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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Amphib. Reptile Sci.</journal-id>
<journal-title>Frontiers in Amphibian and Reptile Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Amphib. Reptile Sci.</abbrev-journal-title>
<issn pub-type="epub">2813-6780</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/famrs.2024.1348251</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Amphibian and Reptile Science</subject>
<subj-group>
<subject>Perspective</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Protecting Japanese giant salamanders (<italic>Andrias japonicus</italic>) in the Nawa River Basin, Japan: policy recommendations addressing water pollution and waterway disruption</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Borz&#xe9;e</surname>
<given-names>Ama&#xeb;l</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="author-notes" rid="fn001">
<sup>*</sup>
</xref>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Angulo</surname>
<given-names>Ariadne</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Meredith</surname>
<given-names>Helen</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Taguchi</surname>
<given-names>Yuki</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2650870"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Groffen</surname>
<given-names>Jordy</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1635613"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Kohler</surname>
<given-names>Dallin Bradshaw</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2650269"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Abernethy</surname>
<given-names>John Peter Duncan</given-names>
</name>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2594037"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Othman</surname>
<given-names>Siti N.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/929525"/>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Messenger</surname>
<given-names>Kevin</given-names>
</name>
<xref ref-type="aff" rid="aff8">
<sup>8</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Heo</surname>
<given-names>Kyongman</given-names>
</name>
<xref ref-type="aff" rid="aff8">
<sup>8</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Wan</surname>
<given-names>Le</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Um</surname>
<given-names>Tae Eun</given-names>
</name>
<xref ref-type="aff" rid="aff9">
<sup>9</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2650268"/>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Xiaoli</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
<role content-type="https://credit.niso.org/contributor-roles/investigation/"/>
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<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Shin</surname>
<given-names>Yucheol</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff10">
<sup>10</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1655483"/>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Bae</surname>
<given-names>Yoonhyuk</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
<role content-type="https://credit.niso.org/contributor-roles/investigation/"/>
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<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Zhenqi</given-names>
</name>
<xref ref-type="aff" rid="aff11">
<sup>11</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Qiu</surname>
<given-names>Zhixin</given-names>
</name>
<xref ref-type="aff" rid="aff11">
<sup>11</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
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</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Pearce</surname>
<given-names>Richard</given-names>
</name>
<xref ref-type="aff" rid="aff12">
<sup>12</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2647566"/>
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</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Amphibian Specialist Group, Species Survival Commission, International Union for the Conservation of Nature</institution>, <addr-line>Toronto, ON</addr-line>, <country>Canada</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Laboratory of Animal Behavior and Conservation, College of Life Sciences, Nanjing Forestry University</institution>, <addr-line>Nanjing, Jiangsu</addr-line>, <country>China</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Amphibian Survival Alliance</institution>, <addr-line>London</addr-line>, <country>United Kingdom</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Asahi Hanzaki Research Association</institution>, <addr-line>Hiroshima</addr-line>, <country>Japan</country>
</aff>
<aff id="aff5">
<sup>5</sup>
<institution>College of Science and Engineering, James Cook University</institution>, <addr-line>Townsville, QLD</addr-line>, <country>Australia</country>
</aff>
<aff id="aff6">
<sup>6</sup>
<institution>Laboratory of Animal Behaviour and Conservation, College of Ecology and the Environment, Nanjing Forestry University</institution>, <addr-line>Nanjing, Jiangsu</addr-line>, <country>China</country>
</aff>
<aff id="aff7">
<sup>7</sup>
<institution>School of Biological and Environmental Sciences, Liverpool John Moores University</institution>, <addr-line>Liverpool</addr-line>, <country>United Kingdom</country>
</aff>
<aff id="aff8">
<sup>8</sup>
<institution>Herpetology and Applied Conservation Laboratory, College of Life Sciences, Nanjing Forestry University</institution>, <addr-line>Nanjing, Jiangsu</addr-line>, <country>China</country>
</aff>
<aff id="aff9">
<sup>9</sup>
<institution>Laboratory of Animal Communication, Department of EcoScience, Ewha Woman&#x2019;s University</institution>, <addr-line>Seoul</addr-line>, <country>Republic of Korea</country>
</aff>
<aff id="aff10">
<sup>10</sup>
<institution>Department of Biological Sciences, College of Natural Science, Kangwon National University</institution>, <addr-line>Chuncheon</addr-line>, <country>Republic of Korea</country>
</aff>
<aff id="aff11">
<sup>11</sup>
<institution>The Co&#x2212;Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University</institution>, <addr-line>Nanjing</addr-line>, <country>China</country>
</aff>
<aff id="aff12">
<sup>12</sup>
<institution>Sustainable Daisen Non-Profit Organization</institution>, <addr-line>Tottori</addr-line>, <country>Japan</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: David Lesbarreres, Environment and Climate Change Canada (ECCC), Canada</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Sara L. Ashpole, St. Lawrence University, United States</p>
<p>Benjamin Tapley, Zoological Society of London, United Kingdom</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Ama&#xeb;l Borz&#xe9;e, <email xlink:href="mailto:amaelborzee@gmail.com">amaelborzee@gmail.com</email>; Richard Pearce, <email xlink:href="mailto:richard@bushidojapan.com">richard@bushidojapan.com</email>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>28</day>
<month>05</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>2</volume>
<elocation-id>1348251</elocation-id>
<history>
<date date-type="received">
<day>02</day>
<month>12</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>17</day>
<month>04</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Borz&#xe9;e, Angulo, Meredith, Taguchi, Groffen, Kohler, Abernethy, Othman, Messenger, Heo, Wan, Um, Zhang, Shin, Bae, Wang, Qiu and Pearce</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Borz&#xe9;e, Angulo, Meredith, Taguchi, Groffen, Kohler, Abernethy, Othman, Messenger, Heo, Wan, Um, Zhang, Shin, Bae, Wang, Qiu and Pearce</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<p>The Japanese giant salamander, <italic>Andrias japonicus</italic>, is an iconic but declining species of aquatic amphibian. A population within the Nawa River Basin of Tottori Prefecture persists but faces two significant threats. The first major threat is waterway obstructions, in the form of dams, weirs, and concrete embankments, which severely fragment and degrade the habitat. The second is water pollution, primarily caused by runoff from animal farms. Both threats to <italic>A. japonicus</italic> can be mitigated with proper actions. We provide science-based recommendations, advocating for the modification of dams and weirs by implementing ladderways to restore habitat connectivity and the provisioning of adequate breeding habitat in the form of artificial nest boxes. We also recommend the implementation of regular water quality monitoring and the enforcement of regulations regarding allowed runoff from animal farms. The Nawa River Basin could also be designated as an official sanctuary area for the Japanese Giant Salamander, lending additional formal protection and providing ecotourism opportunities for economically declining rural areas. Though the threats to <italic>A. japonicus</italic> are serious, the implementation of these mitigation measures and continual monitoring can allow this remarkable species to thrive.</p>
</abstract>
<kwd-group>
<kwd>
<italic>Andrias</italic>
</kwd>
<kwd>conservation needs</kwd>
<kwd>policy recommendation</kwd>
<kwd>habitat connectivity</kwd>
<kwd>giant salamanders</kwd>
<kwd>Japan</kwd>
<kwd>population monitoring</kwd>
<kwd>water pollution</kwd>
</kwd-group>
<counts>
<fig-count count="3"/>
<table-count count="1"/>
<equation-count count="0"/>
<ref-count count="80"/>
<page-count count="9"/>
<word-count count="3929"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Conservation</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<label>1</label>
<title>Introduction</title>
<sec id="s1_1">
<label>1.1</label>
<title>Species introduction</title>
<p>Amphibians are declining globally (<xref ref-type="bibr" rid="B2">Bishop et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B74">Wake, 2012</xref>; <xref ref-type="bibr" rid="B15">Green et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B41">Luedtke et&#xa0;al., 2023</xref>), with more than 41% of species now listed as threatened on the IUCN Red List of Threatened Species, mostly because of habitat loss (<xref ref-type="bibr" rid="B21">IUCN, 2023</xref>). Almost two-thirds of salamander species (Caudata) are under threat (57.8%; <xref ref-type="bibr" rid="B21">IUCN, 2023</xref>), a trend resulting principally from invasive and other problematic species, genes and diseases; agriculture and aquaculture; residential and commercial development; and biological resource use (<xref ref-type="bibr" rid="B21">IUCN, 2023</xref>). Threats are area- and species-specific, and the ecology of each species best predicts the threats to this species, and the steps necessary for their conservation. However, a point shared among all Giant Salamander (Cryptobranchidae) species, the Asian Giant Salamanders (<italic>Andrias</italic> spp.) and North American Hellbenders (<italic>Cryptobranchus</italic> spp.), is the population decline (<xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>).</p>
<p>Japanese Giant Salamanders (<italic>Andrias japonicus</italic>) are an aquatic species of Cryptobranchid found only on three of Japan&#x2019;s main islands of Honshu, Kyushu and Shikoku with the population on Honshu only in the south-west of the island and much of their habitat being highly fragmented (<xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>). As breeding habitat, the sites where spawning nests and juveniles are most common tends to be in relatively small and lotic habitats in the upper tributaries of streams (<xref ref-type="bibr" rid="B52">Okada et&#xa0;al., 2008</xref>) these habitat are especially sensitive to change from construction and modification. The Japanese Giant Salamander is a key umbrella species currently listed as Vulnerable by the IUCN Red List of Threatened Species and the population size of the species has been declining for close to a century, with the peak in decline between the 1950s and 1970s (<xref ref-type="bibr" rid="B23">IUCN SCC Amphibian Specialist Group, 2022</xref>). The population density is currently estimated to be between 40 and 69 individuals per km of river length in good quality habitat with little water pollution, few or no barriers to movement and suitable banks with cavities for nests (<xref ref-type="bibr" rid="B66">Taguchi and Natuhara, 2009</xref>; <xref ref-type="bibr" rid="B64">Taguchi, 2009a</xref>). Habitat loss was the principal threat until the mid-2000s, and it remains the case for some sub-populations (<xref ref-type="bibr" rid="B53">Ota, 2000</xref>; <xref ref-type="bibr" rid="B27">Kaneko and Matsui, 2004</xref>), although hybridization with the introduced Chinese Giant Salamanders (<italic>Andrias davidianus</italic> and <italic>Andrias sligoi</italic>) is increasingly prevalent (<xref ref-type="bibr" rid="B47">Matsui et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B44">Matsui, 2017</xref>; <xref ref-type="bibr" rid="B23">IUCN SCC Amphibian Specialist Group, 2022</xref>; <xref ref-type="bibr" rid="B18">Hara et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B51">Nishikawa et&#xa0;al., 2024</xref>). Specifically, the construction of obstructions along waterways and artificial banks are the main threats (<xref ref-type="bibr" rid="B23">IUCN SCC Amphibian Specialist Group, 2022</xref>), resulting in habitat fragmentation and the loss of breeding habitat respectively (<xref ref-type="bibr" rid="B73">Wakabayashi et&#xa0;al., 1976</xref>; <xref ref-type="bibr" rid="B42">Matsui, 2000</xref>; <xref ref-type="bibr" rid="B66">Taguchi and Natuhara, 2009</xref>; <xref ref-type="bibr" rid="B78">Yamasaki et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B43">Matsui, 2014</xref>). Constructions, like dams and weirs, can modify in-stream habitat and flow regime, disrupt animal behavior, decrease gene flow, alter water-quality parameters, increase sediment deposition, habitat fragmentation, the loss of breeding habitat, and ultimately result in direct displacement and mortality of individuals (<xref ref-type="bibr" rid="B8">Cole and Landres, 1995</xref>; <xref ref-type="bibr" rid="B76">Watters, 1999</xref>; <xref ref-type="bibr" rid="B42">Matsui, 2000</xref>; <xref ref-type="bibr" rid="B6">Bunn and Arthington, 2002</xref>; <xref ref-type="bibr" rid="B35">Lessard and Hayes, 2003</xref>; <xref ref-type="bibr" rid="B43">Matsui, 2014</xref>). Especially, the removal of valuable refugia such as cobble shelters can greatly alter habitat characteristics required by aquatic organisms, including fish, macro-invertebrates, and aquatic (juvenile) salamanders (<xref ref-type="bibr" rid="B31">Kondolf, 2000</xref>; <xref ref-type="bibr" rid="B48">Milner and Piorkowski, 2004</xref>; <xref ref-type="bibr" rid="B11">Diaz et&#xa0;al., 2015</xref>).</p>
<p>Recent research shows that, against original expectations, small streams and tributaries are critical to the development of giant salamander larvae (<xref ref-type="bibr" rid="B3">Bjordahl et&#xa0;al., 2020</xref>), and conservation plans must therefore be adjusted to include small streams and tributaries. In addition, small streams and tributaries are also beneficial for the development of larvae and juveniles, two age groups hard to find, as the species takes about 15 years to reach sexual maturity (<xref ref-type="bibr" rid="B23">IUCN SCC Amphibian Specialist Group, 2022</xref>).</p>
<p>Conservation actions for the Japanese Giant Salamanders have so far included listing the species as a &#x201c;Special Natural Monument&#x201d; under the &#x201c;Act on Protection of Cultural Properties&#x201d; in Japan, resulting in Federal protection from collection and killing, and the protection of some small sections of the species&#x2019; range, including some of the breeding and non-breeding habitat (<xref ref-type="bibr" rid="B52">Okada et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B56">Saitoh et&#xa0;al., 2014</xref>). However, this act it is limited in that it does not request conservation actions to be taken to improve the situation for wildlife by either national or local government (<xref ref-type="bibr" rid="B56">Saitoh et&#xa0;al., 2014</xref>). Much of their habitat outside of these few reserves remains unprotected (<xref ref-type="bibr" rid="B30">Kobara et&#xa0;al., 1980</xref>; <xref ref-type="bibr" rid="B52">Okada et&#xa0;al., 2008</xref>). Japanese Giant Salamanders are also included in CITES Appendix I, and in addition collection is completely forbidden throughout the range of the species (<xref ref-type="bibr" rid="B45">Matsui and Hayashi, 1992</xref>), therefore collection for food, medicine and the pet trade is forbidden and it is now expected to have stopped. In addition, salamander meat is not considered a delicacy worth facing the steep punishments of a fine of up to 300,000 yen and up to 5 years in prison for killing or collecting a Natural Monument (<xref ref-type="bibr" rid="B1">Act on the Protection of Cultural Properties, 1950</xref>). Although the threats from collection within Japan are low, the dangers presented from hybridization with other species of Giant Salamanders originating from China are high and should the Japanese Giant Salamander be delisted and commercially traded, further pressure would be put on the few populations without hybrids. It is thus one of the key reasons that the species is listed as CITES Appendix I (<xref ref-type="bibr" rid="B7">CITES, 2009</xref>).</p>
<p>Japanese Giant Salamanders are not only a Natural Monument due to their endemicity to Japan but also their cultural significance to Japanese culture, they are inspiration for monsters both old and new and a common mascot throughout the country. The legendary Kappa, a Japanese monster or y&#x14d;kai in the form of a half human half monster water demon is supposedly inspired by the Japanese Giant Salamander (<xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>) whilst the modern-day monster, the Pok&#xe9;mon Quagsire is also drawing on the Japanese Giant Salamander for its appearance. Japanese Giant Salamanders are not just seen as monsters though, they are also used as symbols and mascots with Ou-Chan being a mascot in the shape of a giant salamander being used to teach people about the value of clean rivers in Toyooka City in Hy&#x14d;go Prefecture (<xref ref-type="bibr" rid="B36">Leveille, n.d.</xref>). In some parts of Japan, the Japanese Giant Salamanders are celebrated with a festival called the Hanzaki Matsuri held annually in the village of Yubara Onsen in Okayama Prefecture where they are venerated (<xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>).</p>
<p>The species is being supported through <italic>ex situ</italic> conservation such as captive breeding (<xref ref-type="bibr" rid="B30">Kobara et&#xa0;al., 1980</xref>) with the first breeding being recorded at the Amsterdam Zoo in 1904 (<xref ref-type="bibr" rid="B28">Kerbert, 1904</xref>) and it has been reliably bred at the Asa Zoological Park in Japan since 1979 (<xref ref-type="bibr" rid="B32">Kubawara et&#xa0;al., 1989</xref>; <xref ref-type="bibr" rid="B50">Murphy and Gratwicke, 2017</xref>), although re-introductions have not yet been conducted. Current <italic>in situ</italic> support is focused on the development and installation of ladders and artificial nests to help Japanese Giant Salamander traverse dams and weirs to improve movement, connectivity and gene flow between populations (<xref ref-type="bibr" rid="B17">Hara, 2021</xref>; <xref ref-type="bibr" rid="B23">IUCN SCC Amphibian Specialist Group, 2022</xref>).</p>
<p>Little data are available about the population of Japanese Giant Salamanders in the Nawa River Basin area in Tottori Prefecture, but the perceived absence of Chinese Giant Salamanders, the distance from the main urban areas and the comparatively lower pressure due to a lower human density suggests a comparatively stable population. For these populations, conservation actions can have a strong benefit in terms of the number of individuals protected and the conservation of the species in the long run.</p>
</sec>
<sec id="s1_2">
<label>1.2</label>
<title>Risks resulting from obstruction of waterways</title>
<p>Caudata are threatened globally by obstruction to waterways such as dams and weirs (<xref ref-type="bibr" rid="B14">Gratwicke, 2008</xref>; <xref ref-type="bibr" rid="B72">Unger et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>). These structures present obstacles to upstream or downstream movement during the life cycle of salamanders (<xref ref-type="bibr" rid="B24">Jackson, 2003</xref>; <xref ref-type="bibr" rid="B64">Taguchi, 2009a</xref>), resulting in habitat fragmentation and the loss of genetic connectivity (<xref ref-type="bibr" rid="B4">Blank et&#xa0;al., 2013</xref>). The obstruction of waterways through dam building has already contributed to the extinction of other vertebrates, such as the Chinese Paddlefish (<italic>Psephurus gladius</italic>; <xref ref-type="bibr" rid="B58">Scarnecchia, 2023</xref>), and these obstructions are resulting in the decline of freshwater megafauna such as the Russian sturgeon (<italic>Acipenser gueldenstaedii</italic>; <xref ref-type="bibr" rid="B13">Gesner et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B19">He et&#xa0;al., 2017</xref>), the Chinese sturgeon (<italic>A. sinensis</italic>; <xref ref-type="bibr" rid="B77">Wu et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B19">He et&#xa0;al., 2017</xref>), and the Gharial (<italic>Gavialis gangeticus</italic>; <xref ref-type="bibr" rid="B19">He et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B34">Lang et&#xa0;al., 2019</xref>). It is not only freshwater megafauna that are affected but potentially of greater concern is the impact these dams are having on the stocks of diadromous fish; those which require to live in both marine and freshwater habitats to complete their life histories (<xref ref-type="bibr" rid="B68">Tamario et&#xa0;al., 2019</xref>). Many of these species are of significant economic value to humans, such as salmon and shad, with the current stocks of many of these species in North America 90% below historical levels due to the loss of habitat connectivity through dam building (<xref ref-type="bibr" rid="B39">Limburg and Waldman, 2009</xref>).</p>
<p>The development of embankments, generally through concrete layering presents another threat to many freshwater vertebrates and results in the loss of habitat, prey and pollution (<xref ref-type="bibr" rid="B19">He et&#xa0;al., 2017</xref>). Giant salamanders are especially impacted by bankside damage, channelization, dams, and sedimentation (<xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>). While some environmental damage can be mitigated, the impact of dams is generally irreversible (<xref ref-type="bibr" rid="B40">Liu and Lu, 2007</xref>; <xref ref-type="bibr" rid="B9">Dai et&#xa0;al., 2009</xref>; <xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>). For Japanese Giant Salamanders, these waterway alterations have resulted in population fragmentation, followed by an increased risk of extinction because of the absence of genetic exchange (<xref ref-type="bibr" rid="B73">Wakabayashi et&#xa0;al., 1976</xref>; <xref ref-type="bibr" rid="B46">Matsui and Tominaga, 2007</xref>; <xref ref-type="bibr" rid="B66">Taguchi and Natuhara, 2009</xref>). In addition, damages of natural banks impact the breeding habitat and daytime refuge habitat of the species (<xref ref-type="bibr" rid="B70">Tochimoto, 1995</xref>, <xref ref-type="bibr" rid="B71">1996</xref>; <xref ref-type="bibr" rid="B67">Takahashi et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>).</p>
<p>The main threat to the Japanese Giant Salamanders in the Nawa River Basin area is related to habitat connectivity due to the numerous obstructions to the waterway (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). During the development of the region for agricultural purposes, the riverbeds were straightened so that the rice fields that flank them could be made uniform in size and shape, and to facilitate their flooding for agricultural purposes. Once canalized, the rivers needed to be slowed down and rice paddies flooded so weirs and dams were added. In places, there are as many as 15 weirs within a 1 km stretch, obstructing the migration of Japanese Giant Salamanders, their access to mates, and adequate habitat for shelter, breeding and development, as well as direct impacts on their prey (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>).</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Visible anthropogenic impacts upon habitat and water quality within the Nawa River, Tottori Prefecture, Japan which could impact the survival of the Japanese Giant Salamander population within the river. Concrete weirs <bold>(A)</bold> form impassable barriers that severely restrict salamander movement compared to natural habitat <bold>(B)</bold>. The water quality in streams impacted directly by runoff <bold>(C)</bold> compared to those not <bold>(D)</bold> is starkly different.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1348251-g001.tif"/>
</fig>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Local Google Earth map of the Nawa River, Tottori Prefecture, Japan (maps.google.com), with examples waterway obstructions (dam and weirs). The numbers on the map are matching the numbers in the table where the height is indicated. The height of the obstructions is important as while <italic>Andrias</italic> sp. individuals may be able to disperse over-ground in some restricted instances, most obstructions are over a meter heigh, making it impossible to climb over it for the animals. Not all obstructions have been measured, and the ones measures are the ones numbered here. The inset picture is an adult <italic>Andrius japonicus</italic> against the weir number 8, its body pushing against the concrete weir (picture by Kenneth Chin Y. A).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1348251-g002.tif"/>
</fig>
</sec>
<sec id="s1_3">
<label>1.3</label>
<title>Risks due to pollution</title>
<p>Pollution is among the top five threat categories impacting amphibians (<xref ref-type="bibr" rid="B21">IUCN, 2023</xref>), and its impacts on populations can be critical, especially when coupled with other separate threat factors, such as habitat destruction (<xref ref-type="bibr" rid="B54">Perelman et&#xa0;al., 2021</xref>). As a result, numerous caudate species are threatened by water pollution, including the Western Chinese Mountain Salamander (<italic>Batrachuperus pinchonii</italic>) (<xref ref-type="bibr" rid="B12">Fei and Ye, 2004</xref>), the Chinese Warty Newt (<italic>Paramesotriton chinensis</italic>; <xref ref-type="bibr" rid="B16">Gu et&#xa0;al., 2004</xref>), and the Wanggao Warty Newt (<italic>Paramesotriton fuzhongensis</italic>; <xref ref-type="bibr" rid="B79">Zhao and Yuan, 2004</xref>). Pollution can have multiple origins, for example the development of land for residential, urban and agricultural use is a well-known source of pollution in the form of fine sediment which can pose major challenges to aquatic species, and have significant negative impacts on population dynamics (<xref ref-type="bibr" rid="B62">Sutherland et&#xa0;al., 2002</xref>; <xref ref-type="bibr" rid="B37">Li, 2004</xref>; <xref ref-type="bibr" rid="B80">Zhou et&#xa0;al., 2021</xref>). More specifically, activities related to cattle farming have a demonstrated negative impact on amphibian populations (<xref ref-type="bibr" rid="B59">Schmutzer et&#xa0;al., 2008</xref>) and their impact does not need to directly result in the reduction of water quality to levels deadly to amphibians as this pollution can act in synergy with other threats such as disease to have a greater negative impact on amphibians (<xref ref-type="bibr" rid="B55">Preuss et&#xa0;al., 2020</xref>).</p>
<p>The genus of Giant Salamanders (<italic>Andrias</italic> spp.), in China, is also impacted by water pollution (<xref ref-type="bibr" rid="B60">Shu et&#xa0;al., 2021</xref>). While there is little published research on the impact of pollution on Japanese Giant salamanders (<italic>A. japonicus</italic>), the ranges of the species in this genus in China have contracted in part, due to habitat loss and degradation, including water pollution and obstruction of waterways that result in changes in flow regimes and increase in turbidity along with severe overexploitation (e.g. <xref ref-type="bibr" rid="B38">Liang et&#xa0;al., 2004</xref>; <xref ref-type="bibr" rid="B75">Wang et&#xa0;al., 2004</xref>; <xref ref-type="bibr" rid="B9">Dai et&#xa0;al., 2009</xref>; <xref ref-type="bibr" rid="B69">Tapley et&#xa0;al., 2021</xref>). In addition, other pollutants yet to be investigated for the genus are expected to negatively impact the survival of individuals, for example heavy metals, phosphates, nitrates and persistent organic pollutants (<xref ref-type="bibr" rid="B9">Dai et&#xa0;al., 2009</xref>).</p>
<p>Among the threats to the Japanese Giant Salamanders in the Nawa River Basin, pollution is concerning. There is a large number of animal farms in the area that are positioned adjacent to waterways which could be potential sources for pollution from runoff. In particular, animal farms that are positioned next to small tributaries or near the sources of the rivers are of particular concern given that effluence can impact habitats much further down river (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref>).</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>Hydrological basin of the area. The Nawa River is highlighted in dark blue and the range of <italic>Andrias japonicus</italic> is indicated by the light orange shaded area on the inset map (<xref ref-type="bibr" rid="B22">IUCN and NatureServe, 2008</xref>). The area with the dam in the earlier section is highlighted as &#x201c;focal area&#x201d;. A very high number of animal farms is directly adjacent to small streams, ponds and larger rivers which could be potential sources of pollution into these streams.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1348251-g003.tif"/>
</fig>
<p>The legal and illegal discarding of animal waste in fields close to waterways can results in the waste being washed into the watercourse later on, ensuing in an increase in salinity, phosphate and nitrate, and a decrease in dissolved oxygen (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref> with sampling details here-in) that potentially impacts Japanese Giant Salamanders, despite being below the guidelines of the Ministry of Environment of the Government of Japan for waters related to the protection of the living environment (Government Ordinance No.363, 1974; <ext-link ext-link-type="uri" xlink:href="http://www.env.go.jp/en/water/wq/nes.html">www.env.go.jp/en/water/wq/nes.html</ext-link>). In the Nawa River basin, we recorded such variations at several locations, with for instance an increase in salinity, conductivity, pH, phosphate, nitrate and ammonium, and a decrease in dissolved oxygen downstream of a tributary running along a pig farm; and also an increase in nitrate and ammonium, and a decrease in dissolved oxygen downstream of a tributary running along a poultry farm, in comparison with water parameters recorded from samples taken right before the tributaries (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>). As the successful hatching of amphibians is impacted by high values in ammonia, phosphate and biological oxygen (<xref ref-type="bibr" rid="B10">De Solla et&#xa0;al., 2002</xref>), further understanding on the impact of farming on Japanese Giant Salamanders throughout all life stages is required as the levels of nutrient and chemical pollution entering the waterway from farms may be above the threshold tolerated by the focal species and numerous other aquatic species (<xref ref-type="bibr" rid="B49">Muenz et&#xa0;al., 2006</xref>), including some present in the food chain below the Japanese Giant Salamanders and therefore directly or indirectly impacting the species. In the context of Hellbenders, the loss of forest cover upstream stands out as a significant factor. This loss often leads to changes in stream habitat, including siltation and alterations in water chemistry. For instance, increased dissolved ions can elevate conductivity and salinity, which are commonly linked to declines in Hellbender populations (<xref ref-type="bibr" rid="B20">Hopkins et al., 2023</xref>).</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Water quality upstream and downstream of animal farms in the Nawa River Basin, Tottori.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="bottom" align="left"/>
<th valign="bottom" align="left">Water temp. (&#xb0;C)</th>
<th valign="bottom" align="left">pH</th>
<th valign="bottom" align="left">Cond (&#x3bc;S)</th>
<th valign="bottom" align="left">TDS (ppm)</th>
<th valign="bottom" align="left">Salinity (%)</th>
<th valign="bottom" align="left">DO (range in mg/L)</th>
<th valign="bottom" align="left">Turbidity (NTU)</th>
<th valign="bottom" align="left">Phosphate (mg/L)</th>
<th valign="bottom" align="left">Nitrates (mg/L)</th>
<th valign="bottom" align="left">Ammonium (mg/L)</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="bottom" align="left">Down-stream pig farm</td>
<td valign="bottom" align="left">22.4</td>
<td valign="bottom" align="left">8.07</td>
<td valign="bottom" align="left">385</td>
<td valign="bottom" align="left">197</td>
<td valign="bottom" align="left">0.02</td>
<td valign="bottom" align="left">2.6-2.7</td>
<td valign="bottom" align="left">61.2</td>
<td valign="bottom" align="left">2.40</td>
<td valign="bottom" align="left">0.203</td>
<td valign="bottom" align="left">6.83</td>
</tr>
<tr>
<td valign="bottom" align="left">Up-stream pig farm</td>
<td valign="bottom" align="left">22.8</td>
<td valign="bottom" align="left">7.76</td>
<td valign="bottom" align="left">126</td>
<td valign="bottom" align="left">61</td>
<td valign="bottom" align="left">0.00</td>
<td valign="bottom" align="left">4.6-5.5</td>
<td valign="bottom" align="left">4.8</td>
<td valign="bottom" align="left">0.50</td>
<td valign="bottom" align="left">0.000</td>
<td valign="bottom" align="left">3.57</td>
</tr>
<tr>
<td valign="bottom" align="left">Down-stream poultry farm</td>
<td valign="bottom" align="left">21.5</td>
<td valign="bottom" align="left">7.73</td>
<td valign="bottom" align="left">144</td>
<td valign="bottom" align="left">72</td>
<td valign="bottom" align="left">0.00</td>
<td valign="bottom" align="left">8.8-9.1</td>
<td valign="bottom" align="left">1.9</td>
<td valign="bottom" align="left">0.01</td>
<td valign="bottom" align="left">0.050</td>
<td valign="bottom" align="left">4.87</td>
</tr>
<tr>
<td valign="bottom" align="left">Up-stream poultry farm</td>
<td valign="bottom" align="left">23.9</td>
<td valign="bottom" align="left">7.73</td>
<td valign="bottom" align="left">169</td>
<td valign="bottom" align="left">82</td>
<td valign="bottom" align="left">0.00</td>
<td valign="bottom" align="left">10.9-12.5</td>
<td valign="bottom" align="left">5.1</td>
<td valign="bottom" align="left">0.12</td>
<td valign="bottom" align="left">0.010</td>
<td valign="bottom" align="left">2.25</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>Readings were taken by the authors on 22 and 23 August 2023 (point 1 and 2 respectively) at a single point between one and two meters before and after the tributary for each measurement. Cond stands for Conductivity, TDS for Total Dissolved Solids, NTU for nephelometric turbidity units and DO for Dissolved Oxygen. Water measurements taken with a Lohand LH-M900 multimetre (Hangzhou Lohand Biological Co., Ltd, China).</p>
</fn>
</table-wrap-foot>
</table-wrap>
</sec>
</sec>
<sec id="s2">
<label>2</label>
<title>Policies and practices</title>
<p>While Japanese Giant Salamanders are threatened, conservation actions can have a positive outcome, on all species in the river basin. Possible interventions include the restoration of natural breeding habitat (<xref ref-type="bibr" rid="B25">Joly and Grolet, 1996</xref>; <xref ref-type="bibr" rid="B29">Kinne, 2004</xref>), the translocation of individuals under controlled conditions (<xref ref-type="bibr" rid="B61">Smith et&#xa0;al., 2020</xref>), and the provisioning of adequate artificial breeding habitat such as nest boxes (<xref ref-type="bibr" rid="B17">Hara, 2021</xref>; <xref ref-type="bibr" rid="B63">Suzuki, 1999</xref>; <xref ref-type="bibr" rid="B33">Kuwabara et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B26">Jonas et&#xa0;al., 2020</xref>).</p>
<p>The Japanese Giant Salamander urgently requires the restoration of its habitat, and the re-establishment of connectivity across stream segments, such as through the installation of ladderways (<xref ref-type="bibr" rid="B17">Hara, 2021</xref>; <xref ref-type="bibr" rid="B67">Takahashi et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B17">Hara, 2021</xref>). Other beneficial interventions include the creation of nesting and sheltering areas, and population supplementation in some specific areas (<xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>). Examples of supplementary breeding habitats are available from the Intraregional Breeding Program in Asa Zoological Park (<xref ref-type="bibr" rid="B5">Browne et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B17">Hara, 2021</xref>), and several types of spawning areas are known to be successful for aiding reproduction in the species (<xref ref-type="bibr" rid="B70">Tochimoto, 1995</xref>, <xref ref-type="bibr" rid="B71">1996</xref>).</p>
<p>Specific to the Nawa River Basin area, and upon confirmation of the absence of invasive Chinese Giant Salamander basin through broadly sampling methods such as eDNA analyses, the implementation of bypass slopes and fish ladders for each obstruction of the river course will help alleviate their impact and restore connectivity. Such contraptions, or small structural changes to water obstructions, are likely to have near-perfect success rates based on field observations (<xref ref-type="bibr" rid="B65">Taguchi, 2009b</xref>) and experiments with prototypes (<xref ref-type="bibr" rid="B67">Takahashi et&#xa0;al., 2016</xref>). Importantly, this restoration of connectivity should be conducted for all obstructions of the waterway, as dispersion must be facilitated across all habitat types for all life stages to effectively protect the species, but also in a way that enables protection of the food chain that giant salamanders rely upon at all life stages. This habitat restoration can be supplemented by the deployment of nest boxes in suitable portions of the streams. To complement these actions, surveys should be conducted to determine the need for population supplementation, and to determine the effectiveness of any interventions as soon as possible to avoid further decline. Finally, regular monitoring of water quality, especially focused on pollution originating from farming activities, at several locations along the waterway is needed, along with the enforcement of penalties when required. Once protected, the conservation action can be boosted by the establishment of official sanctuary areas recognized as important breeding areas for the Japanese Giant Salamander. This sanctuary area will need to match with some of the critical habitat for the species, such as breeding grounds, but also areas needed to maintain connectivity between breeding and non-breeding areas. In addition, the presence of such a sanctuary will provide important data on carrying capacity of the habitat. Habitat protection, monitoring and sanctuaries may provide a base for the development of conservation projects, which may be funded through ecotourism. Ecotourism is not only a source of funding for conservation but also an opportunity to revitalize the countryside of Japan, which has experienced depopulation, and ecotourism could instead bring people back to these areas. Many local and national government policies incorporate ecotourism as a tool to tackle problems facing rural communities such as those living around the Nawa basin (<xref ref-type="bibr" rid="B57">Sakuma, 2018</xref>).</p>
</sec>
<sec id="s3" sec-type="conclusions">
<label>3</label>
<title>Conclusion</title>
<p>In conclusion, while there are known threats to Japanese Giant Salamanders, a number of important details require confirmation in the Nawa River Basin area, and these can be addresses through research. However, multiple known threats can already be alleviated with adequate conservation actions, which can be implemented by the GOs and NGOs active in the regions. In addition, citizen science monitoring such as the project set-up through iNaturalist (<ext-link ext-link-type="uri" xlink:href="https://www.inaturalist.org/projects/biodiversity-of-the-nawa-river-basin">https://www.inaturalist.org/projects/biodiversity-of-the-nawa-river-basin</ext-link>) could help provide the data needed to further understand the ecology of the species in the area. The primary risks are linked to habitat destruction and loss of connectivity, which can be re-established through appropriate bypass slopes. Once reconnected, populations can also be supplemented to preserve genetic diversity, and their survival supported by the management of the food chain, and provision of shelters. These actions should be implemented following science-based data. Finally, water quality monitoring and maintenance will facilitate continued protection of the species, a monitoring that can be conducted by GOs or NGOs. Although these recommendations are specific to the Japanese Giant Salamanders of the Nawa River Basin area, numerous aquatic species will be protected along this key umbrella species given appropriate interventions and subsequent monitoring, and guidelines can also be transferred to other landscapes.</p>
</sec>
<sec id="s4" sec-type="data-availability">
<title>Data availability statement</title>
<p>The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding authors.</p>
</sec>
<sec id="s5" sec-type="ethics-statement">
<title>Ethics statement</title>
<p>Ethical approval was not required for the study involving animals in accordance with the local legislation and institutional requirements because no animals were handled or observed for this study.</p>
</sec>
<sec id="s6" sec-type="author-contributions">
<title>Author contributions</title>
<p>AB: Conceptualization, Data curation, Funding acquisition, Investigation, Project administration, Resources, Validation, Visualization, Writing &#x2013; original draft, Writing &#x2013; review &amp; editing. AA: Conceptualization, Validation, Writing &#x2013; review &amp; editing. HM: Conceptualization, Validation, Writing &#x2013; review&#xa0;&amp;&#xa0;editing. YT: Conceptualization, Validation, Writing &#x2013; review &amp; editing. JG: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. DK: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. JA: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. SO: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. KM: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. KH: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. LW: Data curation, Investigation, Project administration, Validation, Writing &#x2013; review &amp; editing. TU: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. XZ: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. YS: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. YB: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. ZW: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. ZQ: Data curation, Investigation, Validation, Writing &#x2013; review &amp; editing. RP: Data curation, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing &#x2013; review &amp; editing.</p>
</sec>
</body>
<back>
<sec id="s7" sec-type="funding-information">
<title>Funding</title>
<p>The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.</p>
</sec>
<sec id="s8" 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="s9" 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>
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