presence of foam in the windpipe (<xref ref-type="fig" rid="f10">
<bold>Figure&#xa0;10</bold>
</xref>).</p>
<fig id="f10" position="float">
<label>Figure&#xa0;10</label>
<caption>
<p>
<italic>Caretta caretta</italic> with evidence of drowning <bold>(A)</bold> swallow and red neck <bold>(B, C)</bold> foam produced in the windpipe.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-10-1243153-g010.tif"/>
</fig>
</sec>
<sec id="s4" sec-type="discussion">
<title>Discussion</title>
<p>This study represents a useful baseline assessment of barnacle species composition, abundance and distribution on loggerhead turtles that forage in the North Adriatic Sea, thereby providing valuable data on the ecology of the species. Indeed, as suggested by <xref ref-type="bibr" rid="B15">Casale et&#xa0;al. (2012b)</xref>, each barnacle species showed marked preferences for hosts frequenting pelagic vs. benthic habitats. Furthermore, as we reported in this research, the different species of cirripeds showed clear preferences for the different parts of the body of the host, as these represent specific microhabitats with different conditions, such as food availability and hydrodynamics. It was demonstrated that juveniles of <italic>C. caretta</italic> undergo a deterministic ontogenetic habitat shift, with immature specimens inhabiting neritic (late stage juveniles) and oceanic (early stage juveniles) waters (<xref ref-type="bibr" rid="B7">Bolten et&#xa0;al., 2003</xref>). However, in some cases, this ontogenetic shift is not well defined among individuals, depending on food availability and specific habitat characteristics (<xref ref-type="bibr" rid="B13">Casale et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B15">Casale et&#xa0;al., 2012b</xref>). In our study, the prevalence of juvenile individuals and the associated composition of barnacles suggested that in the investigated area of the North Adriatic, juveniles of <italic>C. caretta</italic> prefer a benthic feeding behavior to a pelagic one. Indeed, the preference of specific species of barnacles depending on the different habitat frequented by sea turtles was directly and indirectly supported by some authors (e.g., <xref ref-type="bibr" rid="B41">Garc&#xed;a Gallego, 2018</xref>; <xref ref-type="bibr" rid="B86">Ten et&#xa0;al., 2019</xref>). For instance, the high abundance of <italic>C. testudinaria</italic> on turtles frequenting benthic habitats of the continental shelve was suggested by <xref ref-type="bibr" rid="B17">Casale et&#xa0;al., (2004a)</xref>. In these habitats, the turtle density is usually high. In the present study, <italic>C. testudinaria</italic> has been found to be the most abundant species on Adriatic specimens of <italic>C. caretta</italic>. The pattern of distribution of <italic>C. testudinaria</italic> on the plastron of <italic>C. caretta</italic> has not been previously investigated, and scant evidence is available for green turtles (<italic>Chelonia mydas</italic>) (<xref ref-type="bibr" rid="B54">Lazo-Wasem et&#xa0;al., 2011</xref>). In this species, the scraping activity during foraging of seagrasses and algae allow sea turtles to remove (or prevent barnacles from attaching), especially the barnacles of the central area of the plastron. On the other hand, barnacles present on the marginal area of the plastron are more difficult to remove due to their peripheral position (<xref ref-type="bibr" rid="B56">L&#xf3;pez-Mendilaharsu et&#xa0;al., 2005</xref>).</p>
<p>Photographic analysis of our samples showed that barnacles were more abundant in the costal scutes of the carapace (52,9%). This can be explained by the fact that in this area of the body, water flow can be lower compared to other areas, and this allows for a higher potential for barnacle feeding. Likewise, other studies demonstrated that barnacles are more abundant in the vertebral zones compared to marginal ones of the carapace (<xref ref-type="bibr" rid="B59">Matsuura and Nakamura, 1993</xref>; <xref ref-type="bibr" rid="B69">Pfaller et&#xa0;al., 2008</xref>). Carapace hydrodynamics probably affect epibiont distributions, with differential drag and water flow patterns (<xref ref-type="bibr" rid="B55">Logan and Morreale, 1994</xref>). Moreover, resting turtles often place their front flippers over the marginal scutes, which may impede colonization and contribute to the lower density of barnacles there (<xref ref-type="bibr" rid="B68">Pfaller et&#xa0;al., 2006</xref>). Smaller individuals are concentrated in the marginal scutes of the carapace and the largest in the anterior part of carapace. This can happen because of a different potential in feeding due to the water flow. Indeed, barnacles located in the rear and marginal areas of the carapace are subjected to lower water flow than those located in other regions in which it is present a higher water flow (<xref ref-type="bibr" rid="B60">Moriarty et&#xa0;al., 2008</xref>). This latter work also demonstrated that <italic>C. testudinaria</italic> is capable of substantial post-settlement locomotion that generally occurs from areas of relatively low flow to higher ones. The likelihood of cyprid settlement is increased by the lower shear stress environment on the posterior region of the carapace. However, in this position barnacles found no optimal position for feeding: the significative turbulence due to the shape of the shell and to the presence of other epibionts positioned anteriorly makes feeding more difficult and therefore result in slower growth (<xref ref-type="bibr" rid="B62">Mullineaux and Butman, 1991</xref>). Moreover, microeddies due to the presence of adjacent epibionts would alter flow direction, thus reducing the particulate matter amount for barnacles located further to the rear than the others, as particulate matter can be consumed by other barnacles before it reaches them (<xref ref-type="bibr" rid="B68">Pfaller et&#xa0;al., 2006</xref>). <xref ref-type="bibr" rid="B60">Moriarty et&#xa0;al. (2008)</xref> discovered that barnacles change their location relative to other individuals on the same scute, thus exhibiting independent movement from one another, and this behavior occurs frequently. Hence, barnacles settled in non-optimal positions actively seek an alternative, searching for a more favorable position as they grow. This would explain at least in part the high incidence of <italic>C. testudinaria</italic> in the anterior and medial part of the body of sea turtles. This indicates us that to understand the processes that underlie the quali-quantitative distribution of the various species of barnacles (and epibionts in general) on sea turtles it is necessary to consider and study various factors (e.g., biology and ecology of barnacle species, hydrodynamics, environmental parameters, sea turtles&#x2019; behavior). Analysis of photos of dead specimen of <italic>C. caretta</italic> and species identification activity of epibionts showed that <italic>P. hexastylos</italic> and <italic>S. elegans</italic> aggregate on the skin of turtles, whilst <italic>C. testudinaria</italic> and <italic>C. caretta</italic> settle on the carapace and plastron, as demonstrated also by other authors (<xref ref-type="bibr" rid="B17">Casale et&#xa0;al., 2004a</xref>; <xref ref-type="bibr" rid="B16">Casale et&#xa0;al., 2012a</xref>). This can also be explained by different attachment methods of <italic>P. hexastylos</italic> and <italic>S. elegans</italic>, both of which use hook-like structures to anchor themselves to the soft (skin) parts of sea turtle&#x2019;s body. Another important observation is the absence of any correlation between turtle size and the number of barnacles recorded. This could be due to the fact that pheromones released from conspecifics attract cyprid larvae independently of turtle size. Attractive pheromones have been found in several barnacle species (<xref ref-type="bibr" rid="B30">Dreanno et&#xa0;al., 2007</xref>). It is therefore probable that epibiont barnacles, in addition to the chemical signals useful to find their basibiont, also are attracted by aggregation pheromones produced by conspecifics (<xref ref-type="bibr" rid="B64">Nogata and Matsumura, 2006</xref>); more research is necessary to confirm this hypothesis. So, barnacle abundance seems not to be affected by turtle size, while their attachment position seems to be affected mainly by carapace water flow and plastron abrasion against the sea floor, according with <xref ref-type="bibr" rid="B63">N&#xe1;jera-Hillman et&#xa0;al. (2012)</xref>. The only confirmed relationship appears to be between the high number of barnacles and turtles affected by debilitative turtles&#x2019; syndrome (<xref ref-type="bibr" rid="B32">Fern&#xe1;ndez et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B78">Rubin et&#xa0;al., 2016</xref>). DTS has become a growing concern for sea turtles. Turtles with DTS are typically emaciated, anemic, hypoglycemic, and are often completely or almost completely covered by barnacles when caught or find stranded (<xref ref-type="bibr" rid="B32">Fern&#xe1;ndez et&#xa0;al., 2015</xref>). Excessive stationary floating due to debilitation may place the turtle in water conditions and concentrations of plankton ideal for abundant cyprid attachment (<xref ref-type="bibr" rid="B84">Sloan et&#xa0;al., 2014</xref>). This condition was previously shown to typically affect juveniles, a fact confirmed by the CCL measurements taken during necropsy. It has been demonstrated that in these extreme and unique cases, the epibiont load may double the volume and mass in juvenile sea turtles resulting in increased drag caused by the substantial barnacle infestation (<xref ref-type="bibr" rid="B6">Bjorndal et&#xa0;al., 2003</xref>). This could further amplify the potentially negative effects of epibiosis on sea turtles already in bad health condition impeding the ability to forage efficiently. Debilitation results in stationary floating and decreased grooming. Furthermore, debilitated turtle carapaces may in some way be more attractive to barnacle cyprids as they display atypical, multifocal beta keratin thickness and they also present keratin eating copepods on the carapace (<xref ref-type="bibr" rid="B4">Badillo et&#xa0;al., 2006</xref>). On the other hand, sea turtles in good health conditions keep the abundance of epibionts in check exhibiting self-grooming patterns. Indeed, these healthy specimens are usually observed actively rubbing against hard submerged structures to remove epibionts (<xref ref-type="bibr" rid="B45">Heithaus et&#xa0;al., 2002</xref>; <xref ref-type="bibr" rid="B81">Schofield et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B34">Frick and McFall, 2007</xref>). Furthermore, it was suggested that the expenditure of self-grooming behaviors may differ between sick and healthy sea turtles (<xref ref-type="bibr" rid="B78">Rubin et&#xa0;al., 2016</xref>). Another interesting finding is that the communities of barnacles seem to be aggregated. This suggests that when a cypris larva attach on a sea turtle that already carries another individual of the same species, the settlement area is not selected simply by chance but is determined by the previous presence of the epibiont. In other words, the presence of conspecifics on sea turtle acts as an &#x201c;attraction point&#x201d; to other. Like most crustacean species, the reproduction of barnacles is characterized by copulation, although they have the peculiar feature of being sessile organisms when adults. Although barnacles are hermaphroditic species and this increases the opportunities of copulation, in all cases at least two mature individuals of the same species are necessary to be on the same sea turtle at a short distance (<xref ref-type="bibr" rid="B48">Kelly and Sanford, 2010</xref>; <xref ref-type="bibr" rid="B16">Casale et&#xa0;al., 2012a</xref>). Moreover, it is known that <italic>C. testudinaria</italic> needs receptive neighbors for cross-fertilization during breeding (<xref ref-type="bibr" rid="B91">Zardus and Hadfield, 2004</xref>); thus, it is not surprising that barnacles were found to aggregate (<xref ref-type="bibr" rid="B63">N&#xe1;jera-Hillman et&#xa0;al., 2012</xref>). <italic>Chelonibia testudinaria</italic> have been found to have complemental males on their edges, confirming this reproduction strategy and that the conditions for these epibionts were good.</p>
<p>This research underlines the importance of analysis on barnacles attached to sea turtles, as they can provide a variety of information about different ecological and biological aspects of their host, such as migration, health conditions and feeding behavior, helping the scientific community to monitor <italic>C. caretta</italic> populations, and sea turtle populations in general. Although the data here reported comes from specimens sampled in a relatively small area and found dead (although most of them were freshly dead), some studies offer strong quantitative evidence that certain barnacles species have the potential to serve as ecological indicators of habitat (<xref ref-type="bibr" rid="B17">Casale et&#xa0;al., 2004a</xref>; <xref ref-type="bibr" rid="B15">Casale et&#xa0;al., 2012b</xref>; <xref ref-type="bibr" rid="B86">Ten et&#xa0;al., 2019</xref>). The study of the qualitative and quantitative composition and distribution of barnacles on <italic>C. caretta</italic> can also be used to infer the habitat of incidental captures of sea turtles. In the Adriatic Sea a high number of sea turtles are incidentally captured by different fishing gears (<xref ref-type="bibr" rid="B53">Lazar and Tvrtkovic, 1995</xref>; <xref ref-type="bibr" rid="B1">Affronte and Scaravelli, 2001</xref>; <xref ref-type="bibr" rid="B19">Casale et al., 2004b</xref>). Every year, in this area, more than 11,000 sea turtles are captured as bycatch, with the majority being captured by bottom trawlers (<xref ref-type="bibr" rid="B12">Casale, 2011</xref>). Lepadomorph (<italic>Lepas anatifera</italic>) and balanomorph (<italic>Platylepas</italic> spp.) barnacles are more commonly associated with turtles frequenting epipelagic habitats (or floating at sea) and then caught by pelagic longlines or drift nets (<xref ref-type="bibr" rid="B2">Alm&#xf3;n et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B86">Ten et&#xa0;al., 2019</xref>). On the other hand, the other balanomorph barnacles, namely <italic>Chelonibia</italic> spp. and <italic>Stomatolepas elegans</italic>, are more commonly associated with turtles frequenting benthic habitats and then caught by bottom and demersal neritic fishing gears (<xref ref-type="bibr" rid="B19">Casale et al., 2004b</xref>; <xref ref-type="bibr" rid="B86">Ten et&#xa0;al., 2019</xref>). Indeed, the observation that stranded sea turtles had also come into contact with fishing gear is realistic, as interactions with fisheries are the most common cause of mortality among Mediterranean specimens of <italic>C. caretta</italic> (<xref ref-type="bibr" rid="B9">Carreras et&#xa0;al., 2004</xref>). The main cause of mortality due to trawling is forced apnea during trawling activities. This aspect was also demonstrated by our analysis, during which we found several specimens with signs of drowning typically resulting from contact with fishing gear, such as swallowing seawater and having a red neck, as well as the presence of foam in the windpipe.</p>
<p>Previous research on the different communities of barnacles found on sea turtles have recommended that basibiont individuals should be included in epibiont studies only if they can be regarded as representative of normal conditions (<xref ref-type="bibr" rid="B16">Casale et&#xa0;al., 2012a</xref>; <xref ref-type="bibr" rid="B86">Ten et&#xa0;al., 2019</xref>). Indeed, in dead specimens of sea turtles washed ashore for a long period of time, the epibiont community may have been <italic>post-mortem</italic> changed. In our case, most specimens of <italic>C. caretta</italic> were freshly dead, hence the barnacle&#x2019;s communities found on sea turtles&#x2019; body can be considered as representative of &#x201c;normal conditions&#x201d;.</p>
</sec>
<sec id="s5" sec-type="conclusions">
<title>Conclusions</title>
<p>Sea turtles are essential to marine ecosystems: as they maintain habitat health, provide nutrients to other species, control jellyfish populations, and host epibiont communities. Several factors determine the presence, distribution and species composition of barnacles, and epibionts in general, on sea turtles. The process that underlines the dynamics of colonization, localization and reproduction of barnacles are still little known, and have we only begun to understand them quite recently. These biological and ecological processes (e.g., settling, feeding, growth, reproduction) of epibiotic barnacles are strictly linked to behavioral and ecological aspects of sea turtles. Hence, the study of epibiotic fauna of sea turtles, and of other marine organisms, can be considered a cost-effective tool to investigate habitat use and habits of sea turtles, helping to track the habitat shift and migration of sea turtles in the Mediterranean. Using barnacles as ecological indicators is a cost-effective method to aid in sea turtle conservation efforts, providing insights into their ecological aspects like distribution, migration routes, habitat preferences, and health status.</p>
</sec>
<sec id="s6" sec-type="data-availability">
<title>Data availability statement</title>
<p>The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.</p>
</sec>
<sec id="s7" sec-type="ethics-statement">
<title>Ethics statement</title>
<p>Ethical review and approval was not required for the study on animals in accordance with the local legislation and institutional requirements.</p>
</sec>
<sec id="s8" sec-type="author-contributions">
<title>Author contributions</title>
<p>FT: conceptualization; statistical analysis; write the original draft and revised it; scientific supervision; barnacles identification. MB: conceptualization; image analysis; write the original draft and revised it; barnacles identification; data collection. SR: conceptualization; revised the draft; funds; data collection. SI: revised the original draft; images curation. VA: data collection; revised the draft. All authors contributed to the article and approved the submitted version.</p>
</sec>
</body>
<back>
<ack>
<title>Acknowledgments</title>
<p>We are grateful to the ENPA (national animal protection association) in Lagosanto (Ferrara), especially to Marco Pozzi and Viviana Prati; the Fondazione Cetacea in Riccione (Rimini), especially Sauro Pari and the Carabinieri Biodiversit&#xe0; in Punta Marina (Ravenna), in particular Ten. Col. Giovanni Nobili and M.llo Capo Emanuele Battani for their active and collaborative role. We are grateful too to the two reviewers for their valuable suggestions that helped us in improving our manuscript.</p>
</ack>
<sec id="s9" sec-type="COI-statement">
<title>Conflict of interest</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 id="s10" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
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