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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Ecol. Evol.</journal-id>
<journal-title>Frontiers in Ecology and Evolution</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Ecol. Evol.</abbrev-journal-title>
<issn pub-type="epub">2296-701X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fevo.2024.1336747</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Ecology and Evolution</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Framework for multi-stressor physiological response evaluation in amphibian risk assessment and conservation</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Awkerman</surname>
<given-names>Jill A.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1996714"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Glinski</surname>
<given-names>Donna A.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Henderson</surname>
<given-names>W. Matthew</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Meter</surname>
<given-names>Robin Van </given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Purucker</surname>
<given-names>S. Thomas</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Center for Ecosystem Measurement and Modeling, Office of Research and Development, US Environmental Protection Agency</institution>, <addr-line>Gulf Breeze, FL</addr-line>, <country>United States</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Center for Ecosystem Measurement and Modeling, Office of Research and Development, US Environmental Protection Agency</institution>, <addr-line>Athens, GA</addr-line>, <country>United States</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Environmental Science and Studies, Washington College</institution>, <addr-line>Chestertown, MD</addr-line>, <country>United States</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Center for Computational Toxicology and Exposure, Office of Research and Development, US Environmental Protection Agency</institution>, <addr-line>Durham, NC</addr-line>, <country>United States</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Mary Ann Ottinger, University of Houston, United States</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Paula Henry, Patuxent Wildlife Research Center (USGS), United States</p>
<p>Caitlin R. Gabor, Texas State University, United States</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Jill A. Awkerman, <email xlink:href="mailto:awkerman.jill@epa.gov">awkerman.jill@epa.gov</email>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>13</day>
<month>03</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>12</volume>
<elocation-id>1336747</elocation-id>
<history>
<date date-type="received">
<day>11</day>
<month>11</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>26</day>
<month>02</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Awkerman, Glinski, Henderson, Meter and Purucker</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Awkerman, Glinski, Henderson, Meter and Purucker</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>Controlled laboratory experiments are often performed on amphibians to establish causality between stressor presence and an adverse outcome. However, in the field, identification of lab-generated biomarkers from single stressors and the interactions of multiple impacts are difficult to discern in an ecological context. The ubiquity of some pesticides and anthropogenic contaminants results in potentially cryptic sublethal effects or synergistic effects among multiple stressors. Although biochemical pathways regulating physiological responses to toxic stressors are often well-conserved among vertebrates, different exposure regimes and life stage vulnerabilities can yield variable ecological risk among species. Here we examine stress-related biomarkers, highlight endpoints commonly linked to apical effects, and discuss differences in ontogeny and ecology that could limit interpretation of biomarkers across species. Further we identify promising field-based physiological measures indicative of potential impacts to health and development of amphibians that could be useful to anuran conservation. We outline the physiological responses to common stressors in the context of altered functional pathways, presenting useful stage-specific endpoints for anuran species, and discussing multi-stressor vulnerability in the larger framework of amphibian life history and ecology. This overview identifies points of physiological, ecological, and demographic vulnerability to provide context in evaluating the multiple stressors impacting amphibian populations worldwide for strategic conservation planning.</p>
</abstract>
<kwd-group>
<kwd>amphibian</kwd>
<kwd>conservation</kwd>
<kwd>risk assessment</kwd>
<kwd>stressor</kwd>
<kwd>physiology</kwd>
</kwd-group>
<counts>
<fig-count count="2"/>
<table-count count="1"/>
<equation-count count="0"/>
<ref-count count="183"/>
<page-count count="16"/>
<word-count count="8294"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Ecophysiology</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1">
<label>1</label>
<title>Stressors</title>
<p>Multiple common sources of physiological stress contribute to the ubiquitous threats to amphibian populations worldwide, including disease, pollution, and habitat loss as well as combinations of these stressors (<xref ref-type="bibr" rid="B154">Stuart et&#xa0;al., 2004</xref>; <xref ref-type="bibr" rid="B172">Wake and Vredenburg, 2008</xref>; <xref ref-type="bibr" rid="B42">Foden et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B52">Grant et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B53">Green et&#xa0;al., 2020</xref>). Stressor impacts can be detected at the organismal level before long-term population decline is apparent. Habitat constraints are frequently observed as higher density resource competition inhibiting metamorphosis, recruitment, or reproductive success in some species (<xref ref-type="bibr" rid="B59">Harper and Semlitsch, 2007</xref>; <xref ref-type="bibr" rid="B123">Rittenhouse and Semlitsch, 2007</xref>). Disease transmission often presents as an immunological response prior to mass mortality (<xref ref-type="bibr" rid="B109">Ohmer et&#xa0;al., 2021</xref>). Pollution, likewise, can result in reduced reproductive success or growth in addition to mortality, and the chronic effects of these stressors can often be detected as systemic responses within the organism that precede impacts apparent at the population level (<xref ref-type="bibr" rid="B157">Thambirajah et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B162">Trudeau et&#xa0;al., 2020</xref>). Oxidative stress, compromised immunity, endocrine disruption, and altered metabolic activity are some physiological indications of perturbations in biological function that can lead to phenotypical impacts on individual fitness, with implications for population dynamics.</p>
<sec id="s1_1">
<label>1.1</label>
<title>Habitat degradation</title>
<p>Habitat conversion, degradation, and fragmentation are the primary global causes of terrestrial biodiversity loss (<xref ref-type="bibr" rid="B56">Haddad et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B106">Newbold et&#xa0;al., 2015</xref>). Though global amphibian declines are linked to multiple stressors and their interactions, habitat loss typically plays an outsized role due to impacts on survival, gene flow, and dispersal (<xref ref-type="bibr" rid="B150">Sodhi et&#xa0;al., 2008</xref>). Spatial range, dispersal rates, or seasonal constraints influence population connectivity, and the abiotic conditions limiting habitat availability are projected to be less favorable in response to climate change (<xref ref-type="bibr" rid="B150">Sodhi et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B47">Funk et&#xa0;al., 2021</xref>). Warmer and drier conditions produced from changing climatic trends provide a direct thermal stressor and are expected to accelerate habitat loss of ephemeral wetlands (<xref ref-type="bibr" rid="B13">Blaustein et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B83">Lertzman-Lepofsky et&#xa0;al., 2020</xref>). Thermal stressors can geographically constrain or shift suitable aquatic (<xref ref-type="bibr" rid="B35">Duarte et&#xa0;al., 2012</xref>) and terrestrial (<xref ref-type="bibr" rid="B62">Hoffmann et&#xa0;al., 2021</xref>) ranges, particularly for cold-adapted species and microclimate-dependent life history stages with limited acclimation capacity (<xref ref-type="bibr" rid="B46">Frishkoff et&#xa0;al., 2015</xref>).</p>
<p>Sources of anthropogenic modifications linked to amphibian habitat loss are driven by deforestation and urbanization (<xref ref-type="bibr" rid="B29">Cordier et&#xa0;al., 2021</xref>). Continued fragmentation of amphibian populations based on their hydroregime dependency has demonstrated that periods of drought effectively isolate numerous endangered species (<xref ref-type="bibr" rid="B180">Zamberletti et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B2">Allen et&#xa0;al., 2020</xref>). Further, conservation of breeding wetlands is insufficient to overcome the challenges presented by anthropogenically or climatically modified habitats (<xref ref-type="bibr" rid="B2">Allen et&#xa0;al., 2020</xref>), particularly the anticipated reduction in temporary wetland inundation (<xref ref-type="bibr" rid="B18">Brice et&#xa0;al., 2022</xref>). Additionally, wetland protection depends on legal decisions that are subject to amendment or revision. Even with ample habitat available, environmental stochasticity increases variance in juvenile recruitment for species dependent on ephemeral wetlands (<xref ref-type="bibr" rid="B54">Greenberg et&#xa0;al., 2017</xref>), particularly for species with high dispersal rates and/or an energetically costly metamorphosis (<xref ref-type="bibr" rid="B47">Funk et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B19">Brooks and Kindsvater, 2022</xref>). Hydroperiod duration could have a greater impact on metapopulation persistence than pathogen or contaminant exposure (<xref ref-type="bibr" rid="B147">Smalling et&#xa0;al., 2019</xref>), specifically anomalous deluge events or multiple years of drought (<xref ref-type="bibr" rid="B173">Walls et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B4">Awkerman and Greenberg, 2022</xref>; cf. <xref ref-type="bibr" rid="B100">Moss et&#xa0;al., 2021</xref>).</p>
</sec>
<sec id="s1_2">
<label>1.2</label>
<title>Pathogens</title>
<p>In addition to the limitations of habitat availability, amphibian populations are also regulated by disease and predation. Many species require fish-free breeding ponds for sufficient reproductive success and are vulnerable to predation by aquatic insects (<xref ref-type="bibr" rid="B108">Ohba, 2011</xref>). Anuran species and life stages vary in inherent susceptibility and ecological likelihood of exposure to waterborne pathogens such as ranaviruses and <italic>Batrachochytrium dendrobatidis</italic> (<italic>Bd</italic>) (<xref ref-type="bibr" rid="B57">Haislip et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B65">Hoverman et&#xa0;al., 2011</xref>). <italic>Bd</italic>, the fungus responsible for chytridiomycosis, is found in cooler, lentic waterbodies (<xref ref-type="bibr" rid="B151">Spitzen-van der Sluijs et&#xa0;al., 2017</xref>), and prevalence is often highest among amphibian larvae, with later life stages more resistant to infection (<xref ref-type="bibr" rid="B86">Li et&#xa0;al., 2021</xref>). Amphibian response to chytridiomycosis often involves the complement system, in an immunological response to the pathogen, and is frequently detected through bacteria-killing assays (BKA; <xref ref-type="bibr" rid="B125">Rodriguez and Voyles, 2020</xref>). Ranavirus is often detected in amphibian communities with greater species diversity (<xref ref-type="bibr" rid="B11">Bienentreu et&#xa0;al., 2022</xref>). Pathogen effects can be exacerbated by transmission via more resilient invasive species that spread disease in addition to competing for the diminishing habitat of native species. For example, the American bullfrog (<italic>Lithobates catesbeianus</italic>) is a particularly invasive species that is less susceptible to ranavirus and chytridiomycosis-induced lethality, and therefore acts as an influential vector facilitating world-wide transmission of ranavirus (<xref ref-type="bibr" rid="B63">Hossack et&#xa0;al., 2023</xref>). The global trade and subsequent farming of this species for human consumption have resulted in the detection of ranavirus in native populations from previously uncontaminated regions such as those of Brazil and Mexico (<xref ref-type="bibr" rid="B132">Ruggeri et&#xa0;al., 2019</xref> and <xref ref-type="bibr" rid="B141">Saucedo et&#xa0;al., 2019</xref>, respectively). International trade of the invasive <italic>Xenopus laevis</italic> has also contributed to the spread of chytridiomycosis (<xref ref-type="bibr" rid="B41">Fisher and Garner, 2020</xref>).</p>
<p>Amphibian species differ in their response to the fungal pathogen <italic>Bd</italic> with some species showing downregulation of cellular and metabolic functions and upregulation of adaptive immune gene response; however, such responses are ultimately insufficient to prevent high microbial infection loads (e.g., <xref ref-type="bibr" rid="B39">Eskew et&#xa0;al., 2018</xref>). Other species with more diverse dermal antimicrobial peptide communities showed minimal response to infection (<xref ref-type="bibr" rid="B39">Eskew et&#xa0;al., 2018</xref>). Lower temperatures may increase inflammation-related responses as opposed to warmer temperatures increasing adaptive immune responses (<xref ref-type="bibr" rid="B38">Ellison et&#xa0;al., 2020</xref>). More bacterial reads, presumably from frog microbiomes, were found in populations with a history of ranavirus (<xref ref-type="bibr" rid="B26">Campbell et&#xa0;al., 2018</xref>). Differential impacts of changing climate on host and pathogen further complicate strategies to prevent transmission (<xref ref-type="bibr" rid="B12">Blaustein et&#xa0;al., 2012</xref>). It is likely that warming climates will impact viral loads, as observed in juveniles at warmer temperatures with less intense but persistent infections (<xref ref-type="bibr" rid="B22">Brunner et&#xa0;al., 2019</xref>), and bacteria-killing ability is reduced at higher temperatures in some species (<xref ref-type="bibr" rid="B125">Rodriguez and Voyles, 2020</xref>). Coinfection of ranavirus and chytrid in several endemic tadpoles underscores the importance of understanding the etiology and interactions of these pathogens for effective conservation of amphibians and other aquatic vertebrates (<xref ref-type="bibr" rid="B177">Warne et&#xa0;al., 2016</xref>).</p>
</sec>
<sec id="s1_3">
<label>1.3</label>
<title>Pesticides</title>
<p>Agricultural and residential pesticide use has also been implicated as a contributing factor in declining amphibian populations (<xref ref-type="bibr" rid="B60">Hayes et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B20">Br&#xfc;hl et&#xa0;al., 2011</xref>, <xref ref-type="bibr" rid="B21">2013</xref>) with agriculture identified as the most common cause of extinction threats for amphibians and other terrestrial vertebrates (<xref ref-type="bibr" rid="B101">Munstermann et&#xa0;al., 2022</xref>). A meta-analysis of pesticide effects revealed moderate impacts on survival and decreased mass and relatively greater impacts from deformities not associated with phylogeny. Although contaminants of emerging concern were underrepresented in pollutant studies, pesticide effects were comparable with those of wastewater, less impactful compared to deicer effects, and relatively greater than those of metals and phosphorus compounds (<xref ref-type="bibr" rid="B37">Egea-Serrano et&#xa0;al., 2012</xref>). Additionally, transgenerational impacts, lethal and sublethal, have been demonstrated from exposure to environmentally relevant pesticide concentrations (<xref ref-type="bibr" rid="B71">Karlsson et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B163">Usal et&#xa0;al., 2021</xref>). The amphibian life cycle allows complex exposure dynamics in both aquatic and terrestrial environments, and recommended application rates of many pesticides result in high mortality from terrestrial exposure (<xref ref-type="bibr" rid="B21">Br&#xfc;hl et&#xa0;al., 2013</xref>), although terrestrial effects are less frequently documented. Indirect effects of pesticide use at lower concentrations than those toxic to amphibians potentially impact the full lifecycle of amphibians through reduction of resources, although aquatic food web effects are more frequently reported than terrestrial food web effects (<xref ref-type="bibr" rid="B121">Relyea and Diecks, 2008</xref>; <xref ref-type="bibr" rid="B120">Relyea, 2009</xref>). Overall, aquatic pesticide exposure can alter various endocrine functions important to development and reproduction and result in a variety of systemic impacts in amphibians (<xref ref-type="bibr" rid="B157">Thambirajah et&#xa0;al., 2019</xref>). A recent review of endocrine disruption by agrochemicals summarized changes in lipid and energy metabolism among fungicides; effects on metabolism, metamorphic success, and gonadal development for some herbicides; and reduced metamorphosis from fertilizer and other pesticide exposures (<xref ref-type="bibr" rid="B162">Trudeau et&#xa0;al., 2020</xref>). Evaluating the non-lethal effects of pesticides is complicated by timing of exposure and sample collection as well as tissue type, such that measured effects vary depending on species, mechanism of action, route of exposure, and the concentration of the compound (<xref ref-type="bibr" rid="B126">Rohr and McCoy, 2010</xref>; <xref ref-type="bibr" rid="B51">Glinski et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B145">Seim et&#xa0;al., 2022</xref>). Even with the abundance of scientific support correlating pesticide exposure to declining amphibian populations, it is unrealistic that impacts of pesticide exposure will be reversed, given the moderate generation times of most amphibians, the complexity of potential exposure based on their life cycle, and the substantial proportion of croplands in protected areas associated with continuing tradeoffs between food security and conservation (<xref ref-type="bibr" rid="B171">Vijay and Armsworth, 2021</xref>).</p>
</sec>
<sec id="s1_4">
<label>1.4</label>
<title>Stressor interactions</title>
<p>Uncertainty surrounding individual response, species vulnerability, and exposure regime complicates risk assessment determinations of multiple stressor impacts at the landscape level (<xref ref-type="bibr" rid="B122">Relyea and Hoverman, 2006</xref>). For instance, co-stressors such as heat, pesticides, and parasites impact amphibian immune responses and can have synergistic effects on fecundity and post-recruitment survival (<xref ref-type="bibr" rid="B73">Kiesecker, 2002</xref>, <xref ref-type="bibr" rid="B159">Thompson et&#xa0;al., 2022</xref>). When anthropogenic stressors and abiotic factors synergize, the immune system is challenged (<xref ref-type="bibr" rid="B74">Kiesecker, 2011</xref>), and early stress experienced during development can affect resilience in later life stages (<xref ref-type="bibr" rid="B78">Kohli et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B84">Le Sage et&#xa0;al., 2022</xref>). Disease susceptibility can increase following herbicide exposure (<xref ref-type="bibr" rid="B127">Rohr et&#xa0;al., 2013</xref>), and lower microbiota diversity, a common result of pesticide exposure, is associated with reduced parasite resistance (<xref ref-type="bibr" rid="B77">Knutie et&#xa0;al., 2017</xref>). Anticipating potential long-term effects in response to various stressors and their interactions, which can promulgate into subsequent life stages, challenges both establishing <italic>in situ</italic> causality from single stressors needed for tighter regulations and effective conservation management. Ultimately, ecological risk assessment is complicated not only by a deficit of toxicological data, but also a lack of ecological data to document changes in land use, species abundance and distribution, and disease transmission that are necessary for adaptive management approaches (<xref ref-type="bibr" rid="B179">Womack et&#xa0;al., 2022</xref>). Extrinsic stressors are presented in <xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref> along with physiological measurements of these effects, endogenous processes affecting the same biochemical pathways, and life stages in which departures from typical functions are detectable and/or problematic (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>).</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Endogenous activity associated with transitional phases of the anuran lifecycle, exogenous stressors that alter biological processes, methods to assess organismal effects, and potential demographic impacts. &#x2191; upregulation or increased expression; &#x2193; downregulation or decreased expression.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" align="left">Stage</th>
<th valign="middle" align="left">Systemic response</th>
<th valign="middle" align="left">Endogenous activity</th>
<th valign="middle" align="left">Exogenous stressors</th>
<th valign="middle" align="left">Assessment methods</th>
<th valign="middle" align="left">Demographic endpoint</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="middle" align="left">
<bold>Embryolarval development</bold>
</td>
<td valign="middle" align="left">Metabolism</td>
<td valign="middle" align="left">Energy production, DNA synthesis, protein synthesis&#x2191;, alanine &#x2193; aspartate &#x2193;, &#x3b1;-ketoglutamine &#x2191; (<xref ref-type="bibr" rid="B168">Vastag et&#xa0;al., 2011</xref>)</td>
<td valign="middle" align="left">Aquatic conditions, including chemical pollution, pathogens, predation (<xref ref-type="bibr" rid="B74">Kiesecker, 2011</xref>) </td>
<td valign="middle" align="left">Whole-organism metabolites (<xref ref-type="bibr" rid="B168">Vastag et&#xa0;al., 2011</xref>)</td>
<td valign="middle" align="left">Embryo mortality; cessation of development</td>
</tr>
<tr>
<td valign="middle" align="left">
<bold>Metamorphosis</bold>
</td>
<td valign="middle" align="left">Metabolism</td>
<td valign="middle" align="left">Increasing energy needs, anabolic activity, tail apoptosis; greater dehydration from fasting (<xref ref-type="bibr" rid="B131">Rowland et&#xa0;al., 2023</xref>); purine, arginine and pyrimidine, urea cycle metabolites, arginine and purine/pyrimidine, cysteine/methionine, sphingolipid, and eicosanoid metabolism (<xref ref-type="bibr" rid="B67">Ichu et&#xa0;al., 2014</xref>)</td>
<td valign="middle" align="left">&#x2191; galactose metabolism and lactose degradation with xenobiotic exposure (<xref ref-type="bibr" rid="B51">Glinski et&#xa0;al., 2021</xref>) or reduced resources; &#x2193; glutathione (<xref ref-type="bibr" rid="B67">Ichu et&#xa0;al., 2014</xref>); galactose predictive of chytrid (<xref ref-type="bibr" rid="B176">Wang et&#xa0;al., 2021</xref>); predation and pesticide exposure alter aminoacyl-tRNA biosynthesis, galactose and glutathione metabolism, arginine biosynthesis (<xref ref-type="bibr" rid="B149">Snyder et&#xa0;al., 2022</xref>); pesticide exposure impacts serine and threonine, histadine, linoleic acid, and sphingolipid metabolism</td>
<td valign="middle" align="left">Whole-organism or tissue metabolomics (<xref ref-type="bibr" rid="B67">Ichu et&#xa0;al., 2014</xref>)</td>
<td valign="middle" align="left">Delayed development, reduced transition to juvenile stage</td>
</tr>
<tr>
<td valign="middle" align="left"/>
<td valign="middle" align="left">Redox signalling</td>
<td valign="middle" align="left">Lipid peroxidation &#x2191;, glutathione &#x2193;, catalase &#x2193;, SOD, CAT, MDA expression altered during intestinal development and tail resorption, ascorbic acid &#x2191; for collagen synthesis (<xref ref-type="bibr" rid="B96">Menon and Rozman, 2007</xref>; <xref ref-type="bibr" rid="B55">Guo et&#xa0;al., 2022</xref>); glutathione peroxidase &#x2193;, GST &#x2193;, sulfhydryl groups &#x2193; (<xref ref-type="bibr" rid="B115">Petrovi&#x107; et&#xa0;al., 2021</xref>)</td>
<td valign="middle" align="left">Lower antioxidant activity and increased lipid peroxidation to xenobiotics or environmental conditions (abiotic or density effects; <xref ref-type="bibr" rid="B23">Burraco et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B115">Petrovi&#x107; et&#xa0;al., 2021</xref>); &#x2191; thiol and CAT in pesticide and nematode infection (<xref ref-type="bibr" rid="B88">Marcogliese et&#xa0;al., 2021</xref>)</td>
<td valign="middle" align="left">ROS production in tissues; antioxidant enzymatic responses of SOD, CAT, MDA, GST (<xref ref-type="bibr" rid="B96">Menon and Rozman, 2007</xref>; <xref ref-type="bibr" rid="B28">Chen et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B55">Guo et&#xa0;al., 2022</xref>); decreased expression of GSH; increased TBARS</td>
<td valign="middle" align="left">Delayed development; reduced transition to juvenile stage</td>
</tr>
<tr>
<td valign="middle" align="left"/>
<td valign="middle" align="left">Endocrine response</td>
<td valign="middle" align="left">CS in response to &#x2191; TH, regulate development via diodination, glucuronidation, sulfation, affecting HPT, HPA, HPG axes (<xref ref-type="bibr" rid="B32">Denver, 2009</xref>; <xref ref-type="bibr" rid="B36">Duarte-Guterman et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B157">Thambirajah et&#xa0;al., 2019</xref>)</td>
<td valign="middle" align="left">GC &#x2191; to some xenobiotics (<xref ref-type="bibr" rid="B24">Burraco and Gomez-Mestre, 2016</xref>; <xref ref-type="bibr" rid="B162">Trudeau et&#xa0;al., 2020</xref>), environmental conditions (<xref ref-type="bibr" rid="B137">Sachs and Buchholz, 2019</xref>; <xref ref-type="bibr" rid="B157">Thambirajah et&#xa0;al., 2019</xref>), predators (<xref ref-type="bibr" rid="B103">Narayan et&#xa0;al., 2013</xref>) ; neurogenerative, oxidative, mitochondrial, teratological effects (<xref ref-type="bibr" rid="B33">Di Lorenzo et&#xa0;al., 2020</xref>)</td>
<td valign="middle" align="left">CS and TH levels in tissue or immersed water (<xref ref-type="bibr" rid="B48">Gabor et&#xa0;al., 2013a</xref>); tissue/organism enzyme activity or DGE in AR, TR, tra, trb, dio2, dio3 (<xref ref-type="bibr" rid="B158">Thambirajah et&#xa0;al., 2022</xref>); ambient water assay; size at metamorphosis (<xref ref-type="bibr" rid="B131">Rowland et&#xa0;al., 2023</xref>); vitellogenin indicative of feminization (<xref ref-type="bibr" rid="B169">Venturino and de D&#x2019;Angelo, 2005</xref>)</td>
<td valign="middle" align="left">Time to metamorphosis; cohort sex ratio; carryover to juvenile immunity, survival, fecundity (<xref ref-type="bibr" rid="B73">Kiesecker, 2002</xref>, <xref ref-type="bibr" rid="B32">Denver, 2009</xref>; <xref ref-type="bibr" rid="B78">Kohli et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B136">Ruthsatz et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B84">Le Sage et&#xa0;al., 2022</xref>)</td>
</tr>
<tr>
<td valign="middle" align="left"/>
<td valign="middle" align="left">Immunity</td>
<td valign="middle" align="left">Endocrine-driven development of immunity; immunosuppression at metamorphosis (<xref ref-type="bibr" rid="B129">Rollins-Smith, 2017</xref>)</td>
<td valign="middle" align="left">Viral loads, resistance, and parasite prevalance affected by pesticides and abiotic factors (<xref ref-type="bibr" rid="B72">Kerby et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B74">Kiesecker, 2011</xref>; <xref ref-type="bibr" rid="B77">Knutie et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B117">Pochini and Hoverman, 2017</xref>); Microbiome in tadpoles impacted by xenobiotic exposure</td>
<td valign="middle" align="left">Gut microbiome diversity; at advanced developmental stages &#x2013; blood leukocytes, white cell lymphocytes and granulocytes (basophils, neutrophils, eosinophils); DGE (<xref ref-type="bibr" rid="B130">Row et&#xa0;al., 2016</xref>)</td>
<td valign="middle" align="left">Reduced survival due to pathogens and parasites (<xref ref-type="bibr" rid="B74">Kiesecker, 2011</xref>)</td>
</tr>
<tr>
<td valign="middle" align="left">
<bold>Juvenile maturation to adult</bold>
</td>
<td valign="middle" align="left">Endocrine</td>
<td valign="middle" align="left">TRH influences TSH (<xref ref-type="bibr" rid="B112">Paul et&#xa0;al., 2022</xref>)</td>
<td valign="middle" align="left">Food constraints &#x2193; CORT (<xref ref-type="bibr" rid="B119">Proki&#x107; et&#xa0;al., 2021</xref>); variance in CORT along latitudinal cline (<xref ref-type="bibr" rid="B84">Le Sage et&#xa0;al., 2022</xref>)</td>
<td valign="middle" align="left">Dermal swab, fecal content, tissue or ambient water assay of CS (<xref ref-type="bibr" rid="B48">Gabor et&#xa0;al., 2013a</xref>)</td>
<td valign="middle" align="left">Behavioral responses to stressors, reduced dispersal</td>
</tr>
<tr>
<td valign="middle" rowspan="3" align="left"/>
<td valign="middle" align="left">Immunity</td>
<td valign="middle" align="left">Gut microbiome linked to resistance of parasites (<xref ref-type="bibr" rid="B77">Knutie et&#xa0;al., 2017</xref>), skin microbiome linked to resistance of pathogens (<xref ref-type="bibr" rid="B80">Krynak et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B94">McCoy and Peralta, 2018</xref>; <xref ref-type="bibr" rid="B69">Jim&#xe9;nez et&#xa0;al., 2021</xref>); possibly compromised by shortened developmental hydroperiod (<xref ref-type="bibr" rid="B16">Brannelly et&#xa0;al., 2019</xref>); Lower juvenile immunity relative to mature adults</td>
<td valign="middle" align="left">Dermal microbiome and pathogen vulnerability impacted by xenobiotic exposure (<xref ref-type="bibr" rid="B80">Krynak et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B94">McCoy and Peralta, 2018</xref>; <xref ref-type="bibr" rid="B69">Jim&#xe9;nez et&#xa0;al., 2021</xref>); habitat degradation affects vulnerability to pathogens (<xref ref-type="bibr" rid="B153">Stevens and Baguette, 2008</xref>; <xref ref-type="bibr" rid="B30">Costa et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B9">Becker et&#xa0;al., 2023</xref>)</td>
<td valign="middle" align="left">Microbiome diversity in skin mucosa (<xref ref-type="bibr" rid="B105">Neely et&#xa0;al., 2022</xref>); antimicrobial peptides (<xref ref-type="bibr" rid="B66">Huang et&#xa0;al., 2016</xref>); white cell lymphocytes and granulocytes (basophils, neutrophils, eosinophils); B and T cells in organs, MHC-II; antibodies - IgA/X, IgD, IgF, IgM, IgY</td>
<td valign="middle" align="left">Susceptibility to pathogens, reduced juvenile survival or limited dispersal due to disease or deformities (<xref ref-type="bibr" rid="B73">Kiesecker, 2002</xref>, <xref ref-type="bibr" rid="B128">Rohr et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B80">Krynak et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B78">Kohli et&#xa0;al., 2019</xref>)</td>
</tr>
<tr>
<td valign="middle" align="left">Metabolism</td>
<td valign="middle" align="left">Related to endocrine activity; longer hydroperiod &#x2191; lipid stores (<xref ref-type="bibr" rid="B144">Scott et&#xa0;al., 2007</xref>)</td>
<td valign="middle" align="left">Influenced by temperature, water loss, xenobiotics; food deprivation &#x2193; CORT; pesticides altered sucrose and starch pathway regulation (<xref ref-type="bibr" rid="B182">Zaya et&#xa0;al., 2011</xref>, <xref ref-type="bibr" rid="B34">Dornelles and Oliveria, 2016</xref>, <xref ref-type="bibr" rid="B165">Van Meter et&#xa0;al., 2018</xref>)</td>
<td valign="middle" align="left">Body condition; energy metabolism in tissue</td>
<td valign="middle" align="left">Reduced juvenile survival</td>
</tr>
<tr>
<td valign="middle" align="left">Redox signalling</td>
<td valign="middle" align="left">Increased antioxidants during estivation in preparation for oxidative stress; lower oxidative metabolism enzyme activity during estivation (<xref ref-type="bibr" rid="B131">Rowland et&#xa0;al., 2023</xref>)</td>
<td valign="middle" align="left">Food constraints &#x2191; lipid peroxide; &#x2193; SOD, glutathione peroxidase, GST, glutathione and sulfhydryl groups (<xref ref-type="bibr" rid="B119">Proki&#x107; et&#xa0;al., 2021</xref>); pesticides and pathogens &#x2191; thiol; nematode infections &#x2191; thiol, &#x2191; catalase (<xref ref-type="bibr" rid="B88">Marcogliese et&#xa0;al., 2021</xref>)</td>
<td valign="middle" align="left">ROS production; anti-oxidant enzymatic responses of SOD, glutathione peroxidase, glutathione, GST, thiol, catalase (<xref ref-type="bibr" rid="B88">Marcogliese et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B119">Proki&#x107; et&#xa0;al., 2021</xref>)</td>
<td valign="middle" align="left">Survival to following breeding season, potentially a function of size/condition at end of season</td>
</tr>
<tr>
<td valign="middle" align="left">
<bold>Adult fecundity</bold>
</td>
<td valign="middle" align="left">Endocrine activity</td>
<td valign="middle" align="left">Gonadotropins released by pituitary; estrogen, androgen, progestogen regulate reproduction (<xref ref-type="bibr" rid="B36">Duarte-Guterman et&#xa0;al., 2014</xref>)</td>
<td valign="middle" align="left">Endocrine disrupting compounds can disrupt gonadal development, sexual differentiation (<xref ref-type="bibr" rid="B82">Lambert et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B89">Marlatt et&#xa0;al., 2022</xref>); temperature impact on sex determination (<xref ref-type="bibr" rid="B82">Lambert et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B133">Ruiz-Garc&#xed;a et&#xa0;al., 2021</xref>); density-dependent resource availability (<xref ref-type="bibr" rid="B76">Kissel et&#xa0;al., 2020</xref>)</td>
<td valign="middle" align="left">ER/AR binding; Aromatase inhibition; impairment of steroidogenesis; vitellogenin expression in response to xenoestrogen exposure; zona radiata, zona pellucida, DGE in er, bteb, tra, trb, thbzip,</td>
<td valign="middle" align="left">Altered population sex ratio (<xref ref-type="bibr" rid="B124">Roco et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B6">Baranek et&#xa0;al., 2022</xref>); reduced fecundity</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p>Endogenous activity associated with transitional phases of the anuran lifecycle, exogenous stressors that alter biological processes, methods to assess organismal effects, and potential demographic impacts. &#x2191; upregulation or increased expression; &#x2193; downregulation or decreased expression. </p>
</table-wrap-foot>
</table-wrap>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Symbols represent influential abiotic factors and extrinsic sources of population regulation. These potential stressors impact endogenous processes (shown in center block) in similar ways physiologically, and can affect individuals differently, depending on the life stage at which the stress occurs.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fevo-12-1336747-g002.tif"/>
</fig>
</sec>
</sec>
<sec id="s2">
<label>2</label>
<title>Lifestage-specific physiology</title>
<p>Effective adaptive conservation management strategies target vulnerable life stages and critical threats to wildlife populations. The biphasic life cycle of anuran amphibians makes them particularly vulnerable to extrinsic stressors because of their dependence on variable aquatic habitat resources as well as terrestrial environmental quality (<xref ref-type="bibr" rid="B107">Nolan et&#xa0;al., 2023</xref>). Their complex life history strategy and multiple potential drivers of population decline require a more nuanced approach to targeting spatial and temporal variability in stressors relative to life stage (<xref ref-type="bibr" rid="B174">Walls and Gabor, 2019</xref>; <xref ref-type="bibr" rid="B3">Awkerman et&#xa0;al., 2020</xref>). Distinguishing stage-specific endogenous variation in physiological processes enables anticipation of compromised physical condition in response to common stressors (<xref ref-type="bibr" rid="B19">Brooks and Kindsvater, 2022</xref>; <xref ref-type="bibr" rid="B107">Nolan et&#xa0;al., 2023</xref>). Here we focus on stressor impacts on transition between life stages (F, T<sub>e</sub>, T<sub>l</sub>, T<sub>j</sub> in <xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>) but present potential effects on survival and development as well.</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Vital rates (indicated by arrows) for the anuran life cycle, including survival rates (green arrows; S) for terrestrial juvenile (Sj) and adult stages (Sa), transition rates (yellow arrows; T) from embryo to larval stage (Te), from larval to juvenile stage (Tl), and from juvenile to adult stage (Tj); and fecundity (purple arrow; F).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fevo-12-1336747-g001.tif"/>
</fig>
<sec id="s2_1">
<label>2.1</label>
<title>Development (embryo transition to tadpole stage; T<sub>e</sub>)</title>
<p>Survival during the relatively brief stage of embryo development is largely dependent on a suitable environment to avoid predators, pathogens, or pollution, and the costs associated with such defenses differ among amphibian species and developmental mode (<xref ref-type="bibr" rid="B19">Brooks and Kindsvater, 2022</xref>). Amphibian clutches can experience high mortality from pathogens or predation, depending on the geographic location and ecological community composition (<xref ref-type="bibr" rid="B74">Kiesecker, 2011</xref>), such that habitat characteristics and regional observations are most informative in identifying these threats (<xref ref-type="bibr" rid="B172">Wake and Vredenburg, 2008</xref>). Pesticides aggregated as runoff in wetlands provide another potential stressor for developing embryos (<xref ref-type="bibr" rid="B148">Smalling et&#xa0;al., 2015</xref>) with lethal or sublethal impacts on individuals. Ultimately, a systematic review revealed that the time to hatching for embryos was influenced more by taxonomy and exposure to pollution, rather than experimental setting (lab vs. field; <xref ref-type="bibr" rid="B37">Egea-Serrano et&#xa0;al., 2012</xref>). Singly or in combinations, stressors during embryogenesis can lead to delayed, wide-ranging effects, resulting in a diverse array of phenotypic outcomes associated with aspects of developmental plasticity that are not observed until later life history stages (<xref ref-type="bibr" rid="B70">Jonsson et&#xa0;al., 2022</xref>).</p>
<p>Given the relatively brief duration of this stage in most anuran species, and rapidly changing metabolism, identifying potential stressors based on organismal condition or response could be a challenging diagnostic approach, compared to assessment of anomalous response during later life stages. Endogenous variation in embryonic metabolite levels is suggestive of energy production primarily, presumably for DNA synthesis (<xref ref-type="bibr" rid="B168">Vastag et&#xa0;al., 2011</xref>). Contaminant levels in egg masses that are linked to deformities and reduced offspring viability can result from maternal transfer of contaminants rather than indicating direct environmental exposure alone (<xref ref-type="bibr" rid="B160">Todd et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B97">Metts et&#xa0;al., 2013</xref>). Determining physiological response to a variety of stressors (e.g., contaminant mixtures and abiotic factors), is a complex challenge that might be approached by evaluating exposure-based epigenetic changes (e.g., DNA methylation, histone acetylation) in developing embryos (<xref ref-type="bibr" rid="B43">Fogliano et&#xa0;al., 2023</xref>) or simply assessing differential responses in later life stages.</p>
</sec>
<sec id="s2_2">
<label>2.2</label>
<title>Metamorphosis (transition from larval to juvenile stage; T<sub>l</sub>)</title>
<p>The morphological restructuring for transition from larval stage to juvenile stage is dependent on endocrine drivers, specifically surges in thyroid hormones (TH), regulated by thyroid hormone receptors and retinoic acid receptors (TR and RXR, respectively; reviewed in <xref ref-type="bibr" rid="B112">Paul et&#xa0;al., 2022</xref>). Endocrine regulation and body morphogenesis during the larval stage are controlled by the hypothalamic-pituitary-thyroid (HPT) and hypothalamic-pituitary-adrenal/interrenal axes (HPA/HPI) as well as the hypothalamus-pituitary-gonadal (HPG) axis (<xref ref-type="bibr" rid="B36">Duarte-Guterman et&#xa0;al., 2014</xref>). Development and metamorphosis are regulated largely by the release of the thyroid hormones thyroxine (T4) and tri-iodothyronine (T3) and modulated by the corticosteroids (CS) corticosterone (CORT) and aldosterone (ALDO; <xref ref-type="bibr" rid="B32">Denver, 2009</xref>). Regulation of TH signal involves cellular processes of deiodination, glucuronidation, and sulfation (<xref ref-type="bibr" rid="B157">Thambirajah et&#xa0;al., 2019</xref>). Metabolism and cardiac functions associated with development and metamorphosis are also regulated by CS. <xref ref-type="bibr" rid="B136">Ruthsatz et&#xa0;al. (2020)</xref> showed that certain metamorphic stages were significantly more susceptible to changes in growth and development due to increased TH levels, with high TH levels associated with reduced weight and size in tadpole and froglet stages as well as increased heart rate and reduced energy stores across all stages.</p>
<p>TH inhibition or impairment can delay development, while CS production is often associated with accelerated metamorphosis in response to pond drying or other stressors (<xref ref-type="bibr" rid="B137">Sachs and Buchholz, 2019</xref>; <xref ref-type="bibr" rid="B157">Thambirajah et&#xa0;al., 2019</xref>), although the role of CORT as a homeostatic response to stress is complex. The corticotropic releasing hormone (CRH) regulates the HPA axis as well as the HPT axis, thereby contributing to additional crosstalk between these pathways and circulating hormone levels (<xref ref-type="bibr" rid="B158">Thambirajah et&#xa0;al., 2022</xref>). CORT levels in southern leopard frogs increased with exposure to multiple aquatic stressors, specifically a nitrogenous fertilizer, a pesticide, and salt (<xref ref-type="bibr" rid="B1">Adelizzi et&#xa0;al., 2019</xref>). However, relatively elevated CORT levels were associated with populations less tolerant to contaminant exposure, such that differences in stress response could be indicative of exposure history (<xref ref-type="bibr" rid="B146">Shidemantle et&#xa0;al., 2022</xref>). Predator detection can also elicit an increased CORT response (<xref ref-type="bibr" rid="B103">Narayan et&#xa0;al., 2013</xref>). Signals of agrochemical disruption of endocrine function among interactions of the thyroid, gonadal, and metabolic axes in amphibians was reviewed in detail by <xref ref-type="bibr" rid="B162">Trudeau et&#xa0;al. (2020)</xref>. Early life stage stressors that elevate CS production can alter endocrine response throughout the lifecycle of the individual (<xref ref-type="bibr" rid="B32">Denver, 2009</xref>).</p>
<p>Stressor perturbations in endocrine functions are particularly impactful in metamorphosing amphibians and can influence immunity, survival, and fecundity in subsequent terrestrial life stages (<xref ref-type="bibr" rid="B73">Kiesecker, 2002</xref>; <xref ref-type="bibr" rid="B78">Kohli et&#xa0;al., 2019</xref>). A meta-analysis determining effects on time to metamorphosis found taxonomy, pollution, and timing of exposure to be more influential than the experimental setting (<xref ref-type="bibr" rid="B37">Egea-Serrano et&#xa0;al., 2012</xref>). Pond drying constraints influencing larval development are expected to be impacted in various ways by climate change, depending on regional location (<xref ref-type="bibr" rid="B173">Walls et&#xa0;al., 2013</xref>). The duration of larval stage and developmental mode, combined with community dynamics between larval competitors and predators, can distinguish species resilience and response to such unpredictable environmental stressors (<xref ref-type="bibr" rid="B10">Belden et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B100">Moss et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B19">Brooks and Kindsvater, 2022</xref>). Interannual variability in hydrologic regime at temporary wetlands determines the length of the developmental period and the density of developing anuran larvae (e.g., <xref ref-type="bibr" rid="B113">Pechmann et&#xa0;al., 1989</xref>). Developmental plasticity in metamorphic climax allows variable phenotypic response to interannual conditions and is driven by the neuroendocrine processes responsible for the development of the immune system, highlighting a potential tradeoff between accelerated development and resistance to disease and parasites (<xref ref-type="bibr" rid="B78">Kohli et&#xa0;al., 2019</xref>). Likewise, tradeoffs between development and microbiota diversity or immunology are demonstrated later in life with increased susceptibility to pathogens (<xref ref-type="bibr" rid="B84">Le Sage et&#xa0;al., 2022</xref>). As northern leopard frog tadpoles approach metamorphic climax, tail tissue decreases expression of mitochondrial energy genes and upregulates expression of immunity genes (<xref ref-type="bibr" rid="B130">Row et&#xa0;al., 2016</xref>). Post-metamorphic immune function may be compromised in amphibians experiencing shorter hydrologic regimes (<xref ref-type="bibr" rid="B16">Brannelly et&#xa0;al., 2019</xref>), which may further exacerbate disease susceptibility. Therefore, interannual variance in aquatic habitat suitability can have lasting impacts on cohort fitness.</p>
<p>During metamorphic climax, metabolic activity changes, reflecting increasing energy needs, anabolic requirements, and tail apoptosis; these energetic requirements and fasting effects create a vulnerable transition from larva to juvenile in which contaminant body burdens can amplify (<xref ref-type="bibr" rid="B131">Rowland et&#xa0;al., 2023</xref>). The aquatic phase of the amphibian life cycle is also susceptible to reduced growth in response to pathogens that have been introduced to waterbodies, although survival is rarely impacted at this stage (<xref ref-type="bibr" rid="B107">Nolan et&#xa0;al., 2023</xref>). Although phylogeny and abiotic environmental variables determine the initial likelihood of <italic>Bd</italic> or ranavirus occurrence in areas of viral compatibility, other stressors such as pesticides can further influence viral loads and the resistance of the host population as well as the prevalence of parasite-induced deformities (e.g., <xref ref-type="bibr" rid="B72">Kerby et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B74">Kiesecker, 2011</xref>; <xref ref-type="bibr" rid="B117">Pochini and Hoverman, 2017</xref>).</p>
</sec>
<sec id="s2_3">
<label>2.3</label>
<title>Maturity (juvenile transition to reproductive adult; T<sub>j</sub>)</title>
<p>The literature on this critical amphibian life stage is scarce, due in part to the complexity of rearing and maintaining juvenile amphibian populations in a laboratory setting through maturation, as well as the challenge of monitoring individual juvenile amphibians from metamorphosis through reproduction in a field setting (see <xref ref-type="bibr" rid="B114">Petrovan and Schmidt, 2019</xref>). Furthermore, a systematic analysis of factors affecting survival found pollutants and the experimental setting (lab vs. field) to be more influential than taxonomic group or developmental stage in the study (<xref ref-type="bibr" rid="B37">Egea-Serrano et&#xa0;al., 2012</xref>). Although pre-metamorphic environmental conditions directly influence post-metamorphic life stages, there may also be distinctly different age or stage-specific stress responses in amphibians, as evidenced by variations in sucrose and starch pathway regulation following pesticide exposure in larval and juvenile amphibians (<xref ref-type="bibr" rid="B182">Zaya et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B34">Dornelles and Oliveria, 2016</xref>; <xref ref-type="bibr" rid="B165">Van Meter et&#xa0;al., 2018</xref>). Survival to reproduction was positively correlated with lipid stores at metamorphosis among two <italic>Ambystoma</italic> salamander species, and lipid stores were greater among individuals emerging from longer hydroperiod wetlands. Furthermore, total rainfall during years of juvenile development was also positively associated with survival to reproduction (<xref ref-type="bibr" rid="B144">Scott et&#xa0;al., 2007</xref>).</p>
<p>Potential carry-over effects from compromised development can exist (<xref ref-type="bibr" rid="B73">Kiesecker, 2002</xref>; <xref ref-type="bibr" rid="B128">Rohr et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B78">Kohli et&#xa0;al., 2019</xref>) with additional risk from stressors in the terrestrial environment. Terrestrial habitat degradation and habitat fragmentation influences the connectivity of both amphibian populations and their potential pathogens (<xref ref-type="bibr" rid="B153">Stevens and Baguette, 2008</xref>; <xref ref-type="bibr" rid="B30">Costa et&#xa0;al., 2021</xref>; <xref ref-type="bibr" rid="B9">Becker et&#xa0;al., 2023</xref>). Reduced skin and gut microbiota in the larval stage can also reduce parasite resistance in adults (<xref ref-type="bibr" rid="B77">Knutie et&#xa0;al., 2017</xref>). Amphibian skin contains antimicrobial peptides linked to immunity and defense functions as well as to biosynthesis and metabolism (<xref ref-type="bibr" rid="B66">Huang et&#xa0;al., 2016</xref>). Skin secretions have demonstrated antimicrobial antioxidant properties and can be beneficial to healing (<xref ref-type="bibr" rid="B175">Wang et&#xa0;al., 2020</xref>). Bacterial and fungal taxonomy in skin secretions is associated with disease resistance (<xref ref-type="bibr" rid="B7">Bates et&#xa0;al., 2022</xref>), with the skin microbiome affected by the same abiotic factors that influence <italic>Bd</italic> occurrence (<xref ref-type="bibr" rid="B136">Ruthsatz et&#xa0;al., 2020</xref>). Some species&#x2019; secretions contain sufficient toxins to be lethal to predators, thereby reducing mortality via predation (<xref ref-type="bibr" rid="B87">Liu et&#xa0;al., 2022</xref>). Compromised skin microbiome diversity is implicated in important physiological functions such as electrolyte and hydration loss, disease susceptibility, and increased pesticide effects. Pesticide exposure has been linked to disruption of the skin microbiome and antimicrobial peptides of amphibians, thereby affecting vulnerability to pathogens (<xref ref-type="bibr" rid="B80">Krynak et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B94">McCoy and Peralta, 2018</xref>; <xref ref-type="bibr" rid="B69">Jim&#xe9;nez et&#xa0;al., 2021</xref>). Habitat disturbance has also been associated with skin microbiome diversity, primarily via pathogen dispersal (<xref ref-type="bibr" rid="B105">Neely et&#xa0;al., 2022</xref>), underscoring the ecological complexity of proximate mechanisms of multiple stressors and their potential interactions. Enhanced data collection efforts on juvenile amphibians are essential to improve risk assessment and inform management decisions at the local scale.</p>
</sec>
<sec id="s2_4">
<label>2.4</label>
<title>Fecundity (adult production of embryos; F)</title>
<p>Reproductive failure associated with insufficient hydroperiod is a determinant of lifetime reproductive success in species dependent on ephemeral wetlands for breeding (<xref ref-type="bibr" rid="B156">Taylor et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B153">Stevens and Baguette, 2008</xref>). In years with suitable hydroregime, terrestrial density dependence and sex ratio can affect fecundity within a population (<xref ref-type="bibr" rid="B76">Kissel et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B6">Baranek et&#xa0;al., 2022</xref>). Effects of endocrine disruption in developmental phases as well as during gamete production could also reduce fecundity via altered gonadal development, or a high incidence of intersex individuals in the population (<xref ref-type="bibr" rid="B82">Lambert et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B89">Marlatt et&#xa0;al., 2022</xref>). Sex-specific age at maturation could further restrict operational sex ratio in amphibian populations (<xref ref-type="bibr" rid="B6">Baranek et&#xa0;al., 2022</xref>). In addition to the endocrine disruption associated with xenobiotic exposure, temperature can affect sex determination, with potential impact on operational sex ratio following extended periods of anomalous temperatures (<xref ref-type="bibr" rid="B82">Lambert et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B133">Ruiz-Garc&#xed;a et&#xa0;al., 2021</xref>). The lasting impact of such shifts will vary depending on the species life history and genetic sex determination (<xref ref-type="bibr" rid="B15">B&#xf3;kony et&#xa0;al., 2017</xref>).</p>
</sec>
</sec>
<sec id="s3">
<label>3</label>
<title>Field-based measures of stressor response</title>
<p>Assessing the status of a wildlife population or relative condition of an individual within its habitat is a challenge complicated by the heterogeneity of both organismal response and stressor distribution. Acquiring an adequate sample size for a meaningful detection of environmental or stressor effects could limit the practical scope of most field-based efforts, while standardization of conditions can bias the interpretation of stressor response in most laboratory or mesocosm settings. Stage-specific physiology, along with ecological or life history vulnerabilities, provides additional context for interpretation of potential stressor effects (<xref ref-type="bibr" rid="B170">Venturino et&#xa0;al., 2003</xref>). For example, intestinal development and tail resorption in larvae are coincident with signs of oxidative stress (<xref ref-type="bibr" rid="B96">Menon and Rozman, 2007</xref>). Establishing baseline physiology with common biomarkers provides context of endogenous variability during the amphibian life cycle. Identifying these informative endpoints and sensitive stages can preclude the need for extensive accounting of stressor-specific effects and interactions.</p>
<sec id="s3_1">
<label>3.1</label>
<title>Physiological processes</title>
<p>Systematic responses to stress include endocrine disruption, oxidative stress, metabolic perturbation, and compromised immunity (<xref ref-type="bibr" rid="B170">Venturino et&#xa0;al., 2003</xref>). Specifically, elevated CORT and standard metabolic rate as well as decreased antioxidant enzymes are common signals of abiotic and xenobiotic physiological stress (<xref ref-type="bibr" rid="B24">Burraco and Gomez-Mestre, 2016</xref>). Endocrine disruption in the interconnected hormonal axes can also trigger responses in other systems, such as neurodegenerative effects, oxidative damage, impairment of mitochondrial function, and teratological effects (<xref ref-type="bibr" rid="B33">Di Lorenzo et&#xa0;al., 2020</xref>). Taxonomic family and pollutant exposure were significant determinants of developmental abnormalities in a systematic review of ecotoxicological studies (<xref ref-type="bibr" rid="B37">Egea-Serrano et&#xa0;al., 2012</xref>), and specific phenotypical abnormalities can be ascribed to different classes of chemicals (<xref ref-type="bibr" rid="B170">Venturino et&#xa0;al., 2003</xref>).</p>
<p>Endocrine-driven developmental processes are highly conserved in vertebrates (<xref ref-type="bibr" rid="B112">Paul et&#xa0;al., 2022</xref>), as are many physiological endpoints associated with both homeostatic and lethal responses to pesticides and contaminant exposure. Larval amphibians are especially susceptible to endocrine disruption due to their reliance on hormonal cues for initiation and timing of metamorphosis and sex determination (<xref ref-type="bibr" rid="B36">Duarte-Guterman et&#xa0;al., 2014</xref>). Crosstalk between hormonal axes includes an evolutionary history of HPT and HPG signaling (<xref ref-type="bibr" rid="B158">Thambirajah et&#xa0;al., 2022</xref>). Genetic sex determination during developmental stages varies between and within amphibian species due to rapid turnover of genes such that either males or females can be heterozygotic, with some species having three sex chromosomes (<xref ref-type="bibr" rid="B99">Miura, 2017</xref>). Sex reversal in response to external temperature or steroid hormones can also affect the sex ratio of a cohort (<xref ref-type="bibr" rid="B124">Roco et&#xa0;al., 2021</xref>). Although estrogenic and androgenic effects have been studied much more extensively in mammals, intersex amphibian larvae resulting from reproductive steroid hormone exposure have been associated with effects on the androgen receptor (AR) and thyroid receptor (TR) and altered expression of dio1, dio2, dio3, and thrb (<xref ref-type="bibr" rid="B158">Thambirajah et&#xa0;al., 2022</xref>). Increased vitellogenin production is a common indication of feminization (<xref ref-type="bibr" rid="B169">Venturino and de D&#x2019;Angelo, 2005</xref>), and increased formic acid has been suggested as an indicator of androgen receptor binding and anti-androgenic effects in larvae (<xref ref-type="bibr" rid="B95">Melvin et&#xa0;al., 2018</xref>).</p>
<p>Endogenous changes in metabolism are also associated with lifecycle-dependent physiological processes (<xref ref-type="bibr" rid="B67">Ichu et&#xa0;al., 2014</xref>). During metamorphosis, metabolic pathways are dramatically altered in the liver and the tail as a result of lipid and carbohydrate metabolism (<xref ref-type="bibr" rid="B183">Zhu et&#xa0;al., 2020</xref>). Metabolomic changes during metamorphosis demonstrate physiological processes associated with morphological restructuring in metabolic pathways, including the urea cycle as well as arginine and purine/pyrimidine, cysteine/methionine, sphingolipid, and eicosanoid metabolism; however, similar metabolite expression in humans is associated with disease (<xref ref-type="bibr" rid="B67">Ichu et&#xa0;al., 2014</xref>). As the tadpole tail regresses and intestines restructure, lipid peroxidation is increased; depleted catalase (CAT) and glutathione contribute to oxidative stress, as demonstrated by CAT, superoxide dismutase (SOD), and malondialdehyde (MDA) expression; and the antioxidant ascorbic acid increases as organs develop (<xref ref-type="bibr" rid="B96">Menon and Rozman, 2007</xref>; <xref ref-type="bibr" rid="B55">Guo et&#xa0;al., 2022</xref>). Epidermal galactose levels, and specifically 25 uniquely expressed genes, are predictive of chytrid outbreaks and are life stage dependent, with higher expression at metamorphosis (<xref ref-type="bibr" rid="B176">Wang et&#xa0;al., 2021</xref>). Food constraints in the juvenile stage were associated with higher lipid peroxidase and lower SOD, glutathione S-transferase (GST), glutathione peroxidase, glutathione and sulfhydryl groups (<xref ref-type="bibr" rid="B119">Proki&#x107; et&#xa0;al., 2021</xref>).</p>
<p>Antioxidant system response (AOS) and oxidative stress is highest at metamorphic peak, and associated with lower glutathione, CAT, glutathione peroxidase, GST, and sulfhydryl groups, and oxidative stress is exacerbated by decreasing water levels (<xref ref-type="bibr" rid="B115">Petrovi&#x107; et&#xa0;al., 2021</xref>). Hepatic GST activity has been proposed as a biomarker indicative of TH signaling imbalance and developmental effects (<xref ref-type="bibr" rid="B28">Chen et&#xa0;al., 2017</xref>). Upregulated pathways include transamination and the urea cycle because of hepatic catabolism, TCA cycle and oxidative phosphorylation resulting from energy metabolism (although these are downregulated in the tail), and hepatic glycogen phosphorylation and gluconeogenesis (<xref ref-type="bibr" rid="B183">Zhu et&#xa0;al., 2020</xref>). Decreased activity occurred in &#x3b2;-oxidation and the pentose phosphate pathway, and downregulation of glycolysis, &#x3b2;-oxidation, and transamination in the tail accompanied reduced protein synthesis and lower energy production and consumption, although glycogenesis, fatty acid elongation and desaturation, and lipid synthesis were maintained (<xref ref-type="bibr" rid="B183">Zhu et&#xa0;al., 2020</xref>).</p>
<p>Indication of oxidative stress is a common detoxification response to many chemical classes and is characterized by altered expression of mixed function oxidases (MFO; e.g., CYP1A, EROD, demethylase), GSH, lipid peroxides, and antioxidant enzymes (CAT, SOD; <xref ref-type="bibr" rid="B169">Venturino and de D&#x2019;Angelo, 2005</xref>). Oxidative stress and lipid peroxidation, as demonstrated by increased SOD and CAT activity were also associated with hepatotoxicity resulting from increasing organophosphate exposure, although GST activity was unchanged, and MDA decreased (<xref ref-type="bibr" rid="B85">Li et&#xa0;al., 2017</xref>). Common indications of oxidative stress as a detoxification response include glutathione deficits and production of GST (<xref ref-type="bibr" rid="B169">Venturino and de D&#x2019;Angelo, 2005</xref>). Interactive oxidative stress effects of pesticide concentration and parasite abundance were observed in thiol levels of recent metamorphs, with nematode infection related to elevated thiol and catalase expression (<xref ref-type="bibr" rid="B88">Marcogliese et&#xa0;al., 2021</xref>).</p>
<p>Amphibian physiological responses to environmental stressors have been well documented (<xref ref-type="bibr" rid="B110">Park and Do, 2023</xref>), and the various threats that impact amphibian populations can elicit similar physical effects. For example, xenobiotic exposure or threatening environmental conditions (e.g., pond drying or predator presence) is commonly associated with oxidative stress and production of reactive oxygen species (ROS; <xref ref-type="bibr" rid="B23">Burraco et&#xa0;al., 2017</xref>). Habitat fragmentation and degradation, coincident with anthropogenic infringement and climate change, contribute to invasive species introduction, disease outbreak, and increased pollution, multiplying threats to immunocompetency (<xref ref-type="bibr" rid="B74">Kiesecker, 2011</xref>). Immune functions impacted by common amphibian stressors and their interactions are indicated in various matrices and measurements. For example, glucocorticoids (GC) are CS hormones influencing the immune system, tissue inflammation, and cardiovascular response (<xref ref-type="bibr" rid="B129">Rollins-Smith, 2017</xref>), and frequently indicate physiological stress. However, some stressors, e.g., food deprivation, can yield differential endocrine responses, with reduced CORT in juveniles conserving energy resources as opposed to increased CORT levels in food-deprived tadpoles (<xref ref-type="bibr" rid="B31">Crespi and Denver, 2005</xref>).</p>
</sec>
<sec id="s3_2">
<label>3.2</label>
<title>Omics technologies</title>
<p>Stressor-specific measurements of organismal response introduce complexity to both laboratory and field-based assessment approaches, as well as to the interpretation of multi-stressor scenarios. Evaluating biomarker expression can help identify biochemical perturbations indicative of systemic stress to environmental conditions. The suite of &#x2018;omics technologies, including genomics, transcriptomics, proteomics, and metabolomics, can shed light on the underlying biological processes and provide a means to identify specific genes, metabolites, and pathways that are affected in an amphibian ecological risk assessment.</p>
<p>Comparative genomics is increasingly recognized as a valuable tool for conservation purposes (<xref ref-type="bibr" rid="B79">Kosch et&#xa0;al., 2023</xref>). This includes the use of reference genomes in eDNA approaches for monitoring populations (<xref ref-type="bibr" rid="B17">Breton et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B138">Saeed et&#xa0;al., 2022</xref>), informing genetic rescue efforts for threatened amphibians (<xref ref-type="bibr" rid="B79">Kosch et&#xa0;al., 2023</xref>), and using sequence information to predict protein similarity and infer ecotoxicological implications across species (<xref ref-type="bibr" rid="B81">LaLone et&#xa0;al., 2023</xref>). However, compared to other vertebrate classes, genomic coverage for amphibians is currently recognized as lacking (<xref ref-type="bibr" rid="B64">Hotaling et&#xa0;al., 2021</xref>). <xref ref-type="bibr" rid="B79">Kosch et&#xa0;al. (2023)</xref> provided a review of the 32 available amphibian reference genomes and found variable annotation quality for the available genomes and uneven coverage across amphibian families, with genomic comparison further complicated by the presence of large, repetitive genomes. This limited availability of amphibian reference genomes presents challenges for generalizing ecotoxicological results to higher taxonomic levels within the class Amphibia. Despite these challenges, genetic approaches can provide conservation insights. This is particularly true for amphibian species with cryptic habits and biphasic life cycles, which complicate traditional field-based measurements of survival, fecundity, and migration (<xref ref-type="bibr" rid="B91">Mazerolle et&#xa0;al., 2007</xref>; <xref ref-type="bibr" rid="B47">Funk et&#xa0;al., 2021</xref>). Landscape genetics, for instance, can reveal connectivity within a population as well as isolated subpopulations (<xref ref-type="bibr" rid="B178">Watts et&#xa0;al., 2015</xref>). This information can then be used to prioritize conservation targets for threatened amphibians (e.g., <xref ref-type="bibr" rid="B45">Forester et&#xa0;al., 2022</xref>). The pressing need for increasing knowledge of amphibian genomes to assist in conservation efforts was highlighted by <xref ref-type="bibr" rid="B25">Calboli et&#xa0;al. (2011)</xref>. It is hypothesized that only a relative few, simple mechanisms of gene alterations are indicated in amphibians&#x2019; response to numerous environmental stressors. Functional genomics has been used to probe the molecular underpinnings of field observations concerning the sexual differentiation in amphibians (<xref ref-type="bibr" rid="B14">B&#xf6;gi et&#xa0;al., 2002</xref>), fragmentation of populations (<xref ref-type="bibr" rid="B93">McCartney-Melstad et&#xa0;al., 2018</xref>), and pathogen-host interactions (<xref ref-type="bibr" rid="B181">Zamudio et&#xa0;al., 2020</xref>).</p>
<p>In the laboratory, transcriptomics approaches leverage differential gene expression (DGE) approaches by contrasting the expression level of transcripts in stressed individuals versus control individuals. Changes in gene expression can reveal which genes are upregulated or downregulated, thereby identifying perturbations in specific biochemical pathways regardless of the origin of the stressor. The magnitude of the response could indicate functional points of departure (e.g., <xref ref-type="bibr" rid="B40">Ewald et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B98">Mittal et&#xa0;al., 2022</xref>). Transcriptomics data, generated from controlled laboratory exposures, provide a comprehensive view of gene expression changes comparable to traditional apical endpoints. The large volume of data, coupled with the fact that the expression responses are specifically associated with the mechanism of the stressor, suggests the possibility of developing expression-based &#x201c;fingerprints&#x201d; or signatures resulting from single and multi-stressor exposures. These can be used to determine if the magnitude of an exposure to a toxicant or stressor of a particular mode of action is likely to elicit biological perturbations that can be linked to or predictive of apical effects. Furthermore, high-throughput transcriptomics (HTTr) methods have been developed to observe changes in gene expression in cells, rather than in test species, after exposure to chemicals (<xref ref-type="bibr" rid="B143">Schirmer et&#xa0;al., 2010</xref>). These methods are less resource-intensive than traditional toxicity testing and can be used to determine at what concentration chemicals impact cellular biology and to develop adverse outcome pathways (AOPs). For vertebrates, such regulatory testing programs aim to evaluate the potential endocrine-disrupting effects of chemicals, utilizing the conservation of certain endocrine pathways among vertebrate classes to evaluate the feasibility of extrapolating data across taxa. These approaches integrate functional genomics with transcriptomics to establish the confidence levels in pathway conservation while identifying the specific needs for additional data to advance read-across methods for estrogen, androgen, thyroid, and steroidogenesis pathways in vertebrate ecological receptors (<xref ref-type="bibr" rid="B92">McArdle et&#xa0;al., 2020</xref>).</p>
<p>Metabolomics technology may also provide a means to address the uncertainties surrounding chemical risk assessment of single and multiple stressors. Available technology measures the changes in hundreds (if not thousands) of metabolites simultaneously, effectively capturing a metabolomic fingerprint as a snapshot of an organism&#x2019;s altered physiology. This metabolomic fingerprint of subcellular biological responses often represents immediate or early response within the organism to stresses and can be associated with signaling networks that are linked to adverse outcomes at higher levels of biological organization. Successful application of metabolomics to differentiate multi-stressor response was achieved by <xref ref-type="bibr" rid="B149">Snyder et&#xa0;al. (2022)</xref>. Similarly, the use of transcriptomics and proteomics for advancing amphibian toxicogenomic studies was reviewed in <xref ref-type="bibr" rid="B61">Helbing (2012)</xref>. Relying on &#x2018;omics technologies to identify meaningful suites of stressor response and target demographic vulnerabilities for sample collection could offer a comparative physiology approach for detecting impacted individuals and populations.</p>
<p>Exogenous impacts of xenobiotic exposure can exacerbate stressors that accompany particular life stages. Reduction in body size during metamorphosis and fasting during hibernation result in increased metabolic demands and greater body burdens of contaminants due to biomagnification (<xref ref-type="bibr" rid="B131">Rowland et&#xa0;al., 2023</xref>). Aquatic exposures of various pesticides were associated with increased galactose metabolism and lactose degradation, indicating effects on energy metabolism (<xref ref-type="bibr" rid="B51">Glinski et&#xa0;al., 2021</xref>). Pathways associated with glucogenesis and glycolysis were also indicators of energy metabolism impacts in terrestrial juvenile frog exposures (<xref ref-type="bibr" rid="B166">Van Meter et&#xa0;al., 2022</xref>). The urea cycle was frequently impacted by various pesticides, and the purine metabolism pathway was also enriched, indicating increased energy production as a response to toxicity. Reduction in glutathione levels is another common result of pesticide exposure indicative of oxidative stress in both larval and juvenile amphibians (<xref ref-type="bibr" rid="B67">Ichu et&#xa0;al., 2014</xref>). Reduced citrate, &#x3b1;-ketaglutarate, and fumarate were also proposed as oxidative stress biomarkers, as intermediates of the tricarboxylic acid cycle (<xref ref-type="bibr" rid="B95">Melvin et&#xa0;al., 2018</xref>).</p>
<p>The magnitude of altered metabolite regulation during later life stage terrestrial exposures was not indicative of bioaccumulation, and exposure to combinations of pesticide did not always have a synergistic effect on juvenile toads (<xref ref-type="bibr" rid="B165">Van Meter et&#xa0;al., 2018</xref>). In fact, extrinsic sources of urea as fertilizer at low concentrations can counteract combined pesticide effects, presumably by facilitating excretion and detoxification, although excessive doses can be detrimental (<xref ref-type="bibr" rid="B166">Van Meter et&#xa0;al., 2022</xref>). Hepatic metabolome analyses revealed altered pathways indicating stress caused by both predation and pesticide exposure; these include aminoacyl-tRNA biosynthesis, galactose metabolism, glutathione metabolism, and arginine biosynthesis (<xref ref-type="bibr" rid="B149">Snyder et&#xa0;al., 2022</xref>). Transgenerational fertility effects of endocrine disruption due to pesticide exposure were associated with greater mass, increased palmitoleic:palmitic acid ratio, and decreased glucose (<xref ref-type="bibr" rid="B71">Karlsson et&#xa0;al., 2021</xref>). As studies of multistressor deviations from normal metabolite activity continue, identification of meaningful pathway perturbations could provide a systematic method of identifying locations of environmental impacts without prerequisite knowledge of specific land use changes or fate and exposure of particular pollutants.</p>
</sec>
<sec id="s3_3">
<label>3.3</label>
<title>Sampling strategies</title>
<p>Traditional measures of contaminant impacts on amphibians focus on body burden concentrations and somatic indices of body condition (e.g., <xref ref-type="bibr" rid="B5">B&#x103;ncil&#x103; et&#xa0;al., 2010</xref>) as well as general indicators of genotoxic and mutagenic impacts (i.e., comet and micronucleus assays) and more targeted analyses of cellular-level endpoints. For larger taxa (e.g., birds and mammals), marking individuals and collecting tissue samples can be a routine, noninvasive procedure conducted in the field to inform physiological condition. However, the small body size of amphibians hinders repeated sampling of blood or plasma for various analyses. For smaller amphibians, sampling techniques might involve toe-clipping for both individual identification as well as tissue collection, or sample collection might require sacrifice of individuals, particularly at earlier life stages.</p>
<p>Many common assays measure hematological enzymatic responses typical of exposure to specific xenobiotic contaminants (<xref ref-type="bibr" rid="B109">Ohmer et&#xa0;al., 2021</xref>). For example, esterase activity (acetylcholinesterase, butyryl cholinesterase, and carboxyl esterase) can indicate potential developmental effects, but response varies greatly within and between species (<xref ref-type="bibr" rid="B170">Venturino et&#xa0;al., 2003</xref>; <xref ref-type="bibr" rid="B169">Venturino and de D&#x2019;Angelo, 2005</xref>). Hematological measures representative of immune response include leukocytes, neutrophil/lymphocyte ratio, bacterial killing assays, and delayed hypersensitivity assays (<xref ref-type="bibr" rid="B109">Ohmer et&#xa0;al., 2021</xref>). Changes in neutrophils and lymphocytes are often proportional with increased glucocorticoid levels, indicating physiological stress; however, neonicotinoid exposure altered leukocyte profiles relative to neutrophils or eosinophils but did not affect CORT levels in northern leopard frogs (<xref ref-type="bibr" rid="B50">Gavel et&#xa0;al., 2021</xref>). Neutrophil to lymphocyte ratios were also a good indication of environmental stressors and were associated with total dissolved solid levels in aquatic habitats that impacted growth and development (<xref ref-type="bibr" rid="B134">Ruso et&#xa0;al., 2021</xref>). Combinations of physiological indices are also informative to link endpoints with individual condition (e.g., <xref ref-type="bibr" rid="B111">Park et&#xa0;al., 2021</xref>).</p>
<p>Several minimally or non-invasive techniques that may be more effective for amphibians are now routinely used including urinalysis, fecal sampling, waterborne sampling, salivary swabs, and dermal swabs (<xref ref-type="bibr" rid="B104">Narayan et&#xa0;al., 2019</xref>). Among these techniques, saliva has only been validated in adults and not juveniles. <xref ref-type="bibr" rid="B68">Janin et&#xa0;al. (2012)</xref> concluded that CORT concentrations in saliva were highly correlated with urine measurements in toads. Urinalysis has been previously used to track endocrine response such as the reproductive hormones estradiol, progesterone, and testosterone within both captive and wild caught amphibians (<xref ref-type="bibr" rid="B102">Narayan, 2013</xref>). Additionally, CORT levels can be quantified from urine to identify differences in stress response due to predation risk or pathogen prevalence (<xref ref-type="bibr" rid="B75">Kindermann et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B104">Narayan et&#xa0;al., 2019</xref>). While urine samples have the distinct advantage of being highly concentrated for measuring endocrine functions along with physiological stress, the method is not always ideal for smaller amphibians producing lower volumes (<xref ref-type="bibr" rid="B102">Narayan, 2013</xref>; <xref ref-type="bibr" rid="B8">Baugh et&#xa0;al., 2018</xref>).</p>
<p>Another minimally invasive technique for endocrine analysis for amphibians of any size is immersing the individual in a clean container of water for a designated length of time, after which the released hormones can be quantified from the water. Most studies have used this technique to measure CORT release rates, which have been validated with circulating plasma levels (<xref ref-type="bibr" rid="B48">Gabor et&#xa0;al., 2013a</xref>). Waterborne sampling has evaluated CORT release rates in the presence or absence of <italic>Bd</italic>, predation, or pesticide exposure (<xref ref-type="bibr" rid="B49">Gabor et&#xa0;al., 2013b</xref>; <xref ref-type="bibr" rid="B164">Van Meter et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B149">Snyder et&#xa0;al., 2022</xref>) and can also be indicative of nitrate stress in amphibians (<xref ref-type="bibr" rid="B135">Ruthsatz et&#xa0;al., 2023</xref>). CORT is a potentially useful biomarker for amphibians to indicate stress, and non-invasive sampling methods offer the potential of serially sampling the same individual (<xref ref-type="bibr" rid="B104">Narayan et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B161">Tornabene et&#xa0;al., 2021</xref>). Therefore, within a short timeframe baseline values and acute elevation in CORT are quantifiable (<xref ref-type="bibr" rid="B58">Hammond et&#xa0;al., 2018</xref>). <xref ref-type="bibr" rid="B155">Szymanski et&#xa0;al. (2006)</xref> collected feces of adult anurans to quantify reproductive hormones, enabling sex identification. In addition to CORT, two other reproductive hormones, progesterone and estradiol, have also been quantified in water from amphibians (<xref ref-type="bibr" rid="B8">Baugh et&#xa0;al., 2018</xref>).</p>
<p>While dermal swabbing is most notable for detecting the presence of pathogens in amphibians (e.g., <xref ref-type="bibr" rid="B152">Standish et&#xa0;al., 2018</xref>), more recent studies have expanded on what can be tested in amphibian mucus, such as DNA collection and glucocorticoids (<xref ref-type="bibr" rid="B118">Poorten et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B104">Narayan et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B140">Santymire et&#xa0;al., 2021</xref>). A lab-based salamander study examined the difference between liver metabolomics and dermal swab metabolomics, to determine if similar pathways are impacted in the presence of pesticides, measuring for presence/absence of pathogens and glutathione as well (<xref ref-type="bibr" rid="B167">Van Meter et&#xa0;al., in press</xref>). Dermal swabs enable <italic>in situ</italic> field sampling with minimal handing time, which is particularly advantageous for threatened and endangered species and allows serial sampling of the same individual or environment (<xref ref-type="bibr" rid="B139">Santymire et&#xa0;al., 2018</xref>, <xref ref-type="bibr" rid="B140">2021</xref>; <xref ref-type="bibr" rid="B142">Scheun et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B161">Tornabene et&#xa0;al., 2021</xref>).</p>
<p>Sampling techniques that are well-established at the individual level can also provide a comparison, through DGE or hepatic metabolites, of localized stressor response indicative of differential population-level effects. Such response-based metrics could preclude the necessity to anticipate synergies, compensation, and interactions between ubiquitous stressors that might be heterogeneously distributed. Rather than spatially explicit analysis of stressors within the species distribution, identifying variance in relative response within the population could target conservation concerns more rapidly within a diverse landscape while accounting for baseline fluxes in physiology. For example, the complex physiological changes during metamorphosis comprise endocrine interactions and changes in energy allocation as tail resorption and leg growth occurs, such that tissues sampled could vary in the cellular-level activity. Stage-specific fluxes in endocrine activity also affect response observed in individuals, such that standardizing measurements within consistent developmental stages is advisable when sampling larvae. Field-based observations could also be influenced by the environment of the individuals, making observations about water quality, larval density, and community composition relevant to evaluating stress response. As measures of individual response are considered within appropriate life stage time points, comparable evaluation of location-specific perturbations in baseline physiological functions can guide more targeted conservation actions.</p>
</sec>
</sec>
<sec id="s4" sec-type="discussion">
<label>4</label>
<title>Discussion</title>
<p>As amphibians are impacted by multiple stressors and their interactions, the capability to assess cumulative impacts on biochemical pathways within an organism&#x2019;s native habitat facilitates quantification of exposure risk and possible additive or synergistic effects. However, even at the organismal level, amphibians often lack sufficient toxicology data for evaluation of cellular-level responses (<xref ref-type="bibr" rid="B90">Marlatt and Martyniuk, 2017</xref>), and variance in individual response and chronic exposure obscure definitive metrics of detrimental effects on the population. Additional research is needed to identify reliable biomarkers that are consistently indicative of points of departure from normal cellular function in response to environmental stressors. Standardized indices of biomarker perturbations in response to stressors enables identification of reliable predictors of long-term impacts (<xref ref-type="bibr" rid="B116">Pham and Sokolova, 2023</xref>); however, caution must be taken to verify cellular responses are linked to demographic effects, rather than a homeostatic response to stressors (<xref ref-type="bibr" rid="B44">Forbes et&#xa0;al., 2006</xref>). Evaluating potential threats linked to synergistic exposure effects (e.g., reduced dermal microbiota) or multiple exposure routes (i.e., aquatic and terrestrial) requires situation-specific ecological context. Implementation of weight of evidence effects could further classify cumulative threat levels of variable biomarker responses (<xref ref-type="bibr" rid="B27">Cecchetto et&#xa0;al., 2023</xref>). An initial step towards multi-stressor risk assessment is outlined here, namely by exploring stage-specific variance in biochemical pathways and identifying points of physiological vulnerability in the life cycle as a screening-level conservation approach.</p>
</sec>
<sec id="s5" sec-type="author-contributions">
<title>Author contributions</title>
<p>JA: Writing &#x2013; review &amp; editing, Writing &#x2013; original draft, Conceptualization. DG: Writing &#x2013; review &amp; editing. WH: Writing &#x2013; review &amp; editing. RM: Writing &#x2013; review &amp; editing. SP: Writing &#x2013; review &amp; editing.</p>
</sec>
</body>
<back>
<sec id="s6" 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>
<ack>
<title>Acknowledgments</title>
<p>Authors thank Jon Haselman and Sandy Raimondo as well as the two reviewers for suggestions on previous drafts.</p>
</ack>
<sec id="s7" 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="s8" 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>
<ref-list>
<title>References</title>
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