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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.2024.1372993</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Amphibian and Reptile Science</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>
<italic>Batrachochytrium dendrobatidis</italic> and <italic>Hannemania</italic> mite&#x2019;s relationships with Mexican amphibians in disturbed environments</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" equal-contrib="yes" corresp="yes">
<name>
<surname>Jacinto-Maldonado</surname>
<given-names>M&#xf3;nica</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup>&#x2020;</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
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<contrib contrib-type="author" equal-contrib="yes">
<name>
<surname>Lesbarr&#xe8;res</surname>
<given-names>David</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup>&#x2020;</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>Rebollar</surname>
<given-names>Eria A.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>Basanta</surname>
<given-names>M. Delia</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>Gonz&#xe1;lez-Grijalva</surname>
<given-names>Belem</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>Robles-Mor&#xfa;a</surname>
<given-names>Agust&#xed;n</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
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<contrib contrib-type="author">
<name>
<surname>&#xc1;lvarez-Bajo</surname>
<given-names>Osiris</given-names>
</name>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>Vizuete-Jaramillo</surname>
<given-names>Efra&#xed;n</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
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<contrib contrib-type="author">
<name>
<surname>Paredes-Le&#xf3;n</surname>
<given-names>Ricardo</given-names>
</name>
<xref ref-type="aff" rid="aff8">
<sup>8</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>Meza-Figueroa</surname>
<given-names>Diana</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
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<aff id="aff1">
<sup>1</sup>
<institution>Departamento de Geolog&#xed;a, Universidad de Sonora</institution>, <addr-line>Hermosillo</addr-line>, <country>Mexico</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Environment and Climate Change Canada, National Wildlife Research Centre</institution>, <addr-line>Ottawa, ON</addr-line>, <country>Canada</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Centro de Ciencias Gen&#xf3;micas, Universidad Nacional Aut&#xf3;noma de M&#xe9;xico</institution>, <addr-line>Cuernavaca, Morelos</addr-line>, <country>Mexico</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Department of Biology, University of Nevada Reno</institution>, <addr-line>Reno, NV</addr-line>, <country>United States</country>
</aff>
<aff id="aff5">
<sup>5</sup>
<institution>Faculltad de Ciencias, Universidad Nacional Aut&#xf3;noma de M&#xe9;xico, Ciudad Universitaria</institution>, <addr-line>Mexico City</addr-line>, <country>Mexico</country>
</aff>
<aff id="aff6">
<sup>6</sup>
<institution>Departamento de Ciencias del Agua y Medio Ambiente, Instituto Tecnol&#xf3;gico de Sonora</institution>, <addr-line>Ciudad Obreg&#xf3;n, Sonora</addr-line>, <country>Mexico</country>
</aff>
<aff id="aff7">
<sup>7</sup>
<institution>Departamento de Investigaci&#xf3;n en F&#xed;sica, Universidad de Sonora</institution>, <addr-line>Hermosillo</addr-line>, <country>Mexico</country>
</aff>
<aff id="aff8">
<sup>8</sup>
<institution>Colecci&#xf3;n Nacional de &#xc1;caros, Instituto de Biolog&#xed;a, Universidad Nacional Aut&#xf3;noma de M&#xe9;xico</institution>, <addr-line>Mexico City</addr-line>, <country>Mexico</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Natalie Elizabeth Wildermann, King Abdullah University of Science and Technology, Saudi Arabia</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Raquel Fernanda Salla, Federal University of Sao Carlos, Brazil</p>
<p>Alain Pagano, Universit&#xe9; d&#x2019;Angers, France</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: M&#xf3;nica Jacinto-Maldonado, <email xlink:href="mailto:monica.jacinto@unison.mx">monica.jacinto@unison.mx</email>
</p>
</fn>
<fn fn-type="equal" id="fn003">
<p>&#x2020;These authors have contributed equally to this work and share first authorship</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>03</day>
<month>04</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>2</volume>
<elocation-id>1372993</elocation-id>
<history>
<date date-type="received">
<day>19</day>
<month>01</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>19</day>
<month>03</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Jacinto-Maldonado, Lesbarr&#xe8;res, Rebollar, Basanta, Gonz&#xe1;lez-Grijalva, Robles-Mor&#xfa;a, &#xc1;lvarez-Bajo, Vizuete-Jaramillo, Paredes-Le&#xf3;n and Meza-Figueroa</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Jacinto-Maldonado, Lesbarr&#xe8;res, Rebollar, Basanta, Gonz&#xe1;lez-Grijalva, Robles-Mor&#xfa;a, &#xc1;lvarez-Bajo, Vizuete-Jaramillo, Paredes-Le&#xf3;n and Meza-Figueroa</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 rapid transformation and pollution of ecosystems have severely impacted biodiversity. Specifically, anthropogenic activities have imposed adverse effects on amphibians, with evidence suggesting that these activities alter parasite and pathogen interactions within their hosts. To investigate these interactions in areas affected by different anthropogenic activities, our study focused on analyzing a pathogen and a parasite known to interact within the amphibian skin (spongy epidermis layer) and both compromising amphibian health: <italic>Batrachochytrium dendrobatidis</italic> (<italic>Bd</italic>), a fungus responsible for chytridiomycosis, a disease associated with massive population declines in amphibians and the <italic>Hannemania</italic> sp. mite in Mexico. Four sampling areas along the Sonora River were selected, representing different human activities: mining, livestock, wastewater discharge, agriculture, and one in an urban zone. We analyzed 135 amphibians across 10 anuran species. Among these, the most abundant species (<italic>Lithobates yavapaiensis</italic>) exhibited the highest prevalence of both pathogen and parasite (90.1% and 27.3%, respectively) and was significantly associated with the intensity of <italic>Bd-</italic>infection. The prevalence of <italic>Hannemania</italic> mites varied significantly across sampling sites as did <italic>Bd</italic> prevalence and infection load, with the highest <italic>Bd</italic> load found at the wastewater discharge site. A significant association between the intensity of <italic>Bd</italic>-infection and both mite abundance and amphibian species was observed when the sampling site was considered. Additionally, sites with <italic>Bd</italic>-positive individuals and <italic>Hannemania</italic> parasitism coincide with refractory elements characterized by mechanical or corrosion resistance. The persistence of these elements in the environment, along with the small particle size (&lt;850 nm) found in sediments, poses a potential risk of internalization, bioaccumulation (e.g., Fe, Co, and Ti), and their transfer through the food chain. It is thus essential to consider monitoring environmental and biotic factors that modulate the relationships between parasites, pathogens, and amphibians if we are to propose conservation strategies adapted to disturbed environments.</p>
</abstract>
<kwd-group>
<kwd>
<italic>Batrachochytrium dendrobatidis</italic>
</kwd>
<kwd>
<italic>Hannemania</italic> mites</kwd>
<kwd>amphibians</kwd>
<kwd>anthropogenic activities</kwd>
<kwd>land use change</kwd>
<kwd>pollution</kwd>
</kwd-group>
<counts>
<fig-count count="6"/>
<table-count count="2"/>
<equation-count count="0"/>
<ref-count count="81"/>
<page-count count="11"/>
<word-count count="4211"/>
</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>
<p>Anthropogenic activities have had detrimental effects on amphibians (<xref ref-type="bibr" rid="B18">Da Rocha et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B77">Yang et&#xa0;al., 2022</xref>), and there is compelling evidence that anthropogenic factors drive disease dynamics for these taxa (<xref ref-type="bibr" rid="B9">Becker et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B11">Bienentreu and Lesbarr&#xe8;res, 2020</xref>; <xref ref-type="bibr" rid="B20">De Andrade Serrano et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B35">Haver et&#xa0;al., 2022</xref>). Land use changes due to anthropogenic activities (e.g., urbanization, mining, industrialization, and agriculture) have intensified, leading to the over-exploitation, deterioration, and pollution of ecosystems (<xref ref-type="bibr" rid="B3">Archer and Stokes, 2000</xref>; <xref ref-type="bibr" rid="B65">Rashid and Romshoo, 2013</xref>; <xref ref-type="bibr" rid="B48">Kija et&#xa0;al., 2020</xref>). These anthropogenic threats have affected many species and biological processes (<xref ref-type="bibr" rid="B72">Thushari and Senevirathna, 2017</xref>; <xref ref-type="bibr" rid="B73">Ukaogo et&#xa0;al., 2020</xref>). Among vertebrates, amphibians present the greatest population decline and the greatest risk of extinction (<xref ref-type="bibr" rid="B31">Green et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B16">Button and Borz&#xe9;e, 2021</xref>). With permeable skin through which they exchange gases, pollutants, or substances, amphibians are more susceptible to changes or diseases than other vertebrate groups (<xref ref-type="bibr" rid="B47">Kaufmann and Dohmen, 2016</xref>) and are considered indicators of ecosystem health.</p>
<p>For instance, the pathogen <italic>Batrachochytrium dendrobatidis</italic> (<italic>Bd</italic>), the main causative agent of the disease chytridiomycosis, has resulted in mass mortalities among amphibians globally (<xref ref-type="bibr" rid="B27">Fisher and Garner, 2020</xref>). Additionally, the incidence of parasites like <italic>Hannemania</italic> mites has been acknowledged for their impact on amphibians, leading to deformities, loss of chemosensory function, reduced foraging capacity, diminished survival, and decreased reproduction (<xref ref-type="bibr" rid="B2">Anthony et&#xa0;al., 1994</xref>; <xref ref-type="bibr" rid="B54">Maksimowich and Mathis, 2000</xref>; <xref ref-type="bibr" rid="B44">Jacinto-Maldonado et&#xa0;al., 2016</xref>). It is recognized that anthropogenic activities, land-use changes, habitat loss, synergistic effects with pollutants (e.g., high concentrations of heavy metals), and other environmental factors (e.g., climate, altitude) may alter parasite and <italic>Bd</italic> infection dynamics, affecting occurrence rates, spread, transmission, prevalence, infection intensity of <italic>Bd</italic>, and host mortality (<xref ref-type="bibr" rid="B19">DeAlto, 2020</xref>; <xref ref-type="bibr" rid="B70">Siddons et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B21">Deknock et&#xa0;al., 2022</xref>). Both <italic>Bd</italic> and <italic>Hannemania</italic> affect amphibians by persisting and developing within the spongy epidermis layer (<xref ref-type="bibr" rid="B23">Duszynski and Jones, 1973</xref>; <xref ref-type="bibr" rid="B71">Stice and Briggs, 2010</xref>). During the larval instar of <italic>Hannemania</italic>, mites might transport toxic nanoparticles to the amphibian body (e.g., cerium oxide nanoparticles), potentially altering the parasite-host relationship and the pathogen-host dynamic, thereby increasing mortality, inducing behavioral changes, and inhibiting amphibians&#x2019; growth (<xref ref-type="bibr" rid="B43">Jacinto-Maldonado et&#xa0;al., 2022</xref>).</p>
<p>Mexico is a hotspot of diversity and endemism of amphibian species (<xref ref-type="bibr" rid="B60">Ochoa-Ochoa et&#xa0;al., 2014</xref>), and the presence of <italic>Bd</italic> and <italic>Hannemania</italic> parasites has been reported throughout the country including the Sonora state (<xref ref-type="bibr" rid="B36">Hoffmann, 1965</xref>; <xref ref-type="bibr" rid="B53">Loomis and Welbourn, 1969</xref>; <xref ref-type="bibr" rid="B30">Goldberg et&#xa0;al., 2002</xref>; <xref ref-type="bibr" rid="B6">Basanta et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B43">Jacinto-Maldonado et&#xa0;al., 2022</xref>). The Sonora state is situated at the northern edge of the country, hosting thirty-eight amphibian species (<xref ref-type="bibr" rid="B49">Lemos-Espinal et&#xa0;al., 2015</xref>, <xref ref-type="bibr" rid="B50">2019</xref>). In 2014, a spill of 40,000 m<sup>3</sup> of copper sulfate occurred in the Sonora River, and the consequences for wildlife remain unknown (<xref ref-type="bibr" rid="B51">Le&#xf3;n-Garc&#xed;a et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B57">Molina-Freaner and Mart&#xed;nez-Rodr&#xed;guez, 2022</xref>). Additionally, the Sonora River receives waste such as garbage and wastewater, alongside ongoing anthropogenic activities like livestock rearing, agriculture, and urbanization. The impacts of these activities on the presence and dynamics of pathogens and parasites in amphibians are still poorly understood. Both the fungus and the mite can potentially interact in the spongy stratum of the amphibians; however, the impact of each one may be different and this can be influenced by the biotic and abiotic variables that characterize various types of disturbance. We aimed to analyze parasite and pathogen presence in amphibians (<italic>Hannemania</italic> mites and <italic>Bd</italic>) and their potential interaction with environmental variables where different anthropogenic activities are being developed in this region. We hypothesized that the presence and infection levels of the fungal pathogen <italic>Bd</italic> and <italic>Hannemania</italic> mites will vary depending on host species, the type of disturbance and the environmental variables associated with each study area.</p>
</sec>
<sec id="s2" sec-type="materials|methods">
<label>2</label>
<title>Materials and methods</title>
<sec id="s2_1">
<label>2.1</label>
<title>Study area</title>
<p>Our sampling was carried out in March, April, and July of 2021. Five sampling sites were selected for their anthropogenic activity. Three of them were affected by the copper sulfate spill that occurred in 2014 in Sonora state, Mexico (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>): Bacanuchi (Mining site, closest to the spill site), Bacoachi (Extensive Livestock farming site, the spill did not reach this site), Aconchi (Wastewater discharge site, site affected by the spill), Ures (Agriculture site affected by the spill), and Hermosillo (Urban site, the spill did not reach this site). Sediment and water quality were analyzed at each sampling site.</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>
<bold>(A)</bold> Sonora state, Mexico. <bold>(B)</bold> Sampling sites where different anthropogenic activities are developing.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1372993-g001.tif"/>
</fig>
</sec>
<sec id="s2_2">
<label>2.2</label>
<title>Environmental samples</title>
<p>At each site, soil samples were collected in three areas (two in the flood zone and one in the river). Sediments were analyzed using a portableX-rayfluorescence (PXRF) Niton FXL analyzer (ThermoScientificInc, MA, USA) and PXRF analyses were performed according to the procedures described in US EPA Method 6200. Three measures were implemented to ensure quality control and precision of PXRF measurements (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Material 1</bold>
</xref>).</p>
<p>Water physicochemical characteristics were analyzed with a multi-parameter (Oakton PCSTestr 35 Impermeable) and the following variables were registered: pH, conductivity, total dissolved solids, and salinity (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Material 1</bold>
</xref>).</p>
</sec>
<sec id="s2_3">
<label>2.3</label>
<title>Amphibian species sampling</title>
<p>The sampling effort for each site equaled 18 person-hours. The amphibians were manually collected wearing new vinyl gloves per each individual. Each specimen was swabbed, weighed, measured, and individuals were identified to species (<xref ref-type="bibr" rid="B49">Lemos-Espinal et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B67">Rorabaugh and Lemos-Espinal, 2016</xref>). Swabs were taken following <xref ref-type="bibr" rid="B38">Hyatt et&#xa0;al. (2007)</xref> protocol, the drink path, thighs, and toes were swabbed (5 times), and then the swab was preserved in liquid nitrogen and stored at &#x2212;80&#xb0; in the laboratory. Morphological variables such as malformations, injuries, or erythema (skin reddening) were also recorded (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Material 2</bold>
</xref>). All&#xa0;individuals were released after sampling. Amphibians were collected under a scientific collector permit (SPARN/DGVS/02985/23) from the Secretar&#xed;a de Medio Ambiente y Recursos Naturales.</p>
</sec>
<sec id="s2_4">
<label>2.4</label>
<title>
<italic>Bd</italic> detection</title>
<p>DNA extraction was conducted with a Qiagen DNA extraction kit and real-time PCR was conducted as described in <xref ref-type="bibr" rid="B13">Boyle et&#xa0;al. (2004)</xref>. All samples were analyzed in duplicate. Standards of DNA synthetic fragments (gBlocks, Integrated DNA Technologies) of 1, 10, 100, and 10,000 internal transcribed spacer (ITS) <italic>Bd</italic> equivalent copies were estimated to know ITS copies of <italic>Bd</italic> in each swab. Samples were considered positive if an exponential amplification curve was generated in both replicates. When one replicate was negative, a third replicate was run to determine the infection status of the sample.</p>
</sec>
<sec id="s2_5">
<label>2.5</label>
<title>Mite detection and taxonomic identification</title>
<p>After amphibian sampling (swab, weight, identification), amphibians with mites were anesthetized using an immersion bath of isoflurane (100%) (<xref ref-type="bibr" rid="B22">Doss et&#xa0;al., 2021</xref>) before mite removal. Subsequently, the area was disinfected with an hyper-oxidase solution, and individuals remained in disinfected containers until release (max. 5 mins). No individual died during this procedure. Once removed, mites were counted and preserved in 70% and 100% ethanol. Mites were cleared with lactophenol and then mounted them with PVA medium in semi-permanent microscope slides. Using the keys by <xref ref-type="bibr" rid="B15">Brennan and Goff (1977)</xref> and <xref ref-type="bibr" rid="B37">Hoffmann (1990)</xref>, taxonomic identification was made. The mites were collected under&#xa0;a scientific collector permit (SGPA/DGVS/05384/22) from&#xa0;the&#xa0;Secretar&#xed;a de Medio Ambiente y Recursos Naturales (SEMARNAT) and were deposited at the Colecci&#xf3;n Nacional de &#xc1;caros (CNAC), Instituto de Biolog&#xed;a, Universidad Nacional Aut&#xf3;noma de M&#xe9;xico, Mexico City, Mexico.</p>
</sec>
<sec id="s2_6">
<label>2.6</label>
<title>Statistical analysis</title>
<p>The amount of sediment composition variance within and among sampling sites was determined using boxplots and a linear Discriminant Analysis (LDA) to model the environmental data (sediment composition and water quality). Five classes based on the environmental variables of each sampling site were delimitated and 20% of samples in each category were chosen to conduct a cross-validation test (<xref ref-type="bibr" rid="B4">Balakrishnama and Ganapathiraju, 1998</xref>; <xref ref-type="bibr" rid="B40">Izenman, 2013</xref>).</p>
<p>A Canonical Correspondence Analysis (CCA) was used to investigate the relationships among matrices of amphibian species, amphibians positive for <italic>Bd</italic>, and amphibians parasitized by <italic>Hannemania</italic> mites and a set of concomitant sediment and water variables. The CCA provided a direct gradient analysis of amphibian species, amphibians parasitized by <italic>Hannemania</italic> mites, and amphibians positive for <italic>Bd</italic> relative to the underlying gradients within the measured environmental variables. The derived axes are linear combinations of environmental variables so that amphibian species, amphibian species parasitized or <italic>Bd</italic> positive were directly related to these axes under the assumption of unimodal amphibian species, amphibian parasitized or <italic>Bd</italic> positive response to environmental variables. The significance of the relationships between the parameters and the canonical axes was tested by permutational multivariate analysis of variance (PermANOVA).</p>
<p>To estimate and analyze the differences in <italic>Bd</italic> and <italic>Hannemania</italic> prevalences (as the proportion of infected individuals per population with 95% confidence intervals) among sampling sites, the prop.test function was used. Additionally, a Kruskal-Wallis test was carried out to analyze the differences in <italic>Bd</italic>-infection load (log<sub>10</sub> transformation was made) among sampling sites. Both analyses were done through RStudio version 4.1.3 and in the R Stats Package (<xref ref-type="bibr" rid="B66">R Core Team, 2021</xref>; <xref ref-type="bibr" rid="B7">Basanta et al., 2022</xref>) (<ext-link ext-link-type="uri" xlink:href="http://www.R-project.org">www.R-project.org</ext-link>). Additionally, a multiple regression analysis was used to identify associations between the intensity of <italic>Bd</italic>-infection (average of ITS copies of <italic>Bd</italic> in each swab of each individual analyzed), and the sampling site, the abundance of mites, and amphibian species. All analyses were done in the statistical environment R version 4.1.3 (<ext-link ext-link-type="uri" xlink:href="http://www.R-project.org">www.R-project.org</ext-link>) using the vegan package (<xref ref-type="bibr" rid="B60">Oksanen et&#xa0;al., 2019</xref>).</p>
</sec>
</sec>
<sec id="s3" sec-type="results">
<label>3</label>
<title>Results</title>
<sec id="s3_1">
<label>3.1</label>
<title>Amphibian species found in the sampling sites</title>
<p>In total, 135 amphibians across 10 species and 7 families were sampled: <italic>Anaxyrus woodhousii, A. punctatus, Gastrophryne mazatlanensis, Lithobates magnaocularis</italic>, <italic>L. yavapaiensis, Incilius alvarius</italic>, <italic>I. mazatlanensis</italic>, <italic>Spea multiplicata, Scaphiopus couchii</italic>, and <italic>Smilisca fodiens</italic>. <italic>Scaphiopus couchii</italic> was observed in all sampling sites. <italic>L. yavapaiensis</italic> and <italic>Smilisca fodiens</italic> were present in three out of five sites with more individuals found in Aconchi. <italic>L. magnaocularis</italic> was present in three out of five sites. Four amphibian species were observed in only one sampling site: <italic>A. woodhousii, A. punctatus, I. alvarius</italic>, and <italic>S. multiplicate</italic> (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>; <xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Material 2</bold>
</xref>).</p>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Amphibian species and the number of individuals per site.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1372993-g002.tif"/>
</fig>
</sec>
<sec id="s3_2">
<label>3.2</label>
<title>
<italic>Bd</italic> prevalence and infection intensity</title>
<p>Three amphibian species were positive for <italic>Bd</italic>: <italic>L. yavapaiensis</italic>, <italic>S. couchii</italic>, and <italic>G. mazatlanensis</italic>, the former showing the highest prevalence of 90.1% among all individuals. <italic>Bd</italic> was recorded at three sites with the highest number of <italic>Bd-</italic>positive individuals observed in Aconchi where wastewater discharges were constant (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>). Three <italic>Bd-</italic>positive individuals of <italic>L. yavapaiensis Bd</italic>-positives had erythema in Aconchi while two negative individuals of <italic>Anaxyrus woodhousii</italic> had erythema in Bacoachi (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Material 2</bold>
</xref>).</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>
<italic>Bd</italic> prevalence per amphibian species at each sampling site.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" align="center">Amphibian species</th>
<th valign="middle" align="center">N</th>
<th valign="top" align="center">
<italic>Bd</italic> <break/>prevalence<break/>(%) per species</th>
<th valign="top" align="center">Bacanuchi (Mining)</th>
<th valign="top" align="center">Bacoachi<break/>(Extensive Livestock<break/>Farming)</th>
<th valign="top" align="center">Aconchi<break/>(Wastewater discharge)</th>
<th valign="top" colspan="2" align="center">Ures<break/>(Agriculture)</th>
<th valign="top" align="center">Hermosillo<break/>(Urban)</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="bottom" align="left">
<italic>A. punctatus</italic>
</td>
<td valign="bottom" align="center">2</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" colspan="2" align="center">0</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>A. woodhousii</italic>
</td>
<td valign="bottom" align="center">2</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" colspan="2" align="center">0</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>G. mazatlanensis</italic>
</td>
<td valign="bottom" align="center">13</td>
<td valign="bottom" align="center">7.69</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">11 (1 +) 9.09%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" colspan="2" align="center">2 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>I. alvarius</italic>
</td>
<td valign="bottom" align="center">2</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" colspan="2" align="center">0</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>I. mazatlanensis</italic>
</td>
<td valign="bottom" align="center">17</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">8 (0 +) 0%</td>
<td valign="bottom" colspan="2" align="center">9 (0+) 0%</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>L. magnaocularis</italic>
</td>
<td valign="bottom" align="center">14</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">1 (0 +) 0%</td>
<td valign="bottom" align="center">1 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" colspan="2" align="center">0</td>
<td valign="bottom" align="center">12 (0+) 0%</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>L. yavapaiensis</italic>
</td>
<td valign="bottom" align="center">22</td>
<td valign="bottom" align="center">90.91</td>
<td valign="bottom" align="center">1 (0 +) 0%</td>
<td valign="bottom" align="center">6 (6 +) 100%</td>
<td valign="bottom" align="center">15 (14 +) 93.33%</td>
<td valign="bottom" colspan="2" align="center">0</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>S. couchii</italic>
</td>
<td valign="bottom" align="center">47</td>
<td valign="bottom" align="center">4.26</td>
<td valign="bottom" align="center">23 (2 +) 8.70%</td>
<td valign="bottom" align="center">5 (0 +) 0%</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
<td valign="bottom" colspan="2" align="center">12 (0 +) 0%</td>
<td valign="bottom" align="center">5 (0 +) 0%</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>S. fodiens</italic>
</td>
<td valign="bottom" align="center">15</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">6 (0 +) 0%</td>
<td valign="bottom" colspan="2" align="center">5 (0 +) 0%</td>
<td valign="bottom" align="center">4 (0 +) 0%</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>S. multiplicata</italic>
</td>
<td valign="bottom" align="center">1</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">1 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" colspan="2" align="center">0</td>
<td valign="bottom" align="center">0</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>Bd prevalence of each amphibian species is expressed as the number of hosts Bd-positive divided by the number of hosts examined. N = number of individuals analyzed for Bd, (<bold>+</bold>) the number of Bd-positive amphibians, <bold>%</bold>. prevalence in percentage.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<p>The prevalence of <italic>Bd</italic> among sampling sites was significantly different (X<sup>2</sup> = 30.937, df = 4, p-value = 3.154e-06) as was <italic>Bd</italic>-infection load (Kruskal-Wallis X<sup>2</sup> = 9.867, df = 2, p-value = 0.007). A higher number of individuals with high <italic>Bd</italic>-infection load were observed in Aconchi and Bacoachi. At Aconchi 75% of individuals had a higher <italic>Bd</italic>-infection load range as compared to Bacoachi where just a few individuals showed a high <italic>Bd</italic>-infection load. No infected individuals were observed at Ures and Hermosillo and only 2 individuals were <italic>Bd</italic>-positive at Bacanuchi (<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>
<italic>Bd</italic>-infection load (number of ITS copies of <italic>Bd</italic>) among sampling sites.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1372993-g003.tif"/>
</fig>
</sec>
<sec id="s3_3">
<label>3.3</label>
<title>
<italic>Hannemania</italic> mites&#x2019; presence and prevalence</title>
<p>Three amphibian species were positive for <italic>Hannemania</italic> mites: <italic>L. yavapaiensis</italic>, <italic>S. couchii</italic>, and <italic>S. fodiens</italic> with the former having the highest prevalence (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). The prevalence of <italic>Hannemania</italic> mites was different among sampling sites (X<sup>2</sup> = 16.682, df = 4, p = 0.002) with the highest prevalence at Bacoachi (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>).</p>
<table-wrap id="T2" position="float">
<label>Table&#xa0;2</label>
<caption>
<p>
<italic>Hannemania</italic> mites&#x2019; prevalence per amphibian species at each sampling site.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" align="center">Amphibian species</th>
<th valign="middle" align="center">N</th>
<th valign="middle" align="center">
<italic>Hannemania</italic> prevalence<break/>% per species</th>
<th valign="bottom" align="center">Bacanuchi<break/>(Mining)</th>
<th valign="bottom" align="center">Bacoachi<break/>(Extensive Livestock Farming)</th>
<th valign="bottom" align="center">Aconchi<break/>(Wastewater discharge)</th>
<th valign="bottom" align="center">Ures<break/>(Agriculture)</th>
<th valign="bottom" align="center">Hermosillo<break/>(Urban)</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="bottom" align="left">
<italic>A. punctatus</italic>
</td>
<td valign="bottom" align="center">2</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>A. woodhousii</italic>
</td>
<td valign="bottom" align="center">2</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>G. mazatlanensis</italic>
</td>
<td valign="bottom" align="center">13</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">11 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>I. alvarius</italic>
</td>
<td valign="bottom" align="center">2</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>I. mazatlanensis</italic>
</td>
<td valign="bottom" align="center">17</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">8 (0 +) 0%</td>
<td valign="bottom" align="center">9 (0+) 0%</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>L. magnaocularis</italic>
</td>
<td valign="bottom" align="center">14</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">1 (0 +) 0%</td>
<td valign="bottom" align="center">1 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">12 (0+) 0%</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>L. yavapaiensis</italic>
</td>
<td valign="bottom" align="center">22</td>
<td valign="bottom" align="center">27.27</td>
<td valign="bottom" align="center">1 (1 +) 100%</td>
<td valign="bottom" align="center">6 (5 +) 83.33%</td>
<td valign="bottom" align="center">15 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>S. couchii</italic>
</td>
<td valign="bottom" align="center">47</td>
<td valign="bottom" align="center">2.13</td>
<td valign="bottom" align="center">23 (0 +) 0%</td>
<td valign="bottom" align="center">5 (1 +) 20%</td>
<td valign="bottom" align="center">2 (0 +) 0%</td>
<td valign="bottom" align="center">12 (0 +) 0%</td>
<td valign="bottom" align="center">5 (0 +) 0%</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>S. fodiens</italic>
</td>
<td valign="bottom" align="center">15</td>
<td valign="bottom" align="center">6.67</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">6 (1 +) 16.67%</td>
<td valign="bottom" align="center">5 (0 +) 0%</td>
<td valign="bottom" align="center">4 (0 +) 0%</td>
</tr>
<tr>
<td valign="bottom" align="left">
<italic>S. multiplicata</italic>
</td>
<td valign="bottom" align="center">1</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">1 (0 +) 0%</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
<td valign="bottom" align="center">0</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>Hannemania prevalence of each amphibian species is expressed as the number of hosts infected with one or more individuals of Hannemania mites divided by the number of hosts examined. N = number of individuals analyzed for mites, (<bold>+</bold>) the number of positive individuals.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</sec>
<sec id="s3_4">
<label>3.4</label>
<title>Environmental variation</title>
<p>Bacanuchi and Aconchi showed the lowest water quality levels (higher conductivity values, salinity, and total dissolved solids). Additionally, the lowest pH value (&lt;6.5) was recorded in Aconchi while the highest value was found in Ures (&gt;8; <xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>). There were also differences among sampling sites in sediment composition. Except for a few outliers, Sr, Cu, As, Zn, Mn, Sb, and Ca had the highest values in Bacanuchi (mining area). The highest concentrations of Cl, Rb, Fe, K, Nb, Y, Co, and Ti were found in Bacoachi (livestock area). In Aconchi (wastewater discharge area), V and Pb had the highest concentrations. By contrast, all elements showed low values In Ures as compared to other sites (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>).</p>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>Water quality and sediment samples at each sampling site.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1372993-g004.tif"/>
</fig>
<p>The LDA indicated a good fit of the data (accuracy, sensitivity, and specificity); 96% (n= 169) of all our environmental data analyzed (n= 176) were classified correctly in one of the five classes based on the environmental variables of each sampling site. Bacanuchi and Bacoachi were well segregated (sampling sites with less environmental similarities) while Hermosillo, Ures, and Aconchi showed some overlap (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5</bold>
</xref>).</p>
<fig id="f5" position="float">
<label>Figure&#xa0;5</label>
<caption>
<p>Linear Discriminant Analysis (LDA) of environmental variables at sampling sites. LDA1 = 39.5% and LDA2 = 26.4%.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1372993-g005.tif"/>
</fig>
</sec>
<sec id="s3_5">
<label>3.5</label>
<title>Interaction among the intensity of <italic>Bd</italic>-infection versus the abundance of mites, the amphibian species, and the sampling site</title>
<p>While sampling site was not a significant predictor of <italic>Bd</italic>-intensity (r<sup>2</sup> = 0.06, p = 0.99, df = 4), we found a significant interaction between <italic>Bd</italic>-infection and the abundance of mites (r<sup>2</sup> = 2.63, p = 0.03, df = 4), and the amphibian species (r<sup>2</sup> = 21.64, p = 0.01, df = 3) with our model explaining 63.71% of the variation in the multiple regression analysis. In particular, the intensity of <italic>Bd</italic>-infection was associated with the presence of <italic>L. yavapaiensis</italic> (p = 0.01).</p>
</sec>
<sec id="s3_6">
<label>3.6</label>
<title>Association of <italic>Bd</italic> and <italic>Hannemania</italic> mites with environmental variables</title>
<p>Both axes of the CCA explained 65.9% of the variance of environmental variables recorded in sediments and water (26.4% and 39.5% for axes 1 and 2 respectively). Environmental variables had significant effects on amphibian species, amphibians <italic>Bd</italic>-positive, and amphibians parasitized by <italic>Hannemania</italic> mites (all p &lt; 0.05). In particular, both <italic>Bd</italic>-positive and <italic>Hannemania</italic>-parasitized amphibians were associated with two sampling sites (Bacoachi and Aconchi), the distribution of four amphibian species (<italic>L. yavapaiensis</italic>, <italic>G. mazatlanensis</italic>, <italic>A. woodhousii</italic>, and <italic>A. punctatus</italic>) and the signature of Ti, V, Y, Nb, Zr, Rb, Fe and Co (<xref ref-type="fig" rid="f6">
<bold>Figure&#xa0;6</bold>
</xref>).</p>
<fig id="f6" position="float">
<label>Figure&#xa0;6</label>
<caption>
<p>Canonical correspondence analysis of the variance of biotic variables (amphibian species, amphibians <italic>Bd</italic>-positive, and amphibians parasitized by <italic>Hannemania</italic> mites) due to environmental variables recorded in sediments and water. Sediments and water quality variables are in black, sampling site names are in color, and amphibian species are in blue. Amphibians positive for <italic>Bd</italic> and parasitized by <italic>Hannemania</italic> mites are in bold letters.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="famrs-02-1372993-g006.tif"/>
</fig>
</sec>
</sec>
<sec id="s4" sec-type="discussion">
<label>4</label>
<title>Discussion</title>
<p>To our knowledge, this is the first investigation of the presence and interaction of the fungal pathogen <italic>Bd</italic> and the <italic>Hannemania</italic> mites in disturbed environments in amphibians. Among sites with different types of perturbation, our results suggest that the prevalence of <italic>Bd</italic> and H<italic>annemania</italic> mites were associated with the presence of four amphibian species and coincided with refractory elements characterized by mechanical or corrosion resistance. Moreover, we observed a positive association between the intensity of <italic>Bd</italic>-infection and the abundance of <italic>Hannemania</italic> mites in <italic>L. yavapaiensis</italic>. Such co-infection highlights the importance of monitoring environmental and biotic factors that modulate the relationship between parasites, pathogens, and hosts&#xa0;in transformed and polluted environments for future conservation strategies.</p>
<p>Aconchi exhibited the highest <italic>Bd</italic> infection load, coinciding with the presence of wastewater discharge at that site, aligning with previous studies that highlighted the association between low water quality or water pollution, particularly wastewater discharges, and <italic>Bd</italic> presence, prevalence, and infection load (<xref ref-type="bibr" rid="B8">Battaglin et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B17">Congram et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B42">Jacinto-Maldonado et&#xa0;al., 2023</xref>). By contrast, <xref ref-type="bibr" rid="B32">Hale et&#xa0;al. (2005)</xref> did not detect <italic>Bd</italic> in specimens collected in Aconchi in 2000, suggesting that <italic>Bd</italic> arrived recently or that changes in environmental conditions, such as water pollution, might have influenced the presence and <italic>Bd</italic> infection load in the region. Moreover, <italic>L. yavapaiensis</italic> showed the highest intensity of infection of <italic>Bd</italic> among amphibian species, with 23.08% of positive individuals showing erythema. The lowland leopard frog is listed as special protection with a declining population (<xref ref-type="bibr" rid="B59">NOM-059-SEMARNAT, 2010</xref>; <xref ref-type="bibr" rid="B39">IUCN, 2023</xref>) and further investigation should test the hypothesis that <italic>L. yavapaiensis</italic> acts as a reservoir or carrier of <italic>Bd</italic> in these sites and a potential threat to other susceptible amphibians (<xref ref-type="bibr" rid="B56">Miaud et&#xa0;al., 2016</xref>).</p>
<p>Among all species, <italic>Bd</italic> was also observed in <italic>G. mazatlanensis</italic> and <italic>S. couchii</italic> for the first time. In Sonora state, <italic>Bd</italic> has been previously reported in seven amphibian species (<italic>L. yavapaiensis, L. magnaocularis; Leptodactylus melanonotus; Agalychnis dacnicolor; Lithobates tarahumarae; Smilisca fodiens; Lithobates pustulosa</italic>) based on museum (<xref ref-type="bibr" rid="B32">Hale et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B6">Basanta et&#xa0;al., 2021</xref>) and live specimens from the Northern Jaguar Reserve and the locality of Tesopaco (<xref ref-type="bibr" rid="B78">Zamora-B&#xe1;rcenas et&#xa0;al., 2012</xref>). Previous reports also indicated the presence of <italic>Bd</italic> in <italic>L. yavapaiensis</italic> in nearby Arizona, United States. While we observed a prevalence of 90.1% in this species, other studies reported higher (93%) and lower (43% and 1.6%) prevalences in Sonora (<xref ref-type="bibr" rid="B69">Schlaepfer et&#xa0;al., 2007</xref>; <xref ref-type="bibr" rid="B68">Savage et&#xa0;al., 2011</xref>). In addition, there are studies of <italic>L. yavapaiensis</italic> in Sonora with no information on prevalence (<xref ref-type="bibr" rid="B14">Bradley et&#xa0;al., 2002</xref>; <xref ref-type="bibr" rid="B32">Hale et&#xa0;al., 2005</xref>). Variations in prevalence, susceptibility, and vulnerability of amphibians to <italic>Bd</italic> infection could be linked to skin microbiome richness and composition, host life-history traits, phylogeny, morphology, physiology, gene expression, immune response, and resistance (<xref ref-type="bibr" rid="B62">Ortiz-Santaliestra et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B24">Eskew et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B74">Varela et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B79">Zamudio et&#xa0;al., 2020</xref>). Yet&#xa0;chytridiomycosis-related symptoms were only observed in three <italic>Bd-</italic>positive lowland leopard frogs (erythema in the ventral region) so more fieldwork, and experimental studies are imperative to better understand infection in this species.</p>
<p>The lowland leopard frog also showed the highest prevalence of <italic>Hannemania</italic> mites (27.27%), followed by <italic>S. fodiens</italic> (6.67%) and <italic>S. couchii</italic> (2.13%). The susceptibility of amphibians to <italic>Hannemania</italic> mites and their infestation rates have been associated with host size, behavior, microhabitat use, sex, the exposure time to the chiggers as well as environmental variables such as high humidity, high air temperature, proximity to water bodies, neutral and alkaline-pH water and areas with low canopy cover (<xref ref-type="bibr" rid="B64">Rankin, 1937</xref>; <xref ref-type="bibr" rid="B45">Jung et&#xa0;al., 2001</xref>; <xref ref-type="bibr" rid="B76">Wohltmann et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B34">Hatano et&#xa0;al., 2007</xref>; <xref ref-type="bibr" rid="B1">Alvarado-Rybak et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B41">Jacinto-Maldonado et&#xa0;al., 2020</xref>). Previous studies reported a higher prevalence of mites in <italic>L. yavapaiensis</italic> in the area (71.42%; <xref ref-type="bibr" rid="B43">Jacinto-Maldonado et&#xa0;al., 2022</xref>) suggesting interannual variation associated with environmental factors such as precipitation or temperature. This species was also the only amphibian species coinfected with <italic>Bd</italic> and <italic>Hannemania</italic> mites, and the only species with a significant relationship with the intensity of <italic>Bd</italic>-infection, suggesting a possible association between parasite-pathogen in this amphibian species. For instance, <italic>Hannemania</italic> mites might more readily infiltrate the stratum corneum and granulosum of the skin of <italic>Bd</italic>-positive amphibians due to skin damage, shedding, or ulcerations (<xref ref-type="bibr" rid="B63">Pessier, 2002</xref>; <xref ref-type="bibr" rid="B10">Berger et&#xa0;al., 2005</xref>). We also present the first report of <italic>Hannemania</italic> mites in <italic>S. fodiens. S. couchii</italic> has been recorded as the host of <italic>Hannemania hylae</italic> in Alamos, Sonora in 1943, but no information about its prevalence is available (<xref ref-type="bibr" rid="B37">Hoffmann, 1990</xref>). Among sites, Bacoachi presented the highest <italic>Hannemania</italic> prevalence, a cause for concern due to prior studies reporting toxic particles in sediments in this area. <italic>Hannemania</italic> mites have been identified as vectors of CeO<sub>2</sub> and TiO<sub>2</sub> particles (<xref ref-type="bibr" rid="B43">Jacinto-Maldonado et&#xa0;al., 2022</xref>). In amphibians, CeO<sub>2</sub> particles can result in high mortality, growth inhibition, and genotoxic effects, while TiO<sub>2</sub> particles may induce hormone disruption (thyroxine and triiodothyronine), cellular stress, decreased survival, altered growth, and cellular metabolism, as well as tissue damage (<xref ref-type="bibr" rid="B81">Zhang, 2011</xref>; <xref ref-type="bibr" rid="B80">Zhang et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B33">Hammond et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B12">Bour et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B29">Galdiero et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B75">Vijayaraj et&#xa0;al., 2018</xref>).</p>
<p>Our results also highlight that sites with a high prevalence of <italic>Bd</italic> or <italic>Hannemania</italic> mites, exhibit elevated levels of Fe, Ti, Co, Zr, V, Rb, Y, and Nb in sediments, particularly if <italic>L. yavapaiensis</italic>, <italic>G. mazatlanensis</italic>, <italic>A. woodhousii</italic>, and <italic>A. punctatus</italic> are present at these sites. These aforementioned elements, characterized as refractory elements renowned for their mechanical or corrosion resistance, find application in various sectors like alloys, ceramics, paints, and coatings (<xref ref-type="bibr" rid="B5">Balazic et&#xa0;al., 2007</xref>; <xref ref-type="bibr" rid="B52">Lodhi et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B46">Karimzadeh et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B55">Meza-Figueroa et&#xa0;al., 2020</xref>). Their extended persistence in the environment and the observed particle size (e.g. &lt;850 nm) increase the risk of internalization, bioaccumulation (e.g. Fe, Co, and Ti), and potential transfer through the food chain, thus impacting aquatic and terrestrial ecosystems, thereby necessitating a more detailed analysis of particles (e.g. chemical composition, charge, surface structure, aerodynamic size, morphology) as well as periodic studies in these areas (<xref ref-type="bibr" rid="B28">G&#xe1;l et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B26">Fabrega et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B33">Hammond et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B43">Jacinto-Maldonado et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B25">Esteves-Aguilar et&#xa0;al., 2023</xref>). With 38 amphibian species reported in Sonora and 21 amphibian species, including six endemics and three under special protection in Aconchi and Bacoachi, the impact of pollution and its association with the disease should be considered (<xref ref-type="bibr" rid="B59">NOM-059-SEMARNAT, 2010</xref>; <xref ref-type="bibr" rid="B50">Lemos-Espinal et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B39">IUCN, 2023</xref>; <xref ref-type="bibr" rid="B58">Naturalista, 2023</xref>).</p>
<p>Anthropogenic activities negatively impact and put at risk ecosystems and the species that live in them. Given the richness of amphibian diversity and the impact of anthropogenic activities in Sonora state and specifically in our study sites, continuous monitoring of environmental conditions, particularly water and sediment pollution should be pursued to understand better parasite-pathogen coinfections as well as better protect amphibian diversity.</p>
</sec>
<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 authors.</p>
</sec>
<sec id="s6" sec-type="ethics-statement">
<title>Ethics statement</title>
<p>The animal study was approved by Secretar&#xed;a de Medio Ambiente y Recursos Naturales. The study was conducted in accordance with the local legislation and institutional requirements.</p>
</sec>
<sec id="s7" sec-type="author-contributions">
<title>Author contributions</title>
<p>MJ-M: Conceptualization, Formal analysis, Investigation, Methodology, Writing &#x2013; original draft, Writing &#x2013; review &amp; editing. DL: Conceptualization, Investigation, Resources, Writing &#x2013; review &amp; editing. ER: Data curation, Formal analysis, Methodology, Writing &#x2013; review &amp; editing, Resources. MB: Conceptualization, Methodology, Resources, Writing &#x2013; review &amp; editing. BG-G: Data curation, Formal analysis, Resources, Writing &#x2013; review &amp; editing. AR-M: Formal analysis, Methodology, Resources, Writing &#x2013; review &amp; editing, Data curation. O&#xc1;-B: Formal analysis, Methodology, Writing &#x2013; review &amp; editing. EV-J: Methodology, Writing &#x2013; review &amp; editing, Data curation, Investigation. RP-L: Writing &#x2013; review &amp; editing. DM-F: Conceptualization, Funding acquisition, Investigation, Project administration, Resources, Supervision, Writing &#x2013; review &amp; editing.</p>
</sec>
</body>
<back>
<sec id="s8" sec-type="funding-information">
<title>Funding</title>
<p>The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was funded by the National Council for Science and Technology in Mexico (CONAHCYT) Grant 309959 PRONACES and Grant A1-S-29697 to DM-F and a postdoctoral scholarship to MJ-M I1200/320/2022.</p>
</sec>
<ack>
<title>Acknowledgments</title>
<p>We gratefully acknowledge Miguel Ernesto Rosas Morales, Lourdes Gabriela Canizalez Ju&#xe1;rez, and Iv&#xe1;n Guillermo Souffle Lamphar from the Herpetology Club at the University of Sonora for field assistance and discussions. We also thank Alberto H. Orta and Griselda Montiel Parra for their valuable comments and technical support.</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>
<p>The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.</p>
</sec>
<sec id="s10" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
<sec id="s11" 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/famrs.2024.1372993/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/famrs.2024.1372993/full#supplementary-material</ext-link>
</p>
<supplementary-material xlink:href="Table_1.xlsx" id="SM1" mimetype="application/vnd.openxmlformats-officedocument.spreadsheetml.sheet"/>
<supplementary-material xlink:href="Table_2.xlsx" id="SM2" mimetype="application/vnd.openxmlformats-officedocument.spreadsheetml.sheet"/>
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