<?xml version="1.0" encoding="utf-8" ?>
<article xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:mml="http://www.w3.org/1998/Math/MathML" article-type="review-article" xml:lang="en" crossmark-status="yes">
    <front>
        <journal-meta>
            <journal-id journal-id-type="publisher-id">TOBIOJ</journal-id>
            <journal-id journal-id-type="nlm-ta">Open Biol J</journal-id>
            <journal-title>The Open Biology Journal</journal-title>
            <abbrev-journal-title abbrev-type="pubmed">Open Biol. J.</abbrev-journal-title>
            <issn pub-type="epub">1874-1967</issn>
            <publisher>
                <publisher-name>Bentham Science Publishers</publisher-name>
            </publisher>
        </journal-meta>
        <article-meta>
            <article-id pub-id-type="publisher-id">TOBIOJ-8-1</article-id>
            <article-id pub-id-type="doi">10.2174/1874196702008010001</article-id>
            <title-group>
                <article-title>Direct At-Sea Observations of Elephant Seals (<italic>Mirounga</italic> spp.) to Help Interpret Digital Bio-logging Data</article-title>
            </title-group>
            <contrib-group>
                <contrib contrib-type="author" corresp="yes">
                    <name>
                        <surname>van den Hoff</surname>
                        <given-names>John</given-names>
                    </name>
                    <xref ref-type="aff" rid="aff1">1</xref>
                    <xref ref-type="corresp" rid="cor1">*</xref>
                </contrib>
                <contrib contrib-type="author">
                    <name>
                        <surname>Thalmann</surname>
                        <given-names>Sam</given-names>
                    </name>
                    <xref ref-type="aff" rid="aff2">2</xref>
                </contrib>
                <aff id="aff1">
                    <label>1</label>Australian Antarctic Division, 203 Channel Highway, <addr-line><city>Kingston</city>, <postal-code>7050</postal-code>, <state>Tasmania</state></addr-line>, <country>Australia</country></aff>
                <aff id="aff2">
                    <label>2</label>Department of Primary Industries, Parks, Water and Environment, GPO Box 44, <addr-line><city>Hobart</city>, <postal-code>7001</postal-code>, <state>Tasmania</state></addr-line>, <country>Australia</country></aff>
            </contrib-group>
            <author-notes>
                <corresp id="cor1">
                    <label>*</label>Address correspondence to this author at: Australian Antarctic Division, 203 Channel Highway, Kingston, 7050, Tasmania, Australia; Email: <email xlink:href="john_van@aad.gov.au">john_van@aad.gov.au</email></corresp>
            </author-notes>
            <pub-date pub-type="epub">
                <day>25</day>
                <month>09</month>
                <year>2020</year>
            </pub-date>
            <pub-date pub-type="collection">
                <year>2020</year>
            </pub-date>
            <volume>8</volume>
            <fpage>1</fpage>
            <lpage>5</lpage>
            <history>
                <date date-type="received">
                    <day>13</day>
                    <month>2</month>
                    <year>2020</year>
                </date>
                <date date-type="rev-recd">
                    <day>13</day>
                    <month>7</month>
                    <year>2020</year>
                </date>
                <date date-type="accepted">
                    <day>26</day>
                    <month>7</month>
                    <year>2020</year>
                </date>
            </history>
            <permissions>
                <copyright-statement>&#x00A9; 2020 John &#x0026; Sam</copyright-statement>
                <copyright-year>2020</copyright-year>
                <copyright-holder>John &#x0026; Sam</copyright-holder>
                <license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/legalcode">
                    <p>This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: <uri xlink:href="https://creativecommons.org/licenses/by/4.0/legalcode">https://creativecommons.org/licenses/by/4.0/legalcode</uri>.  This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</p>
                </license>
            </permissions>
            <abstract>
                <sec>
                    <title>Background:</title>
                    <p>A key short-fall with animal-borne bio-logging instruments, which collect digital time-series data regarding the foraging behaviours of cryptic marine mammal species, is validating those data against <italic>in situ</italic> behaviours.</p>
                </sec>
                <sec>
                    <title>Objective:</title>
                    <p>To collate direct observations of elephant seal feeding behaviour to help interpret foraging behaviours inferred from Time-Depth Recorder (TDR) data.</p>
                </sec>
                <sec>
                    <title>Methods:</title>
                    <p>Direct observations of elephant seal foraging behaviour were collated from the published literature using a search of the world-wide-web. Those observations were supplemented with an unpublished record.</p>
                </sec>
                <sec>
                    <title>Results:</title>
                    <p>Two deep-sea video recordings and six surface sightings of elephant seals ingesting prey were collated. Each observation either supported or suggested an alternative to behaviours derived from digital time-depth profiles. The tendency for elephant seals to surface following the capture of large prey suggests precipitous drops in stomach temperature at the sea-surface, which have been recorded and interpreted as drinking events, more likely represent the ingestion of large prey items.</p>
                </sec>
                <sec>
                    <title>Conclusion:</title>
                    <p>Direct observations of marine mammal foraging behaviours are rare, yet they provide a means to continuously evaluate and interpret outcomes of bio-logging instruments.</p>
                </sec>
            </abstract>
            <kwd-group kwd-group-type="author">
                <title>Keywords</title>
                <kwd>Bio-logging</kwd>
                <kwd>Foraging behaviour</kwd>
                <kwd>Marine mammal</kwd>
                <kwd>Stomach temperature</kwd>
                <kwd>Time-depth recorder</kwd>
                <kwd>Elephant seals (Mirounga spp.)</kwd>
            </kwd-group>
        </article-meta>
    </front>
    <body>
        <sec id="sec1" sec-type="intro">
            <label>1</label>
            <title>INTRODUCTION</title>
            <p>One way to gather information about highly mobile and migratory species, such as marine mammals, is through the use of bio-logging instruments which, depending on the array of sensors deployed, record aspects of an individuals&#x2019; movements and behaviours at set time intervals  [<xref ref-type="bibr" rid="r1">1</xref>]. However, historical bio-logging studies often lack complementary deployments (<italic>e.g.</italic> video recorder + TDR), which combine to provide a more comprehensive picture for foraging behaviours that are beyond the boundary of our visibility or experiences  [<xref ref-type="bibr" rid="r2">2</xref>, <xref ref-type="bibr" rid="r3">3</xref>]. Nevertheless, knowledge of animal migration patterns and foraging behaviours inform us of when, where and how the Earths&#x2019; biota interacts with its environment and also with human resource requirements.</p>
            <p>Elephant seals (<italic>Mirounga</italic> spp.) are large-bodied migratory marine mammals. All age classes have been tracked by satellite telemetry to remote oceanic or continental settings where attached bio-logging instruments have recorded several different functional dive types, including foraging dives where the seals are purported to prey on the suite of benthic and pelagic species during what have been termed &#x201C;wiggles&#x201D; in the dive profiles (Fig. <bold><xref ref-type="figure" rid="F1">1</xref></bold>) [<xref ref-type="bibr" rid="r4">4</xref>-<xref ref-type="bibr" rid="r7">7</xref>]. Compared with females, male elephant seals are up to 10 times larger and differ in their foraging ecology by preferentially hunting for benthic prey over continental shelves whereas females forage in more open pelagic waters [<xref ref-type="bibr" rid="r4">4</xref>]. The cumulative effects of their lengthy temporal migrations to geographically remote locations combined with the near-continuous diving behaviour for both sexes and all age classes  [<xref ref-type="bibr" rid="r8">8</xref>] makes direct observations of elephant seals a novelty.</p>
            <p>Here, we collated direct observations of foraging behaviour for <italic>Mirounga</italic> spp. We supplement those records with an unpublished image of a male <italic>M. leonina</italic> ingesting prey at the sea-surface. Our objective is to discuss those results with respect to dive behaviours that have been inferred from two-dimensional data collected using digital TDRs and stomach temperature sensors.</p>
            <fig id="F1" position="float" fig-type="figure" column="double">
                <label>Fig. (1)</label>
                <caption>Schematic representations of: <bold>A.</bold> Typical two-dimensional (time-depth) dive profiles recorded by free-ranging elephant seals (<italic>Mirounga</italic> spp.) during periods of travel (transit), rest/digestion (drift) and feeding. Benthic (bottom) dive profiles are constrained by depth and therefore have flat-bottom phases compared with mid-water (pelagic) dive profiles. Feeding dives contain a number of brief excursions between depths. <bold>B.</bold> Within dive behaviours of southern elephant seals (<italic>M. leonina</italic>) during type E<sub>b</sub> benthic foraging dives known as &#x201C;wiggles&#x201D; (Source: Sala <italic>et al</italic>. 2011). Note the orientation of the seal during the bottom phase of the dive profile is consistent with that observed directly (van den Hoff <italic>et al.</italic> (2017). <bold>C.</bold> Changes in stomach temperature with swim speed and depth during Type D dives. The precipitous drop in stomach temperature recorded at the sea-surface has been suggested as indicative of surface seawater drinking (Source: Horsburgh <italic>et al</italic>. (2007).</caption>
                <graphic xlink:href="TOBIOJ-8-1_F1.jpg">
                </graphic>
            </fig>
        </sec>
        <sec id="sec2" sec-type="methods">
            <label>2</label>
            <title>METHODS</title>
            <p>Reports of direct observations of elephant seal feeding were collated through an internet search using &#x201C;video footage elephant seal feeding&#x201D; and &#x201C;surface feeding elephant seal&#x201D; as the search terms. Two direct video recordings of elephant seals feeding at extreme depths were found. Two published accounts of elephant seals feeding at the sea-surface were found and those supplemented with a third unpublished observation.</p>
        </sec>
        <sec id="sec3" sec-type="results|discussion">
            <label>3</label>
            <title>RESULTS AND DISCUSSION</title>
            <sec id="sec3.1">
                <label>3.1</label>
                <title>Deep Water Observations</title>
                <p>Two studies have serendipitously captured brief observations of feeding in elephant seals. The first was <italic>via</italic> a video camera anchored to the seafloor at a depth of 894 m in the Barkley Canyon, west of Vancouver Island, Canada. Footage was captured of a free-ranging northern elephant seal (<italic>M. angustirostris</italic>), of unknown sex, predating a soft-bodied hag-fish (<italic>Eptetratus</italic> sp., 25/June/2012, <ext-link ext-link-type="uri" xlink:href="https://bmscblog.wordpress.com/2013/04/03/citizen-scientist-spots-a-hungry-elephant-seal-in-barkley-canyon/">https://bmscblog. wordpress.com/2013/04/03/citizen-scientist-spots-a-hungry-elephant-seal-in-barkley-canyon/</ext-link> (accessed 14/05/2020). No pre/post-ingestion behaviour was witnessed but the seal captured <italic>Eptetratus</italic> sp. by suction feeding and swallowed it immediately at depth.</p>
                <p>The second study captured video footage of <italic>M. leonina</italic> attacking Patagonian toothfish (<italic>Dissostichus eleginoides</italic>) hooked on commercial longlines near Heard Island  [<xref ref-type="bibr" rid="r9">9</xref>] (<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1371/journal.pone.0172396.s004">https://doi.org/10.1371/journal.pone.0172396.s004</ext-link>,and.s005). Although the behaviours recorded were in a somewhat artificial setting (<italic>i.e.</italic> a lit environment with tethered prey), the footage provides insights into the behaviour of the seals as they encountered benthic prey at depths in excess of 1000 m. Seals swam close to the sea-floor and undertook brief (meters) excursions from the seafloor as they circled hook-caught fish of ~ 1 m in length. Prey capture behaviour included a &#x201C;head-down&#x201D; orientation and a turn toward the surface following seizure of the prey item.</p>
            </sec>
            <sec id="sec3.2">
                <label>3.2</label>
                <title>Surface Observations</title>
                <p>Three adult male <italic>M. angustirostris</italic> have been observed consuming large-bodied elasmobranchs such as stingrays (<italic>Urolophus halleri</italic>), blue sharks (<italic>Prionace glauca</italic>) and spiny dogfish (<italic>Squalus acanthis</italic>) head-first at the seas-surface  [<xref ref-type="bibr" rid="r10">10</xref>]. There was one report of a male <italic>M. leonina</italic> feeding at the sea-surface on what was believed to be a large fish, perhaps a <italic>D. eleginoides</italic>, that was presumed captured in about 1000 m of water to the northwest of South Georgia (53&#x00BA;39&apos; S, 38&#x00BA;24&apos; W)  [<xref ref-type="bibr" rid="r11">11</xref>].</p>
                <p>Here, we supplement the record for <italic>M. leonina</italic> with a further sighting of a sub-adult male (aged 6 - 8 y) swallowing head-first a draughtboard shark (<italic>Cephaloscyllium laticeps</italic>) in the near-shore surface waters (&#x2264; 70 m) of south-east Tasmania (43&#x00BA;11&apos; S, 147&#x00BA;58&apos; E; Fig. <bold><xref ref-type="figure" rid="F2">2</xref></bold>). Combined, those five surface observations suggest large hard-bodied prey items captured at depth are bought to the sea-surface for manipulation prior to ingestion.</p>
                <fig id="F2" position="float" fig-type="figure">
                    <label>Fig. (2)</label>
                    <caption>Still image of a male southern elephant seal (<italic>Mirounga leonina</italic>) swallowing a draughtboard shark (<italic>Cephaloscyllium laticeps</italic>) head-first at the sea surface off Munroe Bight, Tasman Peninsula, Tasmania (43&#x00BA; 11&apos;23&#x201D; S, 147&#x00BA; 58&apos;24&#x201D; E) on the 30<sup>th</sup> March 2008. The water depth was ~ 70 m. Photo courtesy of the Department of Primary Industries, Parks, Water and Environment (Tasmania).</caption>
                    <graphic xlink:href="TOBIOJ-8-1_F2.jpg">
                    </graphic>
                </fig>
            </sec>
            <sec id="sec3.3">
                <label>3.3</label>
                <title>Informing TDR Derived Behaviours</title>
                <p>What is currently (2020) known of adult male <italic>Mirounga</italic> foraging behaviours is outweighed by what is known for adult females and juveniles, and for that reason, some male behaviours have been assumed from other age/sex classes. But, behaviours inferred from single-sensor TDR deployments do not always equate with those derived from complementary multi-sensor studies, nor might they be applied across species or even between age classes within species  [<xref ref-type="bibr" rid="r12">12</xref>-<xref ref-type="bibr" rid="r15">15</xref>]. This makes the observations described here valuable for understanding specific foraging behaviours of adult male <italic>Mirounga</italic> spp.</p>
                <p>The behaviours of male <italic>M. leonina</italic> captured directly by video camera [<xref ref-type="bibr" rid="r9">9</xref>] conformed well to behaviours inferred from TDR records. For example, there were small excursions from the seafloor that are characteristic of &#x201C;wiggle&#x201D; type anomalies commonly seen in elephant seal feeding dive profiles (Fig. <bold><xref ref-type="figure" rid="F1">1A</xref></bold>). The head-down orientation observed by video just prior to prey capture has also been digitally recorded and termed &#x201C;up-ending&#x201D; in the benthos (Fig. <bold><xref ref-type="figure" rid="F1">1B</xref></bold>), [16]. It was also clear from the video that not all wiggles and head-down orientations were prey capture attempts, some were searching activities. More- over, up-ending events seem to equate more closely to prey capture attempts than wiggles in feeding dives, confirming the usefulness of complementary sensor deployments.</p>
                <p>Observations of <italic>Mirounga</italic> spp. feeding on large prey items at the sea-surface offer an alternative explanation for the precipitous drops in stomach temperature that have been termed &#x201C;drinking events&#x201D; (Fig. <bold><xref ref-type="figure" rid="F1">1C</xref></bold>)<bold>,</bold> [17]. Practically speaking, stomach temperature telemetry uses measured changes in a predators&#x2019; core body temperature to imply consumption of ectothermic prey and/or the ingestion of water  [<xref ref-type="bibr" rid="r18">18</xref>]. Changes in stomach temperature for one free-ranging female <italic>M. angustirostris</italic>, whose dive behaviour appeared to be unconstrained by bathymetry, occurred during the bottom phases of putative type D pelagic foraging dives (Fig. <bold><xref ref-type="figure" rid="F1">1C</xref></bold>)  [<xref ref-type="bibr" rid="r19">19</xref>]. Feeding was inferred from anomalies in stomach temperature that were associated with increased swim velocity and wiggles (Fig. <bold><xref ref-type="figure" rid="F1">1C</xref></bold>), and importantly an upward movement through the water column to shallower depths [<xref ref-type="bibr" rid="r17">17</xref>]. Unlike other studies [<xref ref-type="bibr" rid="r18">18</xref>, <xref ref-type="bibr" rid="r19">19</xref>], Horsburgh and others [<xref ref-type="bibr" rid="r17">17</xref>] recorded decreases in stomach temperature at the sea-surface which they assigned to drinking events (Fig. <bold><xref ref-type="figure" rid="F1">1C</xref></bold>). However, deliberate drinking of seawater in pinnipeds seems equivocal. Harbor seals (<italic>Phoca vitulina</italic>), for example, did not drink seawater voluntarily  [<xref ref-type="bibr" rid="r20">20</xref>] but a captive leopard seal (<italic>Hydrurga leptonyx</italic>) drank large quantities of seawater when placed in the ocean  [<xref ref-type="bibr" rid="r21">21</xref>].</p>
                <p>All <italic>Mirounga</italic> spp. observed feeding at the surface were manipulating large, hard-bodied, deep-dwelling benthic prey species ([<xref ref-type="bibr" rid="r10">10</xref>, <xref ref-type="bibr" rid="r11">11</xref>,] this study) which can reach at least 1.5 m in length  [<xref ref-type="bibr" rid="r22">22</xref>]. Since the ingestion of large prey causes a rapid decrease in stomach temperature [<xref ref-type="bibr" rid="r18">18</xref>], we consider the stomach temperature changes that recorded at the sea-surface by Horsburgh <italic>et al</italic>. [<xref ref-type="bibr" rid="r17">17</xref>] as evidence for the ingestion of large prey. If it is a requirement for <italic>Mirounga</italic> ssp. to surface to manipulate large prey items prior to ingestion, it follows that anomalously long intervals between dives in the TDR records (known as extended surface intervals [<xref ref-type="bibr" rid="r8">8</xref>]) could indicate successful capture of large prey items.</p>
            </sec>
        </sec>
        <sec sec-type="conclusions">
            <title>CONCLUSION</title>
            <p>Direct observations of feeding by free-ranging, near-continuous deep-diving marine mammals are extremely rare. However, they provide a valuable means for identifying behaviours that will aid in interpreting underwater behaviours digitally recorded with the use of bio-logging instruments  [<xref ref-type="bibr" rid="r23">23</xref>]. Without verification, the risk of subjectivity and preconceived notions of inferred behaviour will continue, but assigning behavioural activities to digital data remains a challenge  [<xref ref-type="bibr" rid="r24">24</xref>]. For that reason, continually re-evaluating TDR data free from predilection and by all means available will refine species prey consumption model estimates. Moreover, humans can more completely appreciate the degree to which marine predators overlap with their own requirements for marine resources.</p>
        </sec>
    </body>
    <back>
        <sec sec-type="competing-interests">
            <title>AUTHORS&#x2019; CONTRIBUTIONS</title>
            <p>JvdH conceived the paper, collated the data and wrote the manuscript.</p>
            <p>ST shared the image of a male southern elephant seal feeding in southern Tasmania and contributed to manuscript preparation.</p>
            <p>Both authors read and approved the final manuscript.</p>
        </sec>
        <sec sec-type="competing-interests">
            <title>CONSENT FOR PUBLICATION</title>
            <p>Not applicable</p>
        </sec>
        <sec sec-type="competing-interests">
            <title>FUNDING</title>
            <p>Not applicable</p>
        </sec>
        <sec sec-type="competing-interests">
            <title>CONFLICT OF INTEREST</title>
            <p>The authors declare no conflicts of interest, financial or otherwise.</p>
        </sec>
        <ack>
            <title>ACKNOWLEDGEMENTS</title>
            <p>We thank the reviewers for their constructive comments. The Australian Antarctic divisions&#x2019; Dan Broun drew Figs. (<bold><xref ref-type="fig" rid="F1">1A</xref></bold> and <bold><xref ref-type="fig" rid="F1">1C</xref></bold>).</p>
        </ack>
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