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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Mamm. Sci.</journal-id>
<journal-title-group>
<journal-title>Frontiers in Mammal Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Mamm. Sci.</abbrev-journal-title>
</journal-title-group>
<issn pub-type="epub">2813-4699</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fmamm.2025.1634280</article-id>
<article-version article-version-type="Version of Record" vocab="NISO-RP-8-2008"/>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Case Report</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Case Report: Ophthalmic and associated systemic disorders in free-ranging giant otters (<italic>Pteronura brasiliensis</italic>) documented through video frames and photographs</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name><surname>Soresini</surname><given-names>Grazielle</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<xref ref-type="corresp" rid="c001"><sup>*</sup></xref>
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<contrib contrib-type="author">
<name><surname>Foerster</surname><given-names>Nathalie</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
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<contrib contrib-type="author">
<name><surname>Somma</surname><given-names>Andr&#xe9; T.</given-names></name>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref>
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<contrib contrib-type="author">
<name><surname>da Silva</surname><given-names>Fabiano A.</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
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<contrib contrib-type="author">
<name><surname>Ribas</surname><given-names>Carolina</given-names></name>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
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<contrib contrib-type="author">
<name><surname>Leuchtenberger</surname><given-names>Caroline</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup></xref>
<xref ref-type="aff" rid="aff6"><sup>6</sup></xref>
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<contrib contrib-type="author">
<name><surname>Mour&#xe3;o</surname><given-names>Guilherme</given-names></name>
<xref ref-type="aff" rid="aff7"><sup>7</sup></xref>
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<aff id="aff1"><label>1</label><institution>Universidade Federal de Mato Grosso do Sul, Programa de P&#xf3;s-Gradua&#xe7;&#xe3;o em Ecologia e Conserva&#xe7;&#xe3;o, Centro de Ci&#xea;ncias Biol&#xf3;gicas e da Sa&#xfa;de - Cidade Universit&#xe1;ria</institution>, <city>Campo Grande</city>, <state>Mato Grosso do Sul</state>,&#xa0;<country country="br">Brazil</country></aff>
<aff id="aff2"><label>2</label><institution>IUCN Species Survival Commission, Otter Specialist Group</institution>, <city>Gland</city>,&#xa0;<country country="ch">Switzerland</country></aff>
<aff id="aff3"><label>3</label><institution>Pontif&#xed;cia Universidade Cat&#xf3;lica Do Paran&#xe1; &#x2013; PUCPR, School of Medicine and Life Sciences. R. Imac. Concei&#xe7;&#xe3;o</institution>, <city>Curitiba</city>,&#xa0;<country country="br">Brazil</country></aff>
<aff id="aff4"><label>4</label><institution>Instituto Pr&#xf3;-Carn&#xed;voros</institution>, <city>Atibaia</city>,&#xa0;<country country="br">Brazil</country></aff>
<aff id="aff5"><label>5</label><institution>Instituto Federal Farroupilha &#x2013; IFFAR, Coordena&#xe7;&#xe3;o de Ci&#xea;ncias Biol&#xf3;gicas</institution>, <city>Panambi</city>,&#xa0;<country country="br">Brazil</country></aff>
<aff id="aff6"><label>6</label><institution>Projeto Ariranhas</institution>, <city>Arroio do Meio</city>,&#xa0;<country country="br">Brazil</country></aff>
<aff id="aff7"><label>7</label><institution>Embrapa Pantanal, Laborat&#xf3;rio de Vida Selvagem</institution>, <city>Corumb&#xe1;</city>, <state>Mato Grosso do Sul</state>,&#xa0;<country country="br">Brazil</country></aff>
<author-notes>
<corresp id="c001"><label>*</label>Correspondence: Grazielle Soresini, <email xlink:href="mailto:grasoresini@gmail.com">grasoresini@gmail.com</email></corresp>
</author-notes>
<pub-date publication-format="electronic" date-type="pub" iso-8601-date="2025-11-26">
<day>26</day>
<month>11</month>
<year>2025</year>
</pub-date>
<pub-date publication-format="electronic" date-type="collection">
<year>2025</year>
</pub-date>
<volume>4</volume>
<elocation-id>1634280</elocation-id>
<history>
<date date-type="received">
<day>24</day>
<month>05</month>
<year>2025</year>
</date>
<date date-type="accepted">
<day>31</day>
<month>10</month>
<year>2025</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2025 Soresini, Foerster, Somma, da Silva, Ribas, Leuchtenberger and Mour&#xe3;o.</copyright-statement>
<copyright-year>2025</copyright-year>
<copyright-holder>Soresini, Foerster, Somma, da Silva, Ribas, Leuchtenberger and Mour&#xe3;o</copyright-holder>
<license>
<ali:license_ref start_date="2025-11-26">https://creativecommons.org/licenses/by/4.0/</ali:license_ref>
<license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License (CC BY)</ext-link>. 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.</license-p>
</license>
</permissions>
<abstract>
<p>The present study aims to report the occurrence of ophthalmic and associated systemic disorders in giant otters (<italic>Pteronura brasiliensis</italic>) from the Brazilian Pantanal. This mustelid species is classified globally as Endangered and faces increasing threats from various human activities and diseases from domestic animals across most of its range, including Brazil. Over a 10-year period, we recorded 12 wild giant otters showing signs of ophthalmic diseases, as well as other systemic abnormalities. In this study, we describe the ocular conditions based on an analysis of digital-video frames and photographs, discuss potential causes, and highlight the concern that the long-term survival of the giant otter population in a specific area of the southern Brazilian Pantanal may be at risk.</p>
</abstract>
<kwd-group>
<kwd>conservation threats</kwd>
<kwd>eye</kwd>
<kwd>lutrinae</kwd>
<kwd>mammal</kwd>
<kwd>ophthalmology</kwd>
<kwd>wildlife health status</kwd>
</kwd-group>
<funding-group>
<funding-statement>The author(s) declare financial support was received for the research and/or publication of this article. This study was partially financed by the Coordenac&#x327;&#xe3;o de Aperfeic&#x327;oamento de Pessoal de N&#x131;&#x301;vel Superior - Brasil (CAPES) - Finance Code 001, Doctoral Scholarship 1461215, and by the National Council for Scientific and Technological Development (CNPq), through project n. 485890/2013&#x2013;5 and the CNPq/Fundect Pronex project n. 006/2015.</funding-statement>
</funding-group>
<counts>
<fig-count count="2"/>
<table-count count="2"/>
<equation-count count="0"/>
<ref-count count="51"/>
<page-count count="9"/>
<word-count count="4083"/>
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<custom-meta-group>
<custom-meta>
<meta-name>section-at-acceptance</meta-name>
<meta-value>Life History and Conservation</meta-value>
</custom-meta>
</custom-meta-group>
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</front>
<body>
<sec id="s1" sec-type="intro">
<title>Introduction</title>
<p>Giant otters (<italic>Pteronura brasiliensis</italic>, Zimmermann 1780) are semiaquatic mammals and the largest among the fourteen mustelid species in the subfamily Lutrinae. They primarily feed on fish and inhabit freshwater ecosystems near tropical forests and floodplains (<xref ref-type="bibr" rid="B10">Duplaix, 1980</xref>). Endemic to South America, the species originally had a wide range of distribution of occurrence. However, intensive hunting for the fur trade between the 1940s and 1970s led to a range reduction of nearly 40% by the 1980s (<xref ref-type="bibr" rid="B7">Colodetti, 2014</xref>). Currently, populations persist in several countries, including Brazil, where it inhabits the Amazon, Cerrado, and Pantanal ecoregions (<xref ref-type="bibr" rid="B35">Rodrigues et&#xa0;al., 2018</xref>). Nevertheless, there is still no reliable estimate of the total population size, as available estimates are restricted to specific regions, and overall population trends remain uncertain (<xref ref-type="bibr" rid="B46">Wallace et&#xa0;al., 2025</xref>).</p>
<p>Many large carnivores, including giant otters, face significant threats leading to population declines, reductions in their geographic ranges, and habitat fragmentation (<xref ref-type="bibr" rid="B34">Ripple et&#xa0;al., 2014</xref>). In Brazil and across most of their range, the main threats to this top predator of aquatic ecosystems include water pollution, competition with human fisheries, diseases transmitted by domestic animals, and habitat degradation (<xref ref-type="bibr" rid="B26">Leuchtenberger et&#xa0;al., 2018</xref>). Climate change alters rainfall patterns and river flow, reducing fish availability and degrading denning sites (<xref ref-type="bibr" rid="B18">Groenendijk et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B46">Wallace et&#xa0;al., 2025</xref>). As a result of these threats, the species is classified as Endangered by the IUCN since 2000 (<xref ref-type="bibr" rid="B18">Groenendijk et&#xa0;al., 2021</xref>) and as Vulnerable on Brazil&#x2019;s national Red List (<xref ref-type="bibr" rid="B35">Rodrigues et&#xa0;al., 2018</xref>).</p>
<p>Information on ophthalmic abnormalities in mustelids, including otters, is mostly limited to isolated cases (<xref ref-type="bibr" rid="B49">Williams, 1989</xref>; <xref ref-type="bibr" rid="B50">Williams et&#xa0;al., 2000</xref>; <xref ref-type="bibr" rid="B51">2004</xref>; <xref ref-type="bibr" rid="B9">Dubey and Thomas, 2011</xref>). Some conditions linked to ocular diseases in wild animals include trauma (e.g. <xref ref-type="bibr" rid="B24">Kumar et&#xa0;al., 2015</xref>), nutritional factors (e.g. <xref ref-type="bibr" rid="B51">Williams et&#xa0;al., 2004</xref>; <xref ref-type="bibr" rid="B25">Lange et&#xa0;al., 2017</xref>), aging (e.g. <xref ref-type="bibr" rid="B37">Roth et&#xa0;al., 2004</xref>; <xref ref-type="bibr" rid="B24">Kumar et&#xa0;al., 2015</xref>), poor environmental or water quality (e.g. contamination through dieldrin pesticide as reported by <xref ref-type="bibr" rid="B51">Williams et&#xa0;al., 2004</xref>), parasites and infectious agents (<xref ref-type="bibr" rid="B31">Pinto et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B9">Dubey and Thomas, 2011</xref>).</p>
<p>Research on ophthalmic disorders (as well as epidemiological studies) in free-ranging giant otters remains limited, largely due to the challenges involved in capturing this species. The only published method employs a funnel-shaped net trap installed at den entrances (<xref ref-type="bibr" rid="B41">Silveira et&#xa0;al., 2011</xref>). While effective, this technique does not allow researchers to choose which individual from the group will be captured and they need to avoid groups with pregnant or lactating females. Additionally, its success also relies on specific environmental conditions, such as the dry season (when dens are more accessible), and certain den characteristics, like having few entrances, no submerged entry points, and entrances that are neither too close to the water nor too wide for effective trapping.</p>
<p>Conducting a detailed ophthalmic examination typically requires specialized optical devices or techniques to properly describe eye lesions. However, certain anatomical features of the eye, such as changes in the color of ocular tissues (e.g. opacity), can be easily detected through standard photography. Ophthalmic imaging has long been a crucial tool for documenting ophthalmic diseases (<xref ref-type="bibr" rid="B1">Bennett and Barry, 2009</xref>). External eye photography is a relevant approach for examining the ocular surface, eyes adnexa, and surrounding facial structures. It is often used in veterinary ophthalmology studies (<xref ref-type="bibr" rid="B1">Bennett and Barry, 2009</xref>; <xref ref-type="bibr" rid="B5">Colitz et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B42">Simeone et&#xa0;al., 2017</xref>) and is particularly useful when physical restraint of the animal is not achievable.</p>
<p>This study aims to document evidence of ophthalmic and associated systemic disorders in free-ranging giant otters using images and discuss potential causes.</p>
</sec>
<sec id="s2">
<title>Methods</title>
<sec id="s2_1">
<title>Study area</title>
<p>The Pantanal, one of the earth&#x2019;s largest wetlands, harbors a significant population of giant otters and spans parts of Brazil, Bolivia, and Paraguay (<xref ref-type="bibr" rid="B19">Harris et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B45">Tomas et&#xa0;al., 2020</xref>). All data were collected in the Brazilian Pantanal, covering both the southern region (including the Miranda and Negro rivers, and pools along the Estrada Parque Pantanal road) and the northern region (Cuiab&#xe1; and Mutum rivers). Rivers are the primary and most suitable habitat for giant otters, whereas the lentic water bodies formed along the Estrada Parque Pantanal are considered less favorable for the species (<xref ref-type="bibr" rid="B38">Schweizer, 1992</xref>; <xref ref-type="bibr" rid="B32">Ribas et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B44">Tomas et&#xa0;al., 2015</xref>).</p>
</sec>
<sec id="s2_2">
<title>Data collection</title>
<p>From December 2009 to October 2019, field surveys on giant otter ecology, behavior, health, and genetics were conducted using a motorized boat on the rivers and a 4x4 vehicle along the Estrada Parque Pantanal road. Data were collected using a high-definition digital video camera (Sony<sup>&#xae;</sup> HDR-CX220, Sony Brasil Ltda, S&#xe3;o Paulo-SP) with a recording resolution of 1920&#xd7;1080 pixels (Full HD). All videos were carefully analyzed, and frames showing otters with apparent ophthalmic affections were selected for analysis by two wildlife veterinarians (GS and AS). Occasionally, photographs were also taken using a Canon<sup>&#xae;</sup> Rebel T6i camera equipped with 70&#x2013;200 mm L-series lenses, with a resolution of 24.2 megapixels.</p>
<p>Giant otters were individually identified by their distinctive white throat and chest patterns (<xref ref-type="bibr" rid="B10">Duplaix, 1980</xref>; <xref ref-type="bibr" rid="B3">Carter and Rosas, 1997</xref>). We recorded each otter&#x2019;s estimated age, sex, social hierarchy, group composition, and location. Otters were classified by age as subadults (1.5-2.5 years) or adults (&gt;2.5 years), based on long-term monitoring (<xref ref-type="bibr" rid="B17">Groenendijk et&#xa0;al., 2015</xref>). Sex was determined by genitalia observation, while social hierarchy and reproductive status were assessed through behavioral patterns, particularly scent-marking (<xref ref-type="bibr" rid="B10">Duplaix, 1980</xref>; <xref ref-type="bibr" rid="B27">Leuchtenberger and Mour&#xe3;o, 2009</xref>). Locations were recorded using GPS.</p>
</sec>
<sec id="s2_3">
<title>Criteria proposed to assess systemic condition</title>
<p>The giant otters included in this study were not captured. Instead, we used visual inspection to classify each individual according to four criteria (<xref ref-type="table" rid="T1"><bold>Table&#xa0;1</bold></xref>):</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Categorical scores used to assess systemic condition of free-ranging giant otters (<italic>Pteronura brasiliensis</italic>).</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" align="left">Criteria</th>
<th valign="middle" align="left">Categories/scores</th>
<th valign="middle" align="left">Description</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="middle" align="left">Body Condition Score (BCS)</td>
<td valign="middle" align="left">1-5</td>
<td valign="middle" align="left">1 = emaciated, 2 = thin, 3 = optimal, 4 = heavy, 5 = obese (see <xref ref-type="fig" rid="f1"><bold>Figure&#xa0;1</bold></xref>)</td>
</tr>
<tr>
<td valign="middle" align="left">Physical Debilitation (PD)</td>
<td valign="middle" align="left">0-2</td>
<td valign="middle" align="left">0 = normal, 1 = mild, 2 = severe<break/>based on activity level and responsiveness</td>
</tr>
<tr>
<td valign="middle" align="left">Trauma (Tr)</td>
<td valign="middle" align="left">absent or present</td>
<td valign="middle" align="left">fresh wounds, bleeding</td>
</tr>
<tr>
<td valign="middle" align="left">Overall Health Status (OHS)</td>
<td valign="middle" align="left">clinically healthy or clinically unhealthy</td>
<td valign="middle" align="left">integration of all criteria</td>
</tr>
</tbody>
</table>
</table-wrap>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Body Condition Scores (BCS) of wild giant otters (<italic>Pteronura brasiliensis</italic>), ranging from 1 (emaciated) to 5 (obese): <bold>(A)</bold> BCS 1 (emaciated), Miranda River, May 2015; <bold>(B)</bold> BCS 2 (thin), Paraguay River, November 2018; <bold>(C)</bold> BCS 3 (optimal), Vermelho River, November 2022; <bold>(D)</bold> BCS 4 (heavy), Miranda River, August 2015; <bold>(E)</bold> BCS 5 (obese), Miranda River, August 2019.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmamm-04-1634280-g001.tif">
<alt-text content-type="machine-generated">Five images showing giant otters in different natural settings. (A) An otter with a cream-colored throat surrounded by foliage. (B) An otter on rocky terrain with grass. (C) An otter walking along a sandy riverbank. (D) An otter standing alert with a patterned throat. (E) An otter on muddy ground near water.</alt-text>
</graphic></fig>
<list list-type="roman-upper">
<list-item>
<p>Body Condition Score: the BCS of each individual was visually assessed from all available images, applying a scale from 1 to 5 that is commonly used in different species of domestic (e.g. <xref ref-type="bibr" rid="B13">Ferguson et&#xa0;al., 2006</xref>) and wild animals (e.g. <xref ref-type="bibr" rid="B4">Clingerman and Summers, 2005</xref>; <xref ref-type="bibr" rid="B20">Harshaw et&#xa0;al., 2016</xref>), given the absence of a species-specific method for otters. On this scale: a score of 1 indicates a severely emaciated animal with very prominent bones (hips, ribs, and spinous processes); a score of 2 denotes a thin otter with minimal fat reserves and visible hip bones and spinous processes; a score of 3 is considered optimal, with no visible bony prominences; a score of 4 indicates a heavy otter, with fat deposits beginning to accumulate in the axillary, inguinal, or abdominal regions; and a score of 5 reflects an obese animal, with clearly visible fat deposits in the axillary, inguinal, and abdominal regions (<xref ref-type="fig" rid="f1"><bold>Figure&#xa0;1</bold></xref>).</p></list-item>
<list-item>
<p>Physical Debilitation: giant otters were classified as &#x201c;physically debilitated&#x201d; based on clinical assessment through visual indicators, including lethargic behavior and minimal responsiveness to human presence. Categorized as normal, mildly debilitated (mild lethargy or reduced activity), or severely debilitated (marked lethargy or minimal responsiveness).</p></list-item>
<list-item>
<p>Trauma: presence of visible signs of recent injury (e.g. fresh wounds, bleeding), recorded as absent or present.</p></list-item>
<list-item>
<p>Overall Health Status: integrated assessment combining the previous criteria, categorized as &#x201c;clinically healthy&#x201d; or &#x201c;clinically unhealthy&#x201d; based on the combination of body condition, behavior, and evidence of trauma. An individual was considered clinically unhealthy if any single parameter scored low, and clinically healthy only when all three were normal, ensuring a conservative health assessment. Previous traumatic injuries (e.g. cranial flattening) were not considered in the classification of individuals as clinically unhealthy.</p></list-item>
</list>
</sec>
</sec>
<sec id="s3" sec-type="results">
<title>Results</title>
<p>Between December 2009 and October 2019, we recorded a total of 12 adult giant otters with presumed ophthalmic disorders (affecting the eyes, eyelids, and surrounding skin) in the Pantanal wetland, Brazil. Sex was determined for nine individuals (75%), of which five were female and four were male. Most cases (83.3%, n=10) were observed in the southern region of the Pantanal. Of the 12 otters, seven animals presented bilateral ocular disorders, two had disorders affecting only the left eye (OS, oculus sinister), and three had disorders in the right eye (OD, oculus dexter). Detailed information available on each individual, as well as their ophthalmic and systemic conditions, is provided in <xref ref-type="table" rid="T2"><bold>Table&#xa0;2</bold></xref>. The images of the eyes exhibiting alterations are presented in <xref ref-type="fig" rid="f2"><bold>Figure 2</bold></xref>.</p>
<table-wrap id="T2" position="float">
<label>Table&#xa0;2</label>
<caption>
<p>Chronological records of 12 adult free-ranging giant otters (<italic>Pteronura brasiliensis</italic>) with ophthalmic disorders in the Brazilian Pantanal, from December 2009 to October 2019, including associated systemic condition and ophthalmic findings.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" align="center">Id</th>
<th valign="middle" align="center">Sex<sup>1</sup></th>
<th valign="middle" align="center">Social status<sup>2</sup></th>
<th valign="middle" align="center">Location<sup>3</sup></th>
<th valign="middle" align="center">Study period</th>
<th valign="middle" align="center">Body condition score (BCS)</th>
<th valign="middle" align="center">Physical debilitation (PD)</th>
<th valign="middle" align="center">Trauma (Tr)</th>
<th valign="middle" align="center">Overall health status (OHS)</th>
<th valign="middle" align="center">Ophthalmic findings<sup>4</sup> OD</th>
<th valign="middle" align="center">Ophthalmic findings<sup>4</sup> OS</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="middle" align="center">B</td>
<td valign="middle" align="center">F</td>
<td valign="middle" align="center">dom</td>
<td valign="middle" align="center">EPP</td>
<td valign="middle" align="center">Dec 2009</td>
<td valign="middle" align="center">BCS 2</td>
<td valign="middle" align="center">1</td>
<td valign="middle" align="center">absent</td>
<td valign="middle" align="center">unhealthy</td>
<td valign="middle" align="center">chronic blepharitis</td>
<td valign="middle" align="center">chronic blepharitis</td>
</tr>
<tr>
<td valign="middle" align="center">C</td>
<td valign="middle" align="center">M</td>
<td valign="middle" align="center">dom</td>
<td valign="middle" align="center">EPP</td>
<td valign="middle" align="center">Dec 2009</td>
<td valign="middle" align="center">BCS 2</td>
<td valign="middle" align="center">1</td>
<td valign="middle" align="center">absent</td>
<td valign="middle" align="center">unhealthy</td>
<td valign="middle" align="center">chronic blepharitis</td>
<td valign="middle" align="center">chronic blepharitis</td>
</tr>
<tr>
<td valign="middle" align="center">D</td>
<td valign="middle" align="center">M</td>
<td valign="middle" align="center">dom</td>
<td valign="middle" align="center">MiR</td>
<td valign="middle" align="center">Apr/May 2015</td>
<td valign="middle" align="center">BCS 1</td>
<td valign="middle" align="center">2</td>
<td valign="middle" align="center">cutaneous lesions</td>
<td valign="middle" align="center">unhealthy<break/>blindness</td>
<td valign="middle" align="center">chronic blepharitis<break/>ocular pruritus</td>
<td valign="middle" align="center">chronic blepharitis<break/>ocular pruritus</td>
</tr>
<tr>
<td valign="middle" align="center">E</td>
<td valign="middle" align="center">F</td>
<td valign="middle" align="center">N/I</td>
<td valign="middle" align="center">MiR</td>
<td valign="middle" align="center">Apr/May 2015</td>
<td valign="middle" align="center">BCS 3</td>
<td valign="middle" align="center">0</td>
<td valign="middle" align="center">absent</td>
<td valign="middle" align="center">healthy</td>
<td valign="middle" align="center">ocular opacity<break/>ocular pruritus</td>
<td valign="middle" align="center">normal<break/>ocular pruritus</td>
</tr>
<tr>
<td valign="middle" align="center">F</td>
<td valign="middle" align="center">F</td>
<td valign="middle" align="center">N/I</td>
<td valign="middle" align="center">MiR</td>
<td valign="middle" align="center">Apr/May 2015</td>
<td valign="middle" align="center">BCS 3</td>
<td valign="middle" align="center">0</td>
<td valign="middle" align="center">absent</td>
<td valign="middle" align="center">healthy</td>
<td valign="middle" align="center">ocular opacity<break/>ocular pruritus</td>
<td valign="middle" align="center">normal<break/>ocular pruritus</td>
</tr>
<tr>
<td valign="middle" align="center">G</td>
<td valign="middle" align="center">M</td>
<td valign="middle" align="center">dom</td>
<td valign="middle" align="center">MuR</td>
<td valign="middle" align="center">Nov 2015</td>
<td valign="middle" align="center">BCS 3</td>
<td valign="middle" align="center">0</td>
<td valign="middle" align="center">flattening of the cranium</td>
<td valign="middle" align="center">healthy</td>
<td valign="middle" align="center">normal</td>
<td valign="middle" align="center">phthisis bulbi</td>
</tr>
<tr>
<td valign="middle" align="center">H</td>
<td valign="middle" align="center">N/I</td>
<td valign="middle" align="center">N/I</td>
<td valign="middle" align="center">CuR</td>
<td valign="middle" align="center">Jul 2019</td>
<td valign="middle" align="center">BCS 3</td>
<td valign="middle" align="center">0</td>
<td valign="middle" align="center">absent</td>
<td valign="middle" align="center">healthy</td>
<td valign="middle" align="center">normal</td>
<td valign="middle" align="center">ocular opacity</td>
</tr>
<tr>
<td valign="middle" align="center">I</td>
<td valign="middle" align="center">F</td>
<td valign="middle" align="center">dom</td>
<td valign="middle" align="center">NeR</td>
<td valign="middle" align="center">Aug 2019</td>
<td valign="middle" align="center">BCS 2</td>
<td valign="middle" align="center">1</td>
<td valign="middle" align="center">cutaneous lesions probably due to intraspecific conflict, with purulent discharge</td>
<td valign="middle" align="center">unhealthy</td>
<td valign="middle" align="center">severe blepharitis<break/>ocular pruritus</td>
<td valign="middle" align="center">severe blepharitis<break/>ocular pruritus</td>
</tr>
<tr>
<td valign="middle" align="center">J1 and J2</td>
<td valign="middle" align="center">N/I</td>
<td valign="middle" align="center">N/I</td>
<td valign="middle" align="center">MiR</td>
<td valign="middle" align="center">Aug-Oct<break/>2019</td>
<td valign="middle" align="center">BCS 3</td>
<td valign="middle" align="center">2</td>
<td valign="middle" align="center">absent</td>
<td valign="middle" align="center">unhealthy<break/>blindness<break/>neurological signs<break/>incoordination</td>
<td valign="middle" align="center">ocular opacity</td>
<td valign="middle" align="center">ocular opacity</td>
</tr>
<tr>
<td valign="middle" align="center">K</td>
<td valign="middle" align="center">F</td>
<td valign="middle" align="center">sub</td>
<td valign="middle" align="center">MiR</td>
<td valign="middle" align="center">Aug 2019</td>
<td valign="middle" align="center">BCS 3</td>
<td valign="middle" align="center">1</td>
<td valign="middle" align="center">absent</td>
<td valign="middle" align="center">unhealthy<break/>blindness</td>
<td valign="middle" align="center">mild protrusion of the third eyelid</td>
<td valign="middle" align="center">ocular opacity<break/>periocular swelling</td>
</tr>
<tr>
<td valign="middle" align="center">L</td>
<td valign="middle" align="center">M</td>
<td valign="middle" align="center">N/I</td>
<td valign="middle" align="center">MiR</td>
<td valign="middle" align="center">Sep 2019</td>
<td valign="middle" align="center">BCS 2, then BCS 1</td>
<td valign="middle" align="center">2</td>
<td valign="middle" align="center">cutaneous lesions</td>
<td valign="middle" align="center">unhealthy<break/>blindness</td>
<td valign="middle" align="center">ocular opacity</td>
<td valign="middle" align="center">ocular opacity</td>
</tr>
<tr>
<td valign="middle" align="center">M</td>
<td valign="middle" align="center">N/I</td>
<td valign="middle" align="center">sub</td>
<td valign="middle" align="center">MiR</td>
<td valign="middle" align="center">Sep 2019</td>
<td valign="middle" align="center">BCS 3, then BCS 2</td>
<td valign="middle" align="center">0</td>
<td valign="middle" align="center">absent</td>
<td valign="middle" align="center">unhealthy</td>
<td valign="middle" align="center">ocular opacity</td>
<td valign="middle" align="center">normal</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p><sup>1</sup>F, Female; M, Male; N/I, not identified.</p></fn>
<fn>
<p><sup>2</sup>dom, dominant (alpha); sub, subordinate; N/I, not identified.</p></fn>
<fn>
<p><sup>3</sup>MiR, Miranda River; NeR, Negro River; EPP, Estrada Parque Pantanal road; CuR, Cuiab&#xe1; River; MuR, Mutum River.</p></fn>
<fn>
<p><sup>4</sup>OD, right eye; OS, left eye.</p></fn>
</table-wrap-foot>
</table-wrap>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Giant otters (<italic>Pteronura brasiliensis</italic>) observed in the Brazilian Pantanal presenting ophthalmic disorders: <bold>(A)</bold> Giant otter eyes with normal appearance; <bold>(B-D)</bold> chronic blepharitis, characterized by thickening and hyperpigmentation of the periocular region; <bold>(E, F)</bold> normal appearance of the left eye (OS) and ocular opacity of the right eye (OD); <bold>(G)</bold> phthisis bulbi of OS with flattening of the cranium on the same side; <bold>(H)</bold> OS ocular opacity; <bold>(I)</bold> severe active bilateral blepharitis, characterized by palpebral ulcerations suspected to be excoriations from self-inflicted ocular pruritus or pain; <bold>(J1, J2)</bold> ocular opacity respectively bilateral and OD; <bold>(K)</bold> ocular opacity and periocular swelling noted in the OS and mild third eyelid protrusion in the OD; <bold>(L, M)</bold> &#x2013; ocular opacity respectively bilateral and OD. Video frames: <bold>(D-F, J2, L)</bold>. Photographs: <bold>(A-C, G-I, J1, K, M)</bold>.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmamm-04-1634280-g002.tif">
<alt-text content-type="machine-generated">A collage of images showing giant otters in various settings. Image A displays an otter with an open mouth in water. Image B shows an otter peeking from a den. Image C features an otter standing on land. Image D presents an otter lying on its side. Image E captures an otter behind leaves. Image F shows an otter looking upward. Image G features an otter feeding. Image H displays an otter in water with a partially submerged body. Image I shows an injured otter on land. Image J1 is a close-up of an otter's face. Image J2 features an otter swimming. Image K shows an otter's head above water. Image L presents an otter eating. Image M displays an otter holding prey.</alt-text>
</graphic></fig>
<sec id="s3_1">
<title>Southern Pantanal</title>
<p><underline>Estrada Parque Pantanal road</underline>: Since monitoring started in 2002, individuals with an unhealthy appearance were first registered in December 2009 in the southern Pantanal (individuals B and C, geographic coordinates 19&#xb0;19&#x2019;7.34&#x201d;S; 57&#xb0;3&#x2019;15.20&#x201d;W). Both had a BCS of 2 and exhibited swollen and hyperemic mucous membranes in the anus and mouth. Chronic blepharitis was observed in both eyes, as previously reported by <xref ref-type="bibr" rid="B32">Ribas et&#xa0;al. (2012)</xref>.</p>
<p><underline>Miranda River</underline>:</p>
<p>Several observations were made in the Miranda River across different years:</p>
<p>April-May 2015: A group composed of one adult male (D) and two adult females (E and F, 19&#xb0;34&#x2019;36.07&#x201d;S; 57&#xb0;2&#x2019;45.05&#x201d;W) showed ophthalmic disorders and signs of physical debilitation. Notably, two of these otters (E and F) had been recorded as clinically healthy in November 2014. All three otters exhibited ocular discomfort, including frequent eye scratching against each other and the ground. The male was severely debilitated and exhibited behaviors suggesting remarkably visual impairment, such as nearly colliding with our boat and failing to notice our presence at the group&#x2019;s campsite. He also had three cutaneous lesions on his cervical region (<xref ref-type="supplementary-material" rid="SM1"><bold>Supplementary Material S1</bold></xref>). Although the images show only chronic blepharitis without obvious globe abnormalities, these behaviors indicate possible visual deficits. The underlying cause could involve the retina, optic nerve, or central visual pathways, but this cannot be determined from visual inspection alone.</p>
<p>August-September 2019: A new group of four giant otters was observed (19&#xb0;33&#x2019;36.48&#x201d;S; 57&#xb0;2&#x2019;54.49&#x201d;W), three of which later developed ophthalmic lesions. One individual (K) presented ocular opacity suspected to be corneal edema in the OS and mild third eyelid protrusion in the OD. In early September, two additional group members (L and M) developed ocular opacity: bilateral in L and unilateral in M. Individual L appeared thin, (BCS 2), with a dorsal cutaneous lesion, later declining to BCS 1 and showing difficulty climbing the riverbank to access the den. Additional cutaneous lesions developed on the right thoracic limb and shoulder (<xref ref-type="supplementary-material" rid="SM1"><bold>Supplementary Material S2</bold></xref>). In contrast, M maintained a BCS of 3 at that time. By late September only three individuals were recorded; L was absent and M showed further health deterioration. Three days later, the group was sighted again, and M was markedly more emaciated and severely debilitated. This encounter represented the last time the group was observed in 2019. In July 2021, the dominant female, the only individual in the group without ophthalmic abnormalities (not included in this study), was observed again, accompanied by a new male.</p>
<p>August-October 2019 (neighboring group): Another group composed of three individuals had an adult otter, of undetermined sex, presenting bilateral ocular opacity, suspected to be corneal edema. Throughout August, the individual appeared clinically healthy despite the ocular findings. However, in September the OD started to present conjunctival hyperemia. By October, the otter showed partial paralysis and evident motor impairment suggestive of near-drowning behavior, characterized by an inability to swim and maintain buoyancy. During this period, the ocular disease had progressed, with both eyes becoming more opaque and prominently protruding, and the OD showing marked conjunctival hyperemia. The individual was observed for approximately two minutes before it submerged (<xref ref-type="supplementary-material" rid="SM1"><bold>Supplementary Material S3</bold></xref>). Despite extensive efforts, we were unable to locate the animal or its carcass. Over several hours, no further traces were found. During this period, the remaining group members were observed engaging in search behaviors, including intense vocalizations and active patrolling the surrounding area. In subsequent monitoring sessions, the affected individual was no longer observed with the group (J1 and J2 refer to this same individual, in its first and last observations).</p>
<p><underline>Negro River</underline>:</p>
<p>In August 2019, an adult otter (I, 19&#xb0;34.676&#x2019;S; 56&#xb0;09.282&#x2019;W) presented cutaneous lesions likely caused by intraspecific conflicts and active bilateral blepharitis. It was observed scratching its face on the ground multiple times, presumably due to pruritus or pain. The other two giant otters in the group appeared healthy. Seventy days later, the same otter was sighted again, showing significant recovery with post-inflammatory hyperpigmentation (darker areas at the lesion sites), consistent with a self-limiting infection.</p>
</sec>
<sec id="s3_2">
<title>Northern Pantanal</title>
<p><underline>Mutum River</underline>:</p>
<p>In November 2015, a dominant adult male (G, 16&#xb0;20&#x2019;16.49&#x201d;S; 55&#xb0;51&#x2019;50.38&#x201d;W) presented with phthisis bulbi on the OS. Although overall clinically healthy, this individual exhibited cranial asymmetry, with a flattening of the upper third of the skull, which may indicate a history of previous cranial trauma.</p>
<p><underline>Cuiab&#xe1; River</underline>:</p>
<p>In July 2019, an adult giant otter of undetermined sex (H, 17&#xb0;17&#x2019;1.30&#x201d;S; 56&#xb0;41&#x2019;48.90&#x201d;W) was recorded exhibiting unilateral ocular opacity.</p>
</sec>
</sec>
<sec id="s4" sec-type="discussion">
<title>Discussion</title>
<p>Ocular anatomy and normal ophthalmic parameters in mustelids are relatively well-documented in the literature (e.g. <xref ref-type="bibr" rid="B29">Montiani-Ferreira and Freeman, 2022</xref>). However, information on ocular disorders in free-ranging Lutrinae remains limited. Notable exceptions include cases of ocular chemical burns caused by oil spills in sea otters (<italic>Enhydra lutris</italic>) (<xref ref-type="bibr" rid="B28">Lipscomb et&#xa0;al., 1993</xref>), and retinal dysplasia observed in Eurasian otters (<italic>Lutra lutra</italic>) (<xref ref-type="bibr" rid="B51">Williams et&#xa0;al., 2004</xref>). To our knowledge, there is no published data on ocular diseases in giant otters, so far. This lack of information may be attributed to several factors, including the Endangered status of the species (<xref ref-type="bibr" rid="B18">Groenendijk et&#xa0;al., 2021</xref>), their low population densities (<xref ref-type="bibr" rid="B11">Duplaix et&#xa0;al., 2015</xref>), and the challenges of developing an effective method of capturing affected individuals from the social group.</p>
<p>Giant otters are territorial social mammals that interact playfully and aggressively, particularly during agonistic encounters between groups, which can be extremely aggressive and often result in wounds and scars (<xref ref-type="bibr" rid="B36">Rosas and Mattos, 2003</xref>; <xref ref-type="bibr" rid="B33">Ribas and Mour&#xe3;o, 2004</xref>). This could explain the lesions observed in a giant otter in this study (I). Cases of myiasis in free-ranging giant otters likely resulted from intraspecific fights and ultimately led to the death of the affected individuals (<xref ref-type="bibr" rid="B14">Foerster et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B16">Gonchoroski et&#xa0;al., 2025</xref>). In aquatic mammals, such as cetaceans, playful behavior can lead to blunt or sharp trauma to the eyes and surrounding structures (<xref ref-type="bibr" rid="B6">Colitz et&#xa0;al., 2016</xref>), suggesting that similar mechanisms of injuries may also occur in otters, although no specific records currently exist.</p>
<p>Epidemiological studies on giant otters are limited, although, like other otter species, they are vulnerable to various pathogens commonly spread by domestic animals (<xref ref-type="bibr" rid="B15">Foster-Turley et&#xa0;al., 1990</xref>), such as canine distemper virus (<xref ref-type="bibr" rid="B48">White et&#xa0;al., 2013</xref>), leptospirosis (<xref ref-type="bibr" rid="B47">White et&#xa0;al., 2018</xref>), and canine parvovirus (<xref ref-type="bibr" rid="B12">Echenique et&#xa0;al., 2018</xref>). Systemic infections caused by <italic>Toxoplasma gondii</italic> can lead to significant morbidity and mortality in mustelids, as observed in southern sea otters (<italic>Enhydra lutris nereis</italic>) and black-footed ferrets (<italic>Mustela nigripes</italic>) (<xref ref-type="bibr" rid="B2">Burns et&#xa0;al., 2003</xref>; <xref ref-type="bibr" rid="B8">Conrad et&#xa0;al., 2005</xref>). In southern sea otters, <italic>T.gondii</italic> was detected in 52% of necropsied and 38% of live-captured animals (<xref ref-type="bibr" rid="B8">Conrad et&#xa0;al., 2005</xref>). Recently, a specific strain of <italic>T. gondii</italic> was identified as the cause of death in several sea otters in California (<xref ref-type="bibr" rid="B39">Shapiro et&#xa0;al., 2019</xref>). Clinical signs of toxoplasmosis in otters can include a range of neurological (ataxia, head tilt, tremors), ocular (corneal edema, uveitis, blindness), respiratory (nasal discharge, dyspnea), and general systemic signs (weight loss, lethargy, weakness) (<xref ref-type="bibr" rid="B8">Conrad et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B39">Shapiro et&#xa0;al., 2019</xref>). Based on observed clinical presentation, toxoplasmosis may be a potential diagnosis for individuals from giant otter groups inhabiting the same area of the Miranda River (D-F and K-M). However, these animals were not captured or sampled, preventing diagnostic confirmation. These groups inhabited areas near a large bridge adjacent to a riverside community, where increased proximity to humans and domestic animals might increase the risk of exposure to contaminated water or prey containing oocysts from feline feces.</p>
<p>Another infectious disease of concern is caused by canine adenovirus type 1, which can lead to incoordination, generalized ataxia, and bilateral ocular opacity, a condition known as the &#x201c;blue eye&#x201d; phenomenon. This pathology was recently described in a hoary fox (<italic>Lycalopex vetulus</italic>) from Brazil, co-infected with canine distemper virus (<xref ref-type="bibr" rid="B40">Silva et&#xa0;al., 2023</xref>). In otters, canine adenovirus type 1 infection can be fatal, as observed in a Eurasian otter showing anorexia, lethargy, and weight loss (<xref ref-type="bibr" rid="B30">Park et&#xa0;al., 2007</xref>). Sea otters can also be infected by this viral agent (<xref ref-type="bibr" rid="B15">Foster-Turley et&#xa0;al., 1990</xref>). Additionally, an outbreak of adenovirus infection causing acute hepatitis was reported in otariids (<xref ref-type="bibr" rid="B21">Inoshima et&#xa0;al., 2013</xref>). These studies suggest that semiaquatic mammals are susceptible to this pathogen, which is commonly found in unvaccinated domestic dogs. One giant otter in our study (identified as J1 and J2) presented systemic signs resembling that observed in the hoary fox, suggesting canine adenovirus as another potential etiological agent. In Brazil, canine adenovirus infection has become less common in urban areas due to widespread vaccination programs. However, in the Pantanal, domestic dogs are generally not vaccinated, and when vaccination occurs, it is usually limited to rabies.</p>
<p>The avian eye trematode <italic>Philophthalmus lachrymosus</italic>, which inhabits the palpebral conjunctiva, has been associated with severe conjunctivitis and blindness in capybaras (<italic>Hydrochoerus hydrochaeris</italic>), a species that frequently comes into close contact with avian definitive hosts (<xref ref-type="bibr" rid="B31">Pinto et&#xa0;al., 2005</xref>). Although we identified four apparently blind giant otters (D, J1/2, K, and L), there are no confirmed records of <italic>P. lachrymosus</italic> occurrence in the Pantanal or in other mammalian species. However, its presence in shared aquatic habitats may pose a risk to other susceptible mammals.</p>
<p>Cases of blindness in Eurasian otters in Britain have been linked to population declines potentially caused by exposure to organochlorine insecticides (<xref ref-type="bibr" rid="B49">Williams, 1989</xref>; <xref ref-type="bibr" rid="B23">Jefferies and Hanson, 2000</xref>). These compounds are known to induce hypothyroidism, which affects vitamin A metabolism leading to hypovitaminosis A (<xref ref-type="bibr" rid="B22">Jefferies, 1975</xref>). In mammals, vitamin A deficiency is associated with ocular discharge, conjunctivitis, keratitis, and corneal hyperkeratosis, conditions that could explain the blindness observed in British otters (<xref ref-type="bibr" rid="B23">Jefferies and Hanson, 2000</xref>).</p>
<p>In the Brazilian Pantanal, agricultural activities are increasing over recent years. According to MapBiomas, a platform for mapping land use and cover in Brazil, agricultural land for crops increased by approximately 100,000 hectares between 2021 and 2023. These data underscore growing pressure on the Pantanal and the urgent need to implement sustainable land use practices to protect this ecoregion. Although agrochemical residue studies in giant otters are lacking, elevated mercury concentrations have been reported in fur samples from giant otters living in the same area where blind otters were observed in the southern Pantanal (Miranda River), suggesting potential toxicological risks (<xref ref-type="bibr" rid="B43">Soresini et&#xa0;al., 2021</xref>). While high concentrations of mercury are known to contribute to neurological effects, including central blindness, there is no evidence that mercury causes the specific ophthalmic abnormalities observed in Pantanal otters. Nonetheless, other environmental contaminants, such as pesticides, may contribute to ocular alterations, as reported in Eurasian otters (<xref ref-type="bibr" rid="B50">Williams et&#xa0;al., 2000</xref>). However, more detailed studies, including clinical evaluation and a complete ophthalmic examination are necessary to identify the prevalence and etiology of ocular pathologies in giant otters.</p>
<p>This study represents the first documented series of ocular disorder cases in free-ranging giant otters. Although limited by the absence of clinical diagnosis confirmed through detailed ophthalmic examinations, these findings presented here expand current knowledge of health issues affecting this endangered species. Furthermore, these conditions may be linked to multiple causes, including trauma, infections, parasitism, and exposure to environmental contaminants such as organochlorine insecticides. These observations highlight the need for comprehensive clinical and ecotoxicological investigations, especially considering the increasing anthropogenic pressures in the Pantanal. Future studies should aim to develop more effective capture techniques for this species, which would allow the safe collection of biological samples and enable accurate clinical and laboratory diagnoses, thereby improving understanding of the causes and prevalence of ocular and systemic disorders in giant otters.</p>
</sec>
</body>
<back>
<sec id="s5" sec-type="data-availability">
<title>Data availability statement</title>
<p>The original contributions presented in the study are included in the article/<xref ref-type="supplementary-material" rid="SM1"><bold>Supplementary Material</bold></xref>. Further inquiries can be directed to the corresponding author.</p></sec>
<sec id="s6" sec-type="ethics-statement">
<title>Ethics statement</title>
<p>The animal study was approved by Embrapa Pantanal Committee on Ethics for the Use of Animals in Research. The study was conducted in accordance with the local legislation and institutional requirements. Written informed consent was obtained from the participant/patient(s) for the publication of this case report.</p></sec>
<sec id="s7" sec-type="author-contributions">
<title>Author contributions</title>
<p>GS: Conceptualization, Data curation, Investigation, Methodology, Project administration, Writing &#x2013; original draft, Visualization. NF: Data curation, Investigation, Methodology, Writing &#x2013; review &amp; editing, Visualization. AS: Data curation, Writing &#x2013; review &amp; editing, Validation. FD: Writing &#x2013; review &amp; editing, Investigation. CR: Writing &#x2013; review &amp; editing, Investigation. CL: Writing &#x2013; review &amp; editing. GM: Project administration, Resources, Supervision, Writing &#x2013; review &amp; editing.</p></sec>
<ack>
<title>Acknowledgments</title>
<p>We thank the Federal University of Mato Grosso do Sul and Embrapa Pantanal for their logistical support. We also thank Stefan Grol for his invaluable help in providing information and pictures of one of the giant otters.</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="ai-statement">
<title>Generative AI statement</title>
<p>The author(s) declare that no Generative AI was used in the creation of this manuscript.</p>
<p>Any alternative text (alt text) provided alongside figures in this article has been generated by Frontiers with the support of artificial intelligence and reasonable efforts have been made to ensure accuracy, including review by the authors wherever possible. If you identify any issues, please contact us.</p></sec>
<sec id="s11" 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></sec>
<sec id="s12" sec-type="supplementary-material">
<title>Supplementary material</title>
<p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="https://www.frontiersin.org/articles/10.3389/fmamm.2025.1634280/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fmamm.2025.1634280/full#supplementary-material</ext-link></p>
<supplementary-material xlink:href="Video1.mp4" id="SM1" mimetype="video/mp4"/>
<supplementary-material xlink:href="Video2.mp4" id="SM2" mimetype="video/mp4"/>
<supplementary-material xlink:href="Video3.mp4" id="SM3" mimetype="video/mp4"/></sec>
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<fn id="n1" fn-type="custom" custom-type="edited-by">
<p>Edited by: <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/490125">Inger Suzanne Prange</ext-link>, Appalachian Wildlife Research Institute, United States</p></fn>
<fn id="n2" fn-type="custom" custom-type="reviewed-by">
<p>Reviewed by: <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/641801">Julie Deanne Sheldon</ext-link>, University of Tennessee, Knoxville, United States</p>
<p><ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/1175598">Braidee Foote</ext-link>, The University of Tennessee, Knoxville, United States</p></fn>
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