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 <!DOCTYPE article PUBLIC "-//NLM//DTD JATS (Z39.96) Journal Publishing DTD v1.0 20120330//EN" "http://jats.nlm.nih.gov/publishing/1.0/JATS-journalpublishing1.dtd"> <article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" article-type="research-article" dtd-version="1.0" xml:lang="en">
  <front>
    <journal-meta>
      <journal-id journal-id-type="publisher-id">IMSJ</journal-id>
      <journal-title-group>
        <journal-title>International Marine Science Journal</journal-title>
      </journal-title-group>
      <issn pub-type="epub">2643-0282</issn>
      <publisher>
        <publisher-name>Open Access Pub</publisher-name>
        <publisher-loc>United States</publisher-loc>
      </publisher>
    </journal-meta>
    <article-meta>
      <article-id pub-id-type="doi">10.14302/issn.2643-0282.imsj-19-2672</article-id>
      <article-id pub-id-type="publisher-id">IMSJ-19-2672</article-id>
      <article-categories>
        <subj-group>
          <subject>research-article</subject>
        </subj-group>
      </article-categories>
      <title-group>
        <article-title>Record of Aggregation of Alien Tropical Schyphozoan Rhopilema nomadica Galil, 1990 in the Mediterranean Coast of Egypt</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="author">
          <name>
            <surname>Fedekar</surname>
            <given-names>Fadel Madkour</given-names>
          </name>
          <xref ref-type="aff" rid="idm1842692292">1</xref>
          <xref ref-type="aff" rid="idm1842690708">*</xref>
        </contrib>
        <contrib contrib-type="author">
          <name>
            <surname>Walaa</surname>
            <given-names>Safwat</given-names>
          </name>
          <xref ref-type="aff" rid="idm1842692292">1</xref>
        </contrib>
        <contrib contrib-type="author">
          <name>
            <surname>Mahmoud</surname>
            <given-names>Hassan Hanafy</given-names>
          </name>
          <xref ref-type="aff" rid="idm1842690492">2</xref>
        </contrib>
      </contrib-group>
      <aff id="idm1842692292">
        <label>1</label>
        <addr-line>Marine Science Department, Faculty of Science, Port Said University, Port Said, Egypt</addr-line>
      </aff>
      <aff id="idm1842690492">
        <label>2</label>
        <addr-line>Marine Science Department, Faculty of Science, Suez Canal University, Ismailia, Egypt</addr-line>
      </aff>
      <aff id="idm1842690708">
        <label>*</label>
        <addr-line>Corresponding Author</addr-line>
      </aff>
      <contrib-group>
        <contrib contrib-type="editor">
          <name>
            <surname>Aurelie</surname>
            <given-names>Moulins</given-names>
          </name>
          <xref ref-type="aff" rid="idm1842542116">1</xref>
        </contrib>
      </contrib-group>
      <aff id="idm1842542116">
        <label>1</label>
        <addr-line>CIMA research Foundation, Italy.</addr-line>
      </aff>
      <author-notes>
        <corresp>
    
    Fedekar Fadel Madkour, <addr-line>Marine Science Department, Faculty of Science, Port Said University, Port Said, Egypt</addr-line>, Email: <email>fedekarmadkour@ymail.com</email></corresp>
        <fn fn-type="conflict" id="idm1850807716">
          <p>The authors have declared that no competing interests exist.</p>
        </fn>
      </author-notes>
      <pub-date pub-type="epub" iso-8601-date="2019-03-28">
        <day>28</day>
        <month>03</month>
        <year>2019</year>
      </pub-date>
      <volume>1</volume>
      <issue>2</issue>
      <fpage>1</fpage>
      <lpage>7</lpage>
      <history>
        <date date-type="received">
          <day>16</day>
          <month>02</month>
          <year>2019</year>
        </date>
        <date date-type="accepted">
          <day>27</day>
          <month>03</month>
          <year>2019</year>
        </date>
        <date date-type="online">
          <day>28</day>
          <month>03</month>
          <year>2019</year>
        </date>
      </history>
      <permissions>
        <copyright-statement>© </copyright-statement>
        <copyright-year>2019</copyright-year>
        <copyright-holder>Fedekar Fadel Madkour, et al.</copyright-holder>
        <license xlink:href="http://creativecommons.org/licenses/by/4.0/" xlink:type="simple">
          <license-p>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.</license-p>
        </license>
      </permissions>
      <self-uri xlink:href="http://openaccesspub.org/imsj/article/1049">This article is available from http://openaccesspub.org/imsj/article/1049</self-uri>
      <abstract>
        <p>Recently, annual swarm of invasive Erythrean schyphozoan <italic>Rhopilema</italic><italic>nomadica</italic>Galil, 1990 appeared along Egyptian Mediterranean coasts causing beach closures and fishing problems. The present study conducted survey and field monitoring on <italic>R. nomadica</italic> during blooming season in the Egyptian Mediterranean coast throughout three consecutive years (2015-2017). Three main features of <italic>R. nomadica</italic> bloom were addressed; viz starting date, duration and maximum density of aggregation. In 2015, the bloom started on 28 July, and over the following two years the bloom starting date shifted earlier being 19 July in 2016 and 15 June in 2017. The duration of the bloom varied yearly giving the longest duration in 2017 when the bloom continued in high density for a month. The highest density of <italic>R. nomadica</italic> was about 896 medusae/1000 m<sup>3</sup> in 2017. The medusae diameter ranged between 21 to 112 cm. The average bell diameter for each year displayed gradual increasing values over the years. The consistent annual <italic>R. nomadica</italic> blooming was attributed to the high level of eutrophication and ecosystem degradation occurred along the Mediterranean coast since last decades. The shifting in the annual bloom starting date and duration may reflect the adaptation of <italic>R. nomadica</italic> to the climate change effect on the Mediterranean Sea temperature.</p>
      </abstract>
      <kwd-group>
        <kwd>Rhopilema nomadica</kwd>
        <kwd>Suez Canal</kwd>
        <kwd>invasive species</kwd>
        <kwd>Mediterranean Sea</kwd>
      </kwd-group>
      <counts>
        <fig-count count="4"/>
        <table-count count="1"/>
        <page-count count="7"/>
      </counts>
    </article-meta>
  </front>
  <body>
    <sec id="idm1842535924" sec-type="intro">
      <title>Introduction</title>
      <p>After a decade of the first recorded specimen of <italic>Rhopilema</italic><italic>nomadica</italic> from lsraeli coast in 1976 <xref ref-type="bibr" rid="ridm1842904820">1</xref> and since the mid-1980's, many studies documented the progressive spreading of this species in the                Mediterranean basin either as few specimens or massive swarms. Throughout the last forty years,<italic> R. nomadica</italic> stretched its range sequentially from eastern Levantine Sea off Israeli, Lebanon and Syrian coasts <xref ref-type="bibr" rid="ridm1842970116">2</xref><xref ref-type="bibr" rid="ridm1842978756">3</xref><xref ref-type="bibr" rid="ridm1842755444">4</xref><xref ref-type="bibr" rid="ridm1842761564">5</xref><xref ref-type="bibr" rid="ridm1842740004">6</xref><xref ref-type="bibr" rid="ridm1842743604">7</xref><xref ref-type="bibr" rid="ridm1842727452">8</xref> to northern-east Levantine at Marmara and Aegean seas off Turkey <xref ref-type="bibr" rid="ridm1842731772">9</xref><xref ref-type="bibr" rid="ridm1842704588">10</xref><xref ref-type="bibr" rid="ridm1842701132">11</xref><xref ref-type="bibr" rid="ridm1842700988">12</xref><xref ref-type="bibr" rid="ridm1842712004">13</xref><xref ref-type="bibr" rid="ridm1842708620">14</xref>, passing through Greece and                 Malta <xref ref-type="bibr" rid="ridm1842683804">15</xref><xref ref-type="bibr" rid="ridm1842679916">16</xref> and ending at the westernmost Mediterranean of the Italian island of Sardinia and Tunisia <xref ref-type="bibr" rid="ridm1842677036">17</xref><xref ref-type="bibr" rid="ridm1842687908">18</xref>.</p>
      <p>Since the first appearance of <italic>R. nomadica</italic> in the eastern Mediterranean Sea in 1976 <xref ref-type="bibr" rid="ridm1842904820">1</xref>, and even though <italic>R. nomadica</italic> purportedly entered to the Mediterranean via Suez Canal <xref ref-type="bibr" rid="ridm1842970116">2</xref>, no scientific publication documented the blooming of <italic>R</italic>.<italic> nomadica</italic> in the Egyptian coast. In 2016, a short article pointed to the presence of <italic>R</italic>.<italic> nomadica</italic> bloom in the Egyptian coast during summer 2015 <xref ref-type="bibr" rid="ridm1842642860">19</xref>. Otherwise, Avian et al. <xref ref-type="bibr" rid="ridm1842743604">7</xref> in their study              on nematocysts of <italic>R. nomadica</italic> in the Eastern Mediterranean stated, "large aggregations have become ubiquitous of <italic>R</italic>.<italic> nomadica</italic> in the summer and winter months along the Levantine coasts from Egypt to Lebanon". Nevertheless, the presence of <italic>R. nomadica</italic> in the Egyptian coast as mentioned in Avian et al.                       study <xref ref-type="bibr" rid="ridm1842743604">7</xref> lack evidence. Although the first scientific record of <italic>R. nomadica</italic> blooms from the Egyptian coast was in 2015 <xref ref-type="bibr" rid="ridm1842642860">19</xref>, it has actually occurred before. </p>
      <p>However, during last two decades, great complains from increasing jellyfish appeared within bathers and fishermen along Egyptian Mediterranean coast in summer. The nuisance effect of these blooms and severe stings from similar-looking jellyfish along the Egyptian coast were reported in a local newspaper                   in 22 August 2001 (http://www.ahram.org.eg/Archive/2001/8/22/INVE4.HTM). Although <italic>R</italic>.<italic> nomadica</italic> bloom is known to have both environmental and economic consequences, including injury to bathers causing beach closures and tourism impact, and reduced fishing harvests due to clogging of fishing net <xref ref-type="bibr" rid="ridm1842761564">5</xref>, no attention was paid to study the blooming density, causes and implications of <italic>R</italic>.<italic> nomadica</italic> along Egyptian coast. The present study conducted survey and field monitoring on <italic>R. nomadica</italic> during blooming season in the Egyptian Mediterranean coast throughout three consecutive years. It aimed to give an overview on the main features of the bloom, represented in the maximum density, the starting date and duration of the aggregation.</p>
    </sec>
    <sec id="idm1842527012" sec-type="materials">
      <title>Materials and Methods</title>
      <p>The outbreak of <italic>R.</italic><italic>nomadica </italic>in the eastern Egyptian Mediterranean off Port Said coast (31<bold>°</bold> 16' N, 32<bold>°</bold> 19' E) (<xref ref-type="fig" rid="idm1842591300">Figure 1</xref>) was monitored during blooming period (summer season) of the three consecutive years (2015 to 2017). Dispersed medusaeof<italic> R.</italic><italic>nomadica</italic> were estimated every couple of days at a distance of 1 km inshore using fishermen beach trawling net, with estimate volume of sampled seawater of 1000 m<sup>3</sup> at each haul. The density of jellyfish was calculated from the total number of medusae counted in hauls and expressed as number of medusae/1000 m<sup>3</sup>. Each year, the bell diameter of randomly selected specimens of <italic>R. nomadica </italic>was measured to the nearest cm (the sample size, N, was 505, 97 and 270 specimens for the three consecutive years, respectively). All measured specimens were investigated for the presence/absence of gonads. Surface water temperature was measured <italic>in situ</italic> using thermometer during sample collection.</p>
      <fig id="idm1842591300">
        <label>Figure 1.</label>
        <caption>
          <title> Egyptian Mediterranean off Port Said coast</title>
        </caption>
        <graphic xlink:href="images/image1.jpg" mime-subtype="jpg"/>
      </fig>
    </sec>
    <sec id="idm1842504156" sec-type="results">
      <title>Results </title>
      <p>Jellyfish specimens observed in the water (<xref ref-type="fig" rid="idm1842577364">Figure 2</xref>) and stranded medusa on the beach (<xref ref-type="fig" rid="idm1842576572">Figure 3</xref>) were inspected for species identification and was found to be identical with Galil et al.'s description of <italic>R. nomadica</italic>. The survey was conducted at the onset of <italic>R. nomadica </italic>bloom along Port Said coast in the southeastern Mediterranean of Egypt during the three consecutive years (2015-2017). To evaluate and compare the aggregation of <italic>R. nomadica </italic>per time, three main features were addressed; they are starting date, duration and maximum density of aggregation. There were marked changes over the years in the starting date and duration of the aggregation, but little variation in maximum density of jellyfish (<xref ref-type="fig" rid="idm1842573044">Figure 4</xref>). Considering each of the starting date and duration of the aggregation, in 2015 the bloom started on 28 July, and over the following two years the bloom starting date shifted earlier being 19 July in 2016 and 15 June in 2017. The duration of the bloom varied yearly giving the longest duration in 2017 when the bloom continued with high density for a month, while during the two preceding years (2015 and 2016), the bloom persisted lower period (11 and 7days, respectively), with longer duration in 2015. Considering <italic>R. nomadica</italic> density, the aggregation of jellyfish during these years showed little variation in the maximum density. In 2015, the aggregation peak (866 medusae/1000 m<sup>3</sup>) observed on 29th July. The value of this peak decreased insignificantly throughout the following year 2016, giving about 768 medusae/1000 m<sup>3</sup> on 21st July. Then, increased again in 2017 reaching the highest peak (896 medusae/1000 m<sup>3</sup>) on 17th June (<xref ref-type="fig" rid="idm1842573044">Figure 4</xref>). </p>
      <fig id="idm1842577364">
        <label>Figure 2.</label>
        <caption>
          <title> Adult Rhopilema nomadica in the Mediterranean coast of Egypt. Photo by </title>
        </caption>
        <graphic xlink:href="images/image2.jpg" mime-subtype="jpg"/>
      </fig>
      <fig id="idm1842576572">
        <label>Figure 3.</label>
        <caption>
          <title> Collecting dispersed medusae of R. nomadica from Port Said coast by beach trawling net.</title>
        </caption>
        <graphic xlink:href="images/image3.jpg" mime-subtype="jpg"/>
      </fig>
      <fig id="idm1842573044">
        <label>Figure 4.</label>
        <caption>
          <title> Density of R. nomadica in Egyptian coast off Port Said during bloom period throughout three consecutive years (2015-2017).</title>
        </caption>
        <graphic xlink:href="images/image4.jpg" mime-subtype="jpg"/>
      </fig>
      <p>Bell diameter of the measured specimens ranged between the minimum of 21 cm and the maximum of 112 cm. The average bell diameter for each year displayed gradual increasing values over the years from the lowest average of 42.1+7.78 cm in 2015 and the highest average of 46.26+13.03 cm in 2017 (<xref ref-type="table" rid="idm1842587732">Table 1</xref>). In 2015, most of individuals released their gonads (76%), this was inverted in 2017 when only 30% of the investigated medusae shed their gonads, while in 2016 about half of medusae (48%) were empty from gonads (<xref ref-type="table" rid="idm1842587732">Table 1</xref>). Sea surface temperature (SST) ranges throughout three years were 25-31 °C in 2015, 24-33°C in 2016 and 29-38°C in 2017 (<xref ref-type="table" rid="idm1842587732">Table 1</xref>).</p>
      <table-wrap id="idm1842587732">
        <label>Table 1.</label>
        <caption>
          <title> Seawater temperature, medusae diameter and gonads presence/absence of R. nomadica in the Egyptian coast off Port Said, during three consecutive years (2015-2017).</title>
        </caption>
        <table rules="all" frame="box">
          <tbody>
            <tr>
              <td colspan="2">Year</td>
              <td>2015</td>
              <td>2016</td>
              <td>2017</td>
            </tr>
            <tr>
              <td colspan="2">Temperature range (°C)</td>
              <td>25-31</td>
              <td>24-33</td>
              <td>29-38</td>
            </tr>
            <tr>
              <td>Medusa diameter (cm)</td>
              <td>Min.</td>
              <td>21</td>
              <td>25</td>
              <td>28</td>
            </tr>
            <tr>
              <td/>
              <td>Max.</td>
              <td>66</td>
              <td>68</td>
              <td>112</td>
            </tr>
            <tr>
              <td/>
              <td>Mean</td>
              <td>42.1 ± 7.78</td>
              <td>43.59±8.42</td>
              <td>46.26±13.03</td>
            </tr>
            <tr>
              <td>Gonad</td>
              <td>Presence (%)</td>
              <td>122 (24 %)</td>
              <td>50 (52 %)</td>
              <td>189 (70 %)</td>
            </tr>
            <tr>
              <td/>
              <td>Absence (%)</td>
              <td>383 (76 %)</td>
              <td>47 (48 %)</td>
              <td>81 (30 %)</td>
            </tr>
          </tbody>
        </table>
      </table-wrap>
    </sec>
    <sec id="idm1842491636" sec-type="discussion">
      <title>Discussion</title>
      <p>Of the all studies carried out on the proliferation of <italic>R. nomadica</italic> along the Mediterranean basin from the southeastern side to the most western side since its appearance in the mid 1970s <xref ref-type="bibr" rid="ridm1842904820">1</xref> up to date, few studies documented its massive occurrence on the coasts. Huge swarms of this species started to appear since late 1980s and were restricted to eastern Levantine Sea off Israeli coast <xref ref-type="bibr" rid="ridm1842978756">3</xref><xref ref-type="bibr" rid="ridm1842761564">5</xref>, Lebanon and Syria coasts <xref ref-type="bibr" rid="ridm1842755444">4</xref>, and the Turkey coast at Mersin and Iskendurun Bay <xref ref-type="bibr" rid="ridm1842731772">9</xref><xref ref-type="bibr" rid="ridm1842704588">10</xref>. Afterward, scattered individuals have only been occasionally recorded in the central Mediterranean (Maltese islands, Italian island of Pantelleria and Sardinia), <xref ref-type="bibr" rid="ridm1842679916">16</xref><xref ref-type="bibr" rid="ridm1842639044">20</xref><xref ref-type="bibr" rid="ridm1842650060">21</xref><xref ref-type="bibr" rid="ridm1842648188">22</xref>. While in the most western Mediterranean, <italic>R. nomadica</italic> was consistently recorded each summer since 2010 within the Gulf of Tunis <xref ref-type="bibr" rid="ridm1842687908">18</xref>, then during 2014-2016, outbreaks of <italic>R. nomadica</italic> started to be established in Bizerte Lagoon, Tunisia <xref ref-type="bibr" rid="ridm1842687908">18</xref>. </p>
      <p>In the present study, the maximum density of <italic>R. nomadica</italic> outbreak (896 medusae/1000 m<sup>3</sup>) was close to those recorded in Israeli coast during 1990 (10 medusae/ m<sup>3</sup><xref ref-type="bibr" rid="ridm1842978756">3</xref>). It was much higher than those recorded in Israeli coast during summer 1989 (160,000 medusae/ km<sup>2</sup><xref ref-type="bibr" rid="ridm1842761564">5</xref>), Turkey coast during summer 1995 (38,000 medusae per square nautical mile <xref ref-type="bibr" rid="ridm1842731772">9</xref> or in Tunisia coast (4.4 medusae/ km<sup>2</sup><xref ref-type="bibr" rid="ridm1842687908">18</xref>). The rapid proliferation of <italic>R. nomadica </italic>in the eastern                      Mediterranean had been related to its high reproductive potential where one settled polyp of this species could produce more than 100 ephyrae within 2 months <xref ref-type="bibr" rid="ridm1842761564">5</xref>. The strobilation process of the species’ polyps of<italic> R. nomadica</italic> seems to be temperature dependence where the synchronization of life cycle and annual occurrence of <italic>R. nomadica</italic> may be controlled by seasonal variations in water temperature regimes <xref ref-type="bibr" rid="ridm1842740004">6</xref>. In the present study, the recorded ranges (24-38°C) of sea temperature throughout the three years seems to be highly convenient for attaining the highest blooming density of <italic>R. nomadica</italic> ever recorded before along the Mediterranean. Moreover, decreasing the percentage of individuals that released their gonads with the increasing of sea temperature, suggesting that increasing temperature may induce influx of the <italic>R. nomadica</italic> swarms from the deep sea to the coast, to be stranded, before releasing their gonads. </p>
      <p>Swarming of jellyfish in the Mediterranean Sea had been suggested to have positive correlation with pollution <xref ref-type="bibr" rid="ridm1842648188">22</xref><xref ref-type="bibr" rid="ridm1842627108">23</xref>. These findings relate jellyfish blooms to the ability of medusae to utilize plankton blooms produced by pollution-caused eutrophication, or by their ability to utilize pollutants directly as food. Another positive correlation between swarming of jellyfish and certain climate change was also found <xref ref-type="bibr" rid="ridm1842622572">24</xref>. For <italic>R. nomadica</italic>, previously recorded outbreaks in the coastal waters of Israel <xref ref-type="bibr" rid="ridm1842761564">5</xref>, Turkey <xref ref-type="bibr" rid="ridm1842731772">9</xref> and Tunisia <xref ref-type="bibr" rid="ridm1842677036">17</xref> were related to degraded ecosystem in addition to climatic changes, in agreement with Purcell’s proposal <xref ref-type="bibr" rid="ridm1842619260">25</xref> who stated that jellyfish can be used as indicators of global warming. Also, the establishment of a viable <italic>R. nomadica</italic> population within the Bizerte lagoon, as opposed to a more ephemeral occurrence within the other central Mediterranean areas, have been attributable to the lagoon trophic status (less oligotrophic) and by virtue of the sheltered nature of the lagoon <xref ref-type="bibr" rid="ridm1842687908">18</xref>. In the same context, the Egyptian Mediterranean coast had sever pollution impact throughout the last decades because of continuous effluents from the coastal lagoons that connected to the sea. The Egyptian Mediterranean coast receives huge volumes of wastewaters every year loaded by variable amounts and types of pollutants, in addition to great amount of nitrogenous and phosphorous compounds through these lagoons <xref ref-type="bibr" rid="ridm1842616524">26</xref>. This situation promotes high level of eutrophication and ecosystem degradation along the Mediterranean coast, providing a great opportunity for consistent annual <italic>R. nomadica</italic> blooming. </p>
      <p>The present study revealed that the annual massive occurrence of <italic>R. nomadica</italic> showed continuous shifting in the starting date with time towards the less warm months experienced in the study area. It shifted over the three years from end of July in 2015 to be during mid-June in 2017. When tracing the past observations on the aggregation dates and duration of <italic>R. nomadica</italic> bloom in other locations of the     Mediterranean basin, a clear change was noticed. In Israeli coast, Mass swarming of <italic>R. nomadica</italic> used to occur mostly in the summer particularly mid-August and ending between September and November <xref ref-type="bibr" rid="ridm1842740004">6</xref>. This change in the annual bloom starting date and duration can be explained in the light of the assumption that the <italic>R. nomadica</italic> adapted itself to the climate change effect on the Mediterranean Sea temperature. Increasing temperature with time was obvious from recorded temperature ranges (<xref ref-type="table" rid="idm1842587732">Table 1</xref>). </p>
      <p>The size range for medusae diameter in the present study (21-112 cm) was wider than given by previous observations in other locations in the Mediterranean Sea. The previously recorded ranges                 of medusa size were 20- ~100 cm, commonly                                 20-60 cm <xref ref-type="bibr" rid="ridm1842978756">3</xref>, 50-58 cm <xref ref-type="bibr" rid="ridm1842731772">9</xref>, 10-85 cm <xref ref-type="bibr" rid="ridm1842743604">7</xref>, 40-42 cm <xref ref-type="bibr" rid="ridm1842731772">9</xref><xref ref-type="bibr" rid="ridm1842712004">13</xref><xref ref-type="bibr" rid="ridm1842683804">15</xref><xref ref-type="bibr" rid="ridm1842679916">16</xref>. The largest medusae size recorded in the present study (112 cm) was higher than those recorded before which did not exceed 100 cm <xref ref-type="bibr" rid="ridm1842743604">7</xref>. It is worth mentioned that the advance in the starting date of aggregation was associated with bigger medusa size.</p>
    </sec>
  </body>
  <back>
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