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<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title>Frontiers in Plant Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Plant Sci.</abbrev-journal-title>
<issn pub-type="epub">1664-462X</issn>
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<publisher-name>Frontiers Media S.A.</publisher-name>
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<article-meta>
<article-id pub-id-type="doi">10.3389/fpls.2024.1506418</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Assessing the establishment risk for parthenogenetic populations of <italic>Lissorhoptrus oryzophilus</italic> in global rice-growing areas and potential economic impact in China</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Li</surname>
<given-names>Luoyuan</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup>&#x2020;</sup>
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<contrib contrib-type="author">
<name>
<surname>Jin</surname>
<given-names>Zhenan</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup>&#x2020;</sup>
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<contrib contrib-type="author">
<name>
<surname>Li</surname>
<given-names>Ming</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
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<name>
<surname>Xue</surname>
<given-names>Yantao</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
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<contrib contrib-type="author">
<name>
<surname>Guo</surname>
<given-names>Jianyang</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
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<contrib contrib-type="author">
<name>
<surname>Jia</surname>
<given-names>Dong</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
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<contrib contrib-type="author">
<name>
<surname>Ma</surname>
<given-names>Ruiyan</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
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<contrib contrib-type="author">
<name>
<surname>L&#xfc;</surname>
<given-names>Zhichuang</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
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<contrib contrib-type="author" corresp="yes">
<name>
<surname>Xian</surname>
<given-names>Xiaoqing</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
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<contrib contrib-type="author" corresp="yes">
<name>
<surname>Liu</surname>
<given-names>Wanxue</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
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<aff id="aff1">
<sup>1</sup>
<institution>College of Plant Protection of Shanxi Agricultural University</institution>, <addr-line>Jinzhong</addr-line>, <country>China</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences</institution>, <addr-line>Beijing</addr-line>, <country>China</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Xiao Ming Zhang, Yunnan Agricultural University, China</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Prashant Sharma, Dr. Yashwant Singh Parmar University of Horticulture and Forestry, India</p>
<p>Michael J. Stout, Louisiana State University, United States</p>
<p>Daniela Lupi, University of Milan, Italy</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Wanxue Liu, <email xlink:href="mailto:liuwanxue@caas.cn">liuwanxue@caas.cn</email>; Xiaoqing Xian, <email xlink:href="mailto:xianxiaoqing@caas.cn">xianxiaoqing@caas.cn</email>
</p>
</fn>
<fn fn-type="other" id="fn003">
<p>&#x2020;These authors share first authorship</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>22</day>
<month>01</month>
<year>2025</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>15</volume>
<elocation-id>1506418</elocation-id>
<history>
<date date-type="received">
<day>05</day>
<month>10</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>16</day>
<month>12</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2025 Li, Jin, Li, Xue, Guo, Jia, Ma, L&#xfc;, Xian and Liu</copyright-statement>
<copyright-year>2025</copyright-year>
<copyright-holder>Li, Jin, Li, Xue, Guo, Jia, Ma, L&#xfc;, Xian and Liu</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 rice water weevil, <italic>Lissorhoptrus oryzophilus</italic> Kuschel (Coleoptera: Curculionidae), threatens global rice production, with invasion events driven by its parthenogenetic populations. However, the global establishment risk in global rice-growing areas and potential economic losses and control benefits of the populations in invaded areas remain unclear. We applied an optimized MaxEnt model to predict the global suitable areas of the populations under current and future climate scenarios. Furthermore, we used @Risk software to estimate the potential economic losses and controlling benefit of this populations to rice production in China. Compared to its native range (North America), this populations has explored novel climates ecological niches in invaded areas (Europe and Asia) and occupies the broadest range of climatic ecological niches in Asia. The highly suitable area is primarily covered in rice-growing areas in China, the Korean Peninsula, and Japan, with all major rice-growing areas concentrated in these countries and regions. Under SSP1-2.6 and SSP5-8.5 emission scenarios, sum of suitable area for the populations in global rice-growing regions is projected to decrease by 0.35% and 0.26%, respectively, by the 2030s and 2050s. Moreover, @Risk analysis indicates that without control measures, the populations could cost China&#x2019;s rice industry $18.95 billion, but management efforts could recover $17.54 billion. These results provide in-depth reference about the impact of climatic changes on the potential global suitable range of <italic>L. oryzophilus</italic> parthenogenetic populations and its economic impact on the rice industry in China.</p>
</abstract>
<kwd-group>
<kwd>invasive alien pest</kwd>
<kwd>
<italic>Lissorhoptrus oryzophilus</italic> parthenogenetic populations</kwd>
<kwd>suitable area</kwd>
<kwd>ecological niche</kwd>
<kwd>potential economic loss</kwd>
</kwd-group>
<contract-num rid="cn001">2022YFC2601400</contract-num>
<contract-sponsor id="cn001">National Key Research and Development Program of China<named-content content-type="fundref-id">10.13039/501100012166</named-content>
</contract-sponsor>
<counts>
<fig-count count="6"/>
<table-count count="3"/>
<equation-count count="5"/>
<ref-count count="94"/>
<page-count count="15"/>
<word-count count="7604"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Sustainable and Intelligent Phytoprotection</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<label>1</label>
<title>Introduction</title>
<p>The advent of globalization and the concomitant enhancement of connectivity through international trade and the frequent movement of agricultural commodities has led to an increase in the incidence of invasive alien pests (IAPs) (<xref ref-type="bibr" rid="B82">Vil&#xe0; et&#xa0;al., 2011</xref>). These present a substantial economic risk to worldwide agricultural crops, causing considerable losses and having a detrimental impact on human livelihoods (<xref ref-type="bibr" rid="B12">Cardinale et&#xa0;al., 2006</xref>; <xref ref-type="bibr" rid="B14">Daehler, 2003</xref>). A multitude of IAPs have undergone rapid evolutionary changes within their novel environments, driven by a combination of factors including genotype sorting, genetic recombination, interspecies hybridization, and natural selection. These changes have also occurred in response to the unique climatic conditions that they have encountered in their new habitats. (<xref ref-type="bibr" rid="B28">Guisan et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B74">Sexton et&#xa0;al., 2017</xref>). Notably, the IAPs with parthenogenetic reproduction have accelerated their spread and establishment in new environments due to their high adaptability and low energy consumption in reproduction (<xref ref-type="bibr" rid="B25">Graziosi and Rieske, 2014</xref>). Additionally, the impacts of climate change will lead to the higher rates, severity, damage, voltinism and geographic spread of IAPs to profound impact on agriculture production (<xref ref-type="bibr" rid="B29">Harrington et&#xa0;al., 2007</xref>; <xref ref-type="bibr" rid="B31">Hill et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B70">Ramasamy et&#xa0;al., 2022</xref>). To measure this threat and create effective biosecurity policies, it is essential to comprehend the origins of IAPs, their chances of establishing themselves in novel region, the region of establishing under climate change, and their possible economic impact in invaded areas. Therefore, assessing the distribution of globally suitable areas for IAPs under climate change, as well as estimating potential economic losses to staple crops in invaded areas and the benefits of control measures, is crucial for formulating pest management strategies to safeguard global food security (<xref ref-type="bibr" rid="B52">Ma and Ma, 2022</xref>).</p>
<p>
<italic>Lissorhoptrus oryzophilus</italic> Kuschel (Coleoptera: Curculionidae) is native to the southern and eastern United States (<xref ref-type="bibr" rid="B2">Aghaee and Godfrey, 2014</xref>). In the southern region of Texas, bisexual and parthenogenetic populations of <italic>L. oryzophilus</italic> are present, but in California, only the parthenogenetic populations has been found to posed a huge threat to local rice production (<xref ref-type="bibr" rid="B37">Jiang et&#xa0;al., 2008</xref>; <xref ref-type="bibr" rid="B3">Aghaee and Godfrey, 2015</xref>). The adult weevils feed on rice leaves and lay their eggs after the fields are flooded, while the larvae feed on the roots, leading to poor root development, seeds dislodgement and reduced grain yields (<xref ref-type="bibr" rid="B26">Grigarick and Beards, 1965</xref>; <xref ref-type="bibr" rid="B94">Zou et&#xa0;al., 2004</xref>). <italic>L. oryzophilus</italic> is renowned for its highly invasive nature due to its ability to spread through a variety of mechanisms, including airborne dispersal, flight, swimming, and human-mediated transport. Additionally, it exhibits a great poliphagy (consuming a wide range of wild grasses) and adapts through various overwintering strategies (utilizing substrates like bunchgrass and leaf litter) (<xref ref-type="bibr" rid="B13">Chen et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B72">Saito et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B1">Adams et&#xa0;al., 2015</xref>). It is also important to recognize that a single individual is theoretically enough to initiate a new infestation due to its parthenogenetic reproduction in invaded areas (<xref ref-type="bibr" rid="B72">Saito et&#xa0;al., 2005</xref>). In the latter half of the 20th century, its parthenogenetic populations became world populations and invaded several high-yielding rice cultivation areas worldwide, including Europe (Italy), East Asia (Japan, China, South Korea and North Korea) and South Asia (India), causing significant economic losses in local agricultural production (<xref ref-type="bibr" rid="B32">Huang et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B51">Lupi et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B72">Saito et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B21">Ferrero, 2005</xref>; <xref ref-type="bibr" rid="B23">Giantsis et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B50">Lupi et&#xa0;al., 2010</xref>). These invasion events demonstrate that the <italic>L. oryzophilus</italic> females have a strong adaptive capability to new climatic environments (<xref ref-type="bibr" rid="B72">Saito et&#xa0;al., 2005</xref>; <xref ref-type="bibr" rid="B10">Caldara et&#xa0;al., 2004</xref>; <xref ref-type="bibr" rid="B51">Lupi et&#xa0;al., 2015</xref>). Previous studies have used CLIMEX to predict the suitable areas for this populations in China based on its biological characteristics and environmental adaptations (<xref ref-type="bibr" rid="B54">Mao et&#xa0;al., 1997</xref>). <xref ref-type="bibr" rid="B67">Qi et&#xa0;al. (2012)</xref> used MaxEnt to explored the suitable areas of the populations in rice-growing areas in China. <xref ref-type="bibr" rid="B87">Xie et&#xa0;al. (2022)</xref> predicted the suitable areas of the populations under current and future climatic conditions by MaxEnt. However, as a widely prevalent invasive populations globally, the establishment risk of this populations in global rice cultivation areas remain unknown, and there have been no quantitative assessments reported regarding the regional potential economic losses and control benefits in invaded areas, especially in China where there is high dependence on rice supply (<xref ref-type="bibr" rid="B6">Bin Rahman and Zhang, 2023</xref>). It is essential to predict the suitable areas of <italic>L. oryzophilus</italic> parthenogenetic populations in global rice growing areas under climate change conditions so that targeted management and control measures to mitigate increasing losses.</p>
<p>Species distribution models (SDMs) use environmental variables from known species locations to predict their distributions and ecological needs; these models are commonly applied in invasion biology, conservation biology, global change biology, and pathogen risk assessments (<xref ref-type="bibr" rid="B69">Raffini et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B66">Pili et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B44">Larson and Olden, 2012</xref>). The MaxEnt model combines machine learning with the principle of maximum entropy, and it is widely used in invasive species risk assessment due to its flexibility and ease of interpretation (<xref ref-type="bibr" rid="B65">Phillips and Dud&#xed;k, 2008</xref>; <xref ref-type="bibr" rid="B19">Elith et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B40">Jin et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B91">Yang et&#xa0;al., 2022</xref>). The ecological niche shifts of IAPs in invaded habitats have been extensively documented (<xref ref-type="bibr" rid="B74">Sexton et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B28">Guisan et&#xa0;al., 2014</xref>). Understanding the ecological niche characteristics occupied by invasive species in invaded areas also provides new insights into their impacts. The n-dimensional hypervolume framework has been used to build and compare ecological niche characteristics, which are more comprehensive than two-dimensional methods that condense multiple niche variables into principal components (<xref ref-type="bibr" rid="B8">Blonder et&#xa0;al., 2018</xref>, <xref ref-type="bibr" rid="B7">2014</xref>). Multidimensional methods provide a fuller depiction of niche differences by capturing all variability across niche dimensions (<xref ref-type="bibr" rid="B63">Pack et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B66">Pili et&#xa0;al., 2020</xref>). Additionally, we are interested in exploring changes in niche characteristics of specific variables related to the environmental suitability of <italic>L. oryzophilus</italic> parthenogenetic populations. This is feasible within the n-dimensional framework, as centroids for each niche dimension can be computed, further quantifying how species differ across various environmental factors during the invasion process. Typically, predictions of potential economic losses caused by harmful organisms rely on @RISK software, which utilizes Monte Carlo stochastic simulation methods. By constructing models of potential economic losses under different scenarios and simulating outcomes using various probability distributions, @RISK software can estimate the potential economic impact of harmful organisms (<xref ref-type="bibr" rid="B46">Li and Qin, 2018</xref>). Previous studies have used @RISK software to predict the potential economic losses and control costs caused by <italic>Bactrocera cucurbitae</italic> and <italic>Spodoptera frugiperda</italic> on host plants in China (<xref ref-type="bibr" rid="B77">Sun et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B68">Qin et&#xa0;al., 2020</xref>). Given that China is the largest rice producer globally (<ext-link ext-link-type="uri" xlink:href="https://www.fao.org/">https://www.fao.org/</ext-link>), this study aims to utilize the @RISK stochastic model to assess the potential economic impact of <italic>L. oryzophilus</italic> parthenogenetic populations on China&#x2019;s rice industry.</p>
<p>Despite extensive efforts both domestically and internationally in developing quantitative risk assessment models and software for IAP, existing models and software to date cannot independently achieve comprehensive assessments covering the invasion potential, suitable areas, and potential economic losses from IAPs (<xref ref-type="bibr" rid="B46">Li and Qin, 2018</xref>). Therefore, it is necessary to integrate these models and software organically in IAPs risk analysis framework (<xref ref-type="bibr" rid="B46">Li and Qin, 2018</xref>). We construct a new framework for global establishment risk assessment of <italic>L. oryzophilus</italic> parthenogenetic populations (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S1</bold>
</xref>). Specifically, (1) reconstruct the invasion history of the populations across recorded countries; (2) identify significant environmental variables affecting the suitable areas of the populations; (3) predict the suitable areas of the populations in global rice-growing areas under two climate change conditions; (4) construct ecological niche characterizations for North America, Europe, and Asia using four major bioclimatic factors that largely impact model results to characterize ecological differences in suitable habitats for the populations. (5) evaluate the potential economic losses of the populations to rice industry under unmanaged scenario and managed scenario.</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>Species distribution record</title>
<p>We obtained global occurrence records of <italic>L. oryzophilus</italic> parthenogenetic populations from the Global Biodiversity Information Facility (<ext-link ext-link-type="uri" xlink:href="https://www.gbif.org/">https://www.gbif.org/</ext-link>; accessed on February 7, 2023 <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.15468/dl.tnzme5">https://doi.org/10.15468/dl.tnzme5</ext-link>), Bold Systems v4 (<ext-link ext-link-type="uri" xlink:href="http://www.boldsystems.org/">http://www.boldsystems.org/</ext-link>; accessed on February 21, 2023) and published literature (China National Knowledge Infrastructure: <ext-link ext-link-type="uri" xlink:href="https://www.cnki.net">https://www.cnki.net</ext-link>; Web of Science, <ext-link ext-link-type="uri" xlink:href="https://www.webofscience.com/">https://www.webofscience.com/</ext-link>; accessed on May 9, 2023). A total of 1991 global occurrence records for <italic>L. oryzophilus</italic> parthenogenetic populations were collected. Most of the sampling points are concentrated in central and northeastern China, as well as mainland Japan. Only a few samples have been recorded in the eastern and southern United States, and southern Europe. To avoid spatial redundancy of the sample points, we also used ENMTools to eliminate spatial autocorrelation by screening occurrence records, ensuring each raster retained a single occurrence record (<xref ref-type="bibr" rid="B84">Warren et&#xa0;al., 2010</xref>). Finally, 1500 occurrence records of <italic>L. oryzophilus</italic> parthenogenetic populations were retained for constructing the MaxEnt model (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>).</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Global occurrence sampling points of <italic>Lissorhoptrus oryzophilus</italic> parthenogenetic populations.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1506418-g001.tif"/>
</fig>
<p>We reconstruct parthenogenetic and bisexual populations of <italic>L. oryzophilus</italic> invasion history in native (the United States) and invasive range based on the time of the first reported in EPPO Global Database (<ext-link ext-link-type="uri" xlink:href="https://www.eppo.int/">https://www.eppo.int/</ext-link>; accessed on February 21, 2023) and the literature for different invasive region (Web of Science, <ext-link ext-link-type="uri" xlink:href="https://www.webofscience.com/">https://www.webofscience.com/</ext-link>; accessed on May 9, 2023) (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S1</bold>
</xref>). For the first occurrence records of <italic>L. oryzophilus</italic> in different provinces of China, we conducted a detailed search based on CNKI (China National Knowledge Infrastructure: <ext-link ext-link-type="uri" xlink:href="https://www.cnki.net">https://www.cnki.net</ext-link>) and the National Agricultural Plant Quarantine Pests Distribution Administrative Region Directory (<ext-link ext-link-type="uri" xlink:href="http://www.moa.gov.cn">www.moa.gov.cn</ext-link>) (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S1</bold>
</xref>). All the countries, provinces and states with documented first reported are visualized using different colors in ArcGIS 10.8 software.</p>
</sec>
<sec id="s2_2">
<label>2.2</label>
<title>Environmental variables</title>
<p>For climatic parameters, we obtained 19 bioclimatic factors (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S2</bold>
</xref>) and altitude variables from the World Climate Database (<ext-link ext-link-type="uri" xlink:href="http://www.worldclim.org/">http://www.worldclim.org/</ext-link>; accessed on October 3, 2022) at a resolution of 5 arc-min (10.0 km resolution at the equator). These 19 bioclimatic factors were derived from minimum temperature, maximum temperature, and precipitation data from 1970 to 2000 to create suitability maps under current climate conditions. We also incorporated the HII (Human Influence Index (<ext-link ext-link-type="uri" xlink:href="https://beta.sedac.ciesin.columbia.edu/data/set/wildareas-v2-human-influence-index-geographic">https://beta.sedac.ciesin.columbia.edu/data/set/wildareas-v2-human-influence-index-geographic</ext-link>)) into our model. To avoid model overfitting, we used the ENMTools to examine correlations among 21 predictor variables and remove highly correlated environmental factors (| <italic>r</italic> |&lt; 0.8, Pearson) to reduce the collinearity between predictor variables (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S2</bold>
</xref>) (<xref ref-type="bibr" rid="B24">Graham, 2003</xref>; <xref ref-type="bibr" rid="B20">Favretti, 2018</xref>). Finally, the ten predictor variables were chosen based on their importance for the MaxEnt model: mean diurnal range (Bio 2), temperature seasonality (Bio 4), mean temperature of warmest Quarter (Bio10), precipitation of driest month (Bio 14), precipitation seasonality (Bio 15), precipitation of wettest quarter (Bio 16), precipitation of warmest quarter (Bio 18), precipitation of coldest quarter (Bio 19), altitude (Alt) and Human Influence Index (HII) (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S3</bold>
</xref>).</p>
<p>We also obtained bioclimatic variables were from the Beijing Climate Center Climate System Model (BCC-CSM2-MR) (<ext-link ext-link-type="uri" xlink:href="http://www.worldclim.org/">http://www.worldclim.org/</ext-link>; accessed on October 3, 2022), developed by the National Climate Center based on the CMIP6 of the sixth assessment report (AR6) of the Intergovernmental Panel on Climate Change (IPCC). Compared to BCC-CSM1.1m, the BCC-CSM2-MR shows notable advancements in tropospheric temperature and circulation on global and East Asian scales, as well as in climate variability across different time scales (<xref ref-type="bibr" rid="B86">Wu et&#xa0;al., 2019</xref>). In our study, SSP1-2.6 (low-emission scenario) and SSP5-8.5 (high-emission scenario) in the 2030s (average of 2041&#x2013;2060) and 2050s (average of 2041&#x2013;2060) were included to predict the suitable areas under future climatic conditions.</p>
</sec>
<sec id="s2_3">
<label>2.3</label>
<title>Model optimization and parameterization</title>
<p>The default parameter settings in MaxEnt can lead to models that are either overly complex or too simplistic (<xref ref-type="bibr" rid="B85">Warren and Seifert, 2011</xref>). Therefore, the alternative combinations of feature classes (FCs) and regularization multipliers (RMs) optimization of the MaxEnt model was conducted using the ENMeval package in the R software to obtain appropriate parameter settings (<xref ref-type="bibr" rid="B60">Morales et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B61">Muscarella et&#xa0;al., 2014</xref>). The MaxEnt model has five basic features: linear (L), quadratic (Q), hinge (H), product (P), and threshold (T) (<xref ref-type="bibr" rid="B73">Santana et&#xa0;al., 2019</xref>). We set five parameter combinations for these five arithmetic features as L, LQ, H, LQH, and LQHP (<xref ref-type="bibr" rid="B61">Muscarella et&#xa0;al., 2014</xref>). The regularization multipliers were set from 0.5 to 6, with a 0.5 interval, resulting in 60 combinations of model parameters.</p>
<p>We selected the minimum values of delta Akaike information criterion correction (&#x394;AICc) as criteria (<xref ref-type="bibr" rid="B36">Jarnevich et&#xa0;al., 2015</xref>). A model with a lower AICc score indicates lower complexity and better fit, making it the preferred choice. Thus, select the model with the minimum &#x394;AICc value (choose &#x394;AICc = 0) to build the final MaxEnt model. The FC parameters were set as LQHP with a regularization multiplier of 0.5. The global occurrence records of <italic>L. oryzophilus</italic> were divided, and 75% and 25% were selected as the training and testing datasets, respectively (<xref ref-type="bibr" rid="B57">Merow et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B17">Dud&#xed;k et&#xa0;al., 2005</xref>). We also set the maximum iteration value to 500, selected the run type as &#x201c;Bootstrap&#x201d;, the maximum background points were 10,000, 10 times running repetition of the model and random seeds were selected to enhance model randomness (<xref ref-type="bibr" rid="B85">Warren and Seifert, 2011</xref>). The other parameters were maintained at their default settings.</p>
</sec>
<sec id="s2_4">
<label>2.4</label>
<title>Model result evaluation and GIS analysis</title>
<p>We used the AUC of the receiver operating characteristic (ROC) analysis to assess and calibrate the accuracy of the MaxEnt model. The AUC was examined for additional accuracy analyses, including the agreement between introduced observations and predictive logistic regression results (<xref ref-type="bibr" rid="B19">Elith et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B22">Ficetola et&#xa0;al., 2007</xref>). AUC values range from 0 to 1, with larger values indicating greater credibility in model performance: the values&lt; 0.6, 0.6&#x2013;0.9, and &gt; 0.9 were considered poor, useful, and excellent, respectively (<xref ref-type="bibr" rid="B48">Liu et&#xa0;al., 2005</xref>). The probabilistic prediction results generated by the MaxEnt model are presented in a grid raster format, with values ranging from 0 to 1. Using the spatial projection outputs from the MaxEnt model, we estimated the future suitable areas of the species under climate change scenarios (SSP1-2.6 and SSP5-8.5). The suitable areas were divided into suitable habitats and unsuitable habitats based on the cloglog threshold value of the maximum training presence (MTP). The cloglog threshold for the MTP was set at 0.1039, classifying areas below this threshold as unsuitable habitats and those above as suitable (<xref ref-type="bibr" rid="B48">Liu et&#xa0;al., 2005</xref>). Accordingly, the suitable areas of the pest were reclassified into four categories: unsuitable habitats (0-MTP), low suitable habitats (MTP-0.4), moderate suitable habitats (0.4-0.6), and high suitable habitats (0.6-1).</p>
<p>The successful invasion and establishment of new areas by IAPs also depend on the suitability of the preferred host (<xref ref-type="bibr" rid="B15">de Godoy et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B33">Huber and Geist, 2019</xref>; <xref ref-type="bibr" rid="B18">Dukes and Mooney, 1999</xref>). To assess the impact of <italic>L. oryzophilus</italic> parthenogenetic populations on global rice- growing areas, we obtained distribution data in global rice-growing areas from the EarthStat database (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S3</bold>
</xref>; <ext-link ext-link-type="uri" xlink:href="http://www.earthstat.com">www.earthstat.com</ext-link>). The global rice-growing area was overlaid on the suitable areas of the populations under current and future climate scenarios. Additionally, we evaluated the proportion of the range of suitable areas for the species in the global rice-growing area to quantify the impact of this species parthenogenetic populations on global rice cultivation areas under current and future climate scenarios.</p>
</sec>
<sec id="s2_5">
<label>2.5</label>
<title>Hypervolume of climate ecological niche</title>
<p>In this study, we used four predictor variables (Bio18, Bio4, Bio10 &amp; Bio16), which significantly contribute to the model results, to constructed ecological niche characterization of <italic>L. oryzophilus</italic> parthenogenetic populations for North America, Europe, and Asia. The analysis data comes from extracting values from four predictor variables using known occurrence points in ArcGIS 10.8. For each continent, we used a full set of occurrence records to construct a complete ecological niche hypervolume. We used the &#x201c;hypervolume&#x201d; package to analysis in R software (<xref ref-type="bibr" rid="B8">Blonder et&#xa0;al., 2018</xref>). Based on the selected four climate variables, we used the Z-score to standardize the four predictor variables for constructing three niche hypervolume structures in three continent and adopted a cross-validation approach to select the bandwidth of each variable axis for optimization (<xref ref-type="bibr" rid="B8">Blonder et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B41">Jin et&#xa0;al., 2024</xref>). Then we mapped hypervolumes onto orthogonal axes comprising pairs of climatic variables and characterized the ecological niche similarity of <italic>L. oryzophilus</italic> across the three continents by calculating hypervolume distances between centers of mass (Euclidean distances) and similarities between hypervolume structures (Sorensen indices) (<xref ref-type="bibr" rid="B53">Mammola, 2019</xref>).</p>
</sec>
<sec id="s2_6">
<label>2.6</label>
<title>Assessment of economic losses to rice production in China under current climate scenarios</title>
<p>We analyzed and assesses the potential economic losses to rice production in China caused by <italic>L. oryzophilus</italic> parthenogenetic populations under unmanaged scenario and managed scenario (<xref ref-type="bibr" rid="B81">Ullah et&#xa0;al., 2023</xref>; <xref ref-type="bibr" rid="B88">Xu et&#xa0;al., 2020</xref>):</p>
<p>Unmanaged scenario:</p>
<p>Potential economic loss caused by production quantity decline-F1</p>
<disp-formula>
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</mml:mrow>
<mml:mo stretchy="false">)</mml:mo>
</mml:mrow>
</mml:mrow>
</mml:math>
</disp-formula>
<p>Managed scenario:</p>
<p>Management costs-F2</p>
<disp-formula>
<mml:math display="block" id="M2">
<mml:mrow>
<mml:mi>F</mml:mi>
<mml:mn>2</mml:mn>
<mml:mi>=</mml:mi>
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<mml:mo>&#x2217;</mml:mo>
<mml:mi>I</mml:mi>
<mml:mo>&#x2217;</mml:mo>
<mml:mi>C</mml:mi>
</mml:mrow>
</mml:math>
</disp-formula>
<p>Potential economic loss after management-F3</p>
<disp-formula>
<mml:math display="block" id="M3">
<mml:mrow>
<mml:mi>F</mml:mi>
<mml:mn>3</mml:mn>
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<mml:mi>Q</mml:mi>
<mml:mo>&#x2217;</mml:mo>
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<mml:mo>&#x2217;</mml:mo>
<mml:mi>E</mml:mi>
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</mml:mrow>
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</mml:mrow>
</mml:mrow>
</mml:math>
</disp-formula>
<p>Potential economic loss under management scenario-F4</p>
<disp-formula>
<mml:math display="block" id="M4">
<mml:mrow>
<mml:mi>F</mml:mi>
<mml:mn>4</mml:mn>
<mml:mo>=</mml:mo>
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<mml:mi>F</mml:mi>
<mml:mn>3</mml:mn>
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</disp-formula>
<p>Potential savings after management-F5</p>
<disp-formula>
<mml:math display="block" id="M5">
<mml:mrow>
<mml:mi>F</mml:mi>
<mml:mn>5</mml:mn>
<mml:mo>=</mml:mo>
<mml:mi>F</mml:mi>
<mml:mn>1</mml:mn>
<mml:mo>&#x2212;</mml:mo>
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</mml:mrow>
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</disp-formula>
<p>We obtained the statistical data on rice production and planting area for each province from 2018 to 2022 from the National Bureau of Statistics (<ext-link ext-link-type="uri" xlink:href="http://www.stats.gov.cn/">http://www.stats.gov.cn/</ext-link>) and Strategic Reserves Administration (<ext-link ext-link-type="uri" xlink:href="http://www.chinagrain.gov.cn/">http://www.chinagrain.gov.cn/</ext-link>). Based on the market price of pesticides in China and the suitable area of the populations, we assessed the required investment in prevention cost (<xref ref-type="bibr" rid="B88">Xu et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B30">He et&#xa0;al., 2016</xref>). We combined the rice production and planting area data with the proportion of suitable areas for the populations in each province to calculate the annual rice production and planting area within its suitable areas (<xref ref-type="bibr" rid="B68">Qin et&#xa0;al., 2020</xref>). The specific indicator setting for harm and economic parameters under Unmanaged and managed scenarios are shown in <xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>. All parameters were entered into the @Risk software as distribution functions (using the Pert function for fitting), and a Latin hypercube sampling method was employed to draw samples from each distribution with a total of 100,000 iterations conducted (<xref ref-type="bibr" rid="B81">Ullah et&#xa0;al., 2023</xref>).</p>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Calculate specific parameter settings for potential economic losses.</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" align="center">Scenarios</th>
<th valign="middle" align="center">Parameters types</th>
<th valign="middle" align="center">Unite</th>
<th valign="middle" align="center">Parameters setting</th>
<th valign="middle" align="center">Reference</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="middle" rowspan="4" align="center">Unmanagement scenario</td>
<td valign="middle" align="center">The yield of rice plants in suitable habitats - Q</td>
<td valign="middle" align="center">t</td>
<td valign="middle" align="center">Pert (192633999.68, 194501221, 196083353.35)</td>
<td valign="middle" align="center">
<ext-link ext-link-type="uri" xlink:href="http://www.stats.gov.cn/">http://www.stats.gov.cn/</ext-link>
</td>
</tr>
<tr>
<td valign="middle" align="center">The damage rate of rice-I</td>
<td valign="middle" align="center">%</td>
<td valign="middle" align="center">Pert (10, 30, 50)</td>
<td valign="middle" align="center">(<xref ref-type="bibr" rid="B94">Zou et&#xa0;al., 2004</xref>)</td>
</tr>
<tr>
<td valign="middle" align="center">The yield loss rate of rice-R</td>
<td valign="middle" align="center">%</td>
<td valign="middle" align="center">Pert (15.9, 51.35, 86.8)</td>
<td valign="middle" align="center">(<xref ref-type="bibr" rid="B93">Zhou et&#xa0;al., 2007</xref>)</td>
</tr>
<tr>
<td valign="middle" align="center">Rice market price-Pa</td>
<td valign="middle" align="center">$/t</td>
<td valign="middle" align="center">Pert (374.12, 402.32, 544.83)</td>
<td valign="middle" align="center">
<ext-link ext-link-type="uri" xlink:href="http://www.chinagrain.gov.cn/">http://www.chinagrain.gov.cn/</ext-link>
</td>
</tr>
<tr>
<td valign="middle" rowspan="6" align="center">management scenario</td>
<td valign="middle" align="center">The area of rice plants in suitable habitats -S</td>
<td valign="middle" align="center">hm<sup>2</sup>
</td>
<td valign="middle" align="center">Pert (27363597.06, 27683966.83, 27966379.44)</td>
<td valign="middle" align="center">
<ext-link ext-link-type="uri" xlink:href="http://www.stats.gov.cn/">http://www.stats.gov.cn/</ext-link>
</td>
</tr>
<tr>
<td valign="middle" align="center">Unit prevention cost-C</td>
<td valign="middle" align="center">$/t</td>
<td valign="middle" align="center">Pert (5.87, 39.85, 110.64)</td>
<td valign="middle" align="center">(<xref ref-type="bibr" rid="B30">He et&#xa0;al., 2016</xref>)</td>
</tr>
<tr>
<td valign="middle" align="center">Unit yield of rice in suitable area-W</td>
<td valign="middle" align="center">t/hm<sup>2</sup>
</td>
<td valign="middle" align="center">Pert (6.99, 7.03, 7.07)</td>
<td valign="middle" align="center">&#x2013;</td>
</tr>
<tr>
<td valign="middle" align="center">Control effect -M</td>
<td valign="middle" align="center">%</td>
<td valign="middle" align="center">Pert (72.44, 78.35, 84.25)</td>
<td valign="middle" align="center">(<xref ref-type="bibr" rid="B30">He et&#xa0;al., 2016</xref>)</td>
</tr>
<tr>
<td valign="middle" align="center">Benefit correction coefficient -D</td>
<td valign="middle" align="center">&#x2013;</td>
<td valign="middle" align="center">2</td>
<td valign="middle" align="center">(<xref ref-type="bibr" rid="B88">Xu et&#xa0;al., 2020</xref>)</td>
</tr>
<tr>
<td valign="middle" align="center">Economic loss level -E</td>
<td valign="middle" align="center">%</td>
<td valign="middle" align="center">E=C/(W*Pa*M) *D*100%</td>
<td valign="middle" align="center">&#x2013;</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
</sec>
<sec id="s3" sec-type="results">
<label>3</label>
<title>Results</title>
<sec id="s3_1">
<label>3.1</label>
<title>Invasion history of <italic>L. oryzophilus</italic>
</title>
<p>Since the first discovery the bisexual populations of this species in Texas in 1904, subsequent findings of the bisexual populations occurred within 20 years in Louisiana, Kansas, and Florida (<xref ref-type="fig" rid="f2">
<bold>Figures&#xa0;2A, B</bold>
</xref>). Following the initial report of the parthenogenetic populations in California in 1958, this populations rapidly invaded northern Latin America, eastern Asia, and southern Europe over the next 70 years, propelled by the acceleration of global trade (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2A</bold>
</xref>). As of 2020, the distribution of this species is primarily concentrated in the Northern Hemisphere, particularly in regions with extensive rice cultivation, such as China and Japan (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2</bold>
</xref>). Especially in China, since the first discovery of the parthenogenetic populations of <italic>L. oryzophilus</italic> in Hebei Province in 1988, this populations rapidly spread along the coastal regions of China during the 1990s. After entering the 21st century, the populations gradually showed a trend of spreading from the coastal areas to the inland regions. As of 2024, approximately 5/6 of the provinces have recorded the distribution of the parthenogenetic populations in China (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2C</bold>
</xref>).</p>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>
<bold>(A)</bold> Global invasion history reconstruction of <italic>Lissorhoptrus oryzophilus</italic>; <bold>(B)</bold> Historical spread dynamics of <italic>L. oryzophilus</italic> in the United States; <bold>(C)</bold> Historical spread dynamics of <italic>L. oryzophilus</italic> in China.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1506418-g002.tif"/>
</fig>
</sec>
<sec id="s3_2">
<label>3.2</label>
<title>Model accuracy evaluation and importance of bioclimatic variables</title>
<p>Based on the model optimization results, with RM = 0.5 and FC = LQHP, the &#x394;AICc value was 0. Therefore, these were selected as the final parameter settings (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S4A</bold>
</xref>). The resulting mean training and testing AUC values were 0.939 (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S4B</bold>
</xref>), indicating the outcomes of the model were reliable. The precipitation of the warmest quarter (Bio18, 57.9%), temperature seasonality (Bio4, 22%), mean temperature of the warmest quarter (Bio10, 13.7%), and precipitation of the wettest quarter (Bio16, 1.7%) were the four most significant bioclimatic variables affecting the suitable areas of parthenogenetic populations (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S3</bold>
</xref>). The effect of precipitation on the suitable areas of the populations was more significant than that of temperature, as indicated through the jackknife and percent contributions (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Table S1</bold>
</xref>, <xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S5</bold>
</xref>). According to the precipitation during the warmest quarter (Bio18), the probability of survivability increased from 0.03 to 0.86 within the range of 26.50 to 562.20 mm and subsequently declined rapidly (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S6A</bold>
</xref>). The response curves of temperature seasonality (Bio4) showed that within the range of 1.86&#x2013;751.26, the probability of occurrence increased from 0.006 to 0.92, rapidly decreased until approximately 976.63, the probability of occurrence increased from 0.92 to 0.38 (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S6B</bold>
</xref>). Regarding the Bio10 and Bio16 precipitation variables, the probability of occurrence peaked when the variables were 26.36&#xb0;C and 1567.56 mm, respectively (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figures S6C, D</bold>
</xref>).</p>
</sec>
<sec id="s3_3">
<label>3.3</label>
<title>Suitable areas of <italic>L. oryzophilus</italic> parthenogenetic populations under the current climate</title>
<p>Current global suitable areas forecast of the populations are depicted in <xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref>. The global suitable areas for the parthenogenetic populations establishment was 1068.4 &#xd7; 10<sup>4</sup> km<sup>2</sup> under the current climate (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). Highly suitable habitats for the populations are predicted in the northeastern and southern of China, the western Japan, and Korea peninsula (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3A</bold>
</xref>). The area of high suitability was 143.83 &#xd7; 10<sup>4</sup> km<sup>2</sup> (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). Moderately suitable habitats for the populations are predicted in the northeastern and southern of China (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3A</bold>
</xref>). The area of moderate suitability was 209.67 &#xd7; 10<sup>4</sup> km<sup>2</sup> (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>). Lowly suitable habitats for the populations are predicted in eastern and southeastern United States, northern Argentina, southern Europe (Italy, Macedonia, Greece, France, Spain), western Asia (Turkey and Kazakhstan), northern Southeast Asia (Vietnam, Myanmar, Laos and northeastern India) and the northeastern and southern of China (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3A</bold>
</xref>). The area of low suitability was 714 &#xd7; 10<sup>4</sup> km<sup>2</sup> (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>).</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>
<bold>(A)</bold> The suitable areas of <italic>Lissorhoptrus oryzophilus</italic> parthenogenetic populations under current climatic scenarios. <bold>(B)</bold> The suitable areas of <italic>L. oryzophilus</italic> parthenogenetic populations in global rice-growing areas under current climatic scenarios.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1506418-g003.tif"/>
</fig>
<table-wrap id="T2" position="float">
<label>Table&#xa0;2</label>
<caption>
<p>Predicted suitable habitat areas for <italic>Lissorhoptrus oryzophilus</italic> parthenogenetic populations under current and future climatic scenarios (&#xd7;10<sup>4</sup>km<sup>2</sup>).</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" rowspan="2" align="left"/>
<th valign="middle" rowspan="2" align="left">Current</th>
<th valign="middle" colspan="3" align="left">SSP1-2.6</th>
<th valign="middle" colspan="3" align="left">SSP5-8.5</th>
</tr>
<tr>
<th valign="middle" align="left">2030s</th>
<th valign="middle" align="left">2050s</th>
<th valign="middle" align="left">Ave</th>
<th valign="middle" align="left">2030s</th>
<th valign="middle" align="left">2050s</th>
<th valign="middle" align="left">Ave</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="middle" align="left">low suitability</td>
<td valign="middle" align="left">714.90</td>
<td valign="middle" align="left">772.86 (8.11)</td>
<td valign="middle" align="left">659.29 (-7.78)</td>
<td valign="middle" align="left">716.08 (0.16)</td>
<td valign="middle" align="left">723.79 (1.24)</td>
<td valign="middle" align="left">807.62 (12.97)</td>
<td valign="middle" align="left">765.71 (7.11)</td>
</tr>
<tr>
<td valign="middle" align="left">moderate suitability</td>
<td valign="middle" align="left">143.83</td>
<td valign="middle" align="left">149.69 (4.07)</td>
<td valign="middle" align="left">152.65 (6.13)</td>
<td valign="middle" align="left">151.17 (5.10)</td>
<td valign="middle" align="left">152.42 (5.97)</td>
<td valign="middle" align="left">145.38 (1.08)</td>
<td valign="middle" align="left">148.90 (3.52)</td>
</tr>
<tr>
<td valign="middle" align="left">high suitability</td>
<td valign="middle" align="left">209.67</td>
<td valign="middle" align="left">196.99 (-6.05)</td>
<td valign="middle" align="left">206.90 (-1.32)</td>
<td valign="middle" align="left">201.95 (-3.68)</td>
<td valign="middle" align="left">198.71 (-5.23)</td>
<td valign="middle" align="left">196.20 (-6.42)</td>
<td valign="middle" align="left">197.46 (-5.83)</td>
</tr>
<tr>
<td valign="middle" align="left">Total suitability</td>
<td valign="middle" align="left">1068.40</td>
<td valign="middle" align="left">1119.54 (4.79)</td>
<td valign="middle" align="left">1018.85 (-4.64)</td>
<td valign="middle" align="left">1069.20 (0.07)</td>
<td valign="middle" align="left">1074.93 (0.61)</td>
<td valign="middle" align="left">1149.20 (7.56)</td>
<td valign="middle" align="left">1112.07 (4.09)</td>
</tr>
<tr>
<td valign="middle" align="left">Total suitability in global rice-growing areas</td>
<td valign="middle" align="left">221.94</td>
<td valign="middle" align="left">225.10 (1.43)</td>
<td valign="middle" align="left">217.22 (-2.13)</td>
<td valign="middle" align="left">221.16 (-0.35)</td>
<td valign="middle" align="left">223.34 (0.63)</td>
<td valign="middle" align="left">219.368 (-1.16)</td>
<td valign="middle" align="left">221.35 (-0.26)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn>
<p>The parentheses following the numbers indicate the percentage change in suitable habitat area relative to the current climate scenario across different time periods and climate scenarios.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<p>The range of suitable areas for the populations within the global rice-growing area is 221.94 &#xd7; 10<sup>4</sup> km<sup>2</sup>, accounting for 30.6% of the total global rice-growing area under current conditions (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3B</bold>
</xref>, <xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). The regions primarily affected by this populations in the rice industry include North America (the southern unite states), South America (Southern Brazil), southern Europe (Northern Italy and coastal areas of Spain), and Asia (northern Vietnam, northern Myanmar, northeastern and northern India, northeastern and southern of China, Western Korean Peninsula, Southern and Western Japan). Among these regions, the populations have notably impacted rice-growing areas in China, the Korean Peninsula, and Japan, with all major rice-growing areas concentrated in these countries and regions (<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3B</bold>
</xref>).</p>
</sec>
<sec id="s3_4">
<label>3.4</label>
<title>Suitable areas of <italic>L. oryzophilus</italic> parthenogenetic populations under future climate scenarios</title>
<p>The suitable areas of the parthenogenetic populations under two climate change scenarios (SSP1-2.6 and SSP5-8.5) and in two time periods (2030s and 2050s) is shown in <xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>. Overall, compared to current climate scenarios, the populations present insignificant changes in global suitability under two future climate scenarios. Its primary suitability remains concentrated in eastern North America, southern South America, southern Europe, and eastern Asia. Northeastern China, western Korean Peninsula, and western and southern parts of Japan continue to be identified as major high suitability areas (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4</bold>
</xref>). The low-emission SSP1-2.6 scenario suggested the total suitable habitat areas are 1069.20 &#xd7; 10<sup>4</sup> km<sup>2</sup>, with an increase of 0.07% in the current suitable area for the establishment of the populations (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). The low and moderate suitability areas cover 716.07 &#xd7; 10<sup>4</sup> km<sup>2</sup> and 151.17 &#xd7; 10<sup>4</sup> km<sup>2</sup> (increase 0.16% and 5.10% compared to the current area), while high suitability areas are 201.95 &#xd7; 10<sup>4</sup> km<sup>2</sup> (decrease 3.63% compared to the current area) (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). The MaxEnt model further predicted higher habitat suitability areas and spread of RSW under high-emission scenario SSP5-8.5 in 2030s and 2050s. The high-emission SSP5-8.5 scenario suggested the total suitable habitat areas are 1111.80 &#xd7; 10<sup>4</sup> km<sup>2</sup>, with an increase of 4.0% in the current suitable area for the establishment of the populations (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). The low and moderate suitability areas cover 765.71 &#xd7; 10<sup>4</sup> km<sup>2</sup> and 151.17 &#xd7; 10<sup>4</sup> km<sup>2</sup> (increase 7.1% and 3.5% compared to the current area), while high suitability areas are 201.95 &#xd7; 10<sup>4</sup> km<sup>2</sup> (decrease 5.82% compared to the current area) (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>).</p>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>The suitable areas of <italic>Lissorhoptrus oryzophilus</italic> parthenogenetic populations under two future climatic scenarios in 2030s and 2050s (SSP1-2.6 (low-emission scenario) and SSP5-8.5 (high-emission scenario)).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1506418-g004.tif"/>
</fig>
<p>Changes in the establishment risk of the populations in global rice-growing areas under two future climate scenarios is shown in <xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5</bold>
</xref>. Overall, sum of suitability areas will decrease to 221.16&#xd7;10<sup>4</sup> km<sup>2</sup> and 221.35&#xd7;10<sup>4</sup> km<sup>2</sup> (decrease 0.35% and 0.26% compared to the current area) (<xref ref-type="table" rid="T2">
<bold>Table&#xa0;2</bold>
</xref>). The establishment risk of this populations in global rice-growing areas is primarily concentrated in North America (the southern unite states), South America (Southern Brazil), southern Europe (Northern Italy and coastal areas of Spain), and Asia (northern Vietnam, northern Myanmar, northeastern and northern India, northeastern and southern of China, Western Korean Peninsula, Southern and Western Japan) under SSP1-2.6 and SSP5-8.5 scenarios (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5</bold>
</xref>). Fortunately, the increased suitability areas for the establishment of the populations are generally stable, concentrated in northern and northeastern India, and northern and central Myanmar (<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>The change of the suitable areas of <italic>Lissorhoptrus oryzophilus</italic> parthenogenetic populations in global rice growing areas under future climatic scenarios from current to 2030s <bold>(A, B)</bold> and 2050s <bold>(C, D)</bold> under SSP1-2.6 (low-emission scenario) and SSP5-8.5 (high-emission scenario).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1506418-g005.tif"/>
</fig>
</sec>
<sec id="s3_5">
<label>3.5</label>
<title>Ecological niche similarity of <italic>L. oryzophilus</italic> parthenogenetic populations in three continents</title>
<p>Here, we utilized the n-hypervolume framework to comprehensively assess the niche similarity between the native range (North America) and invasive ranges (Europe and Asia) using the Sorensen index and Euclidean distance (<xref ref-type="table" rid="T3">
<bold>Table&#xa0;3</bold>
</xref>). Overall, this population exhibits significant differences in climatic niche occupancy between the invasive and native ranges. The Euclidean distance is 0.5495 between European and North American populations, with a Sorensen index of 0.1482. However, Asian population shows even greater Euclidean distance (0.6727) and a smaller Sorensen index (0.0133) relative to North American populations. Furthermore, compared to North America and Europe, this population occupies a larger and more distinct climatic niche space in Asia (<xref ref-type="fig" rid="f6">
<bold>Figure&#xa0;6</bold>
</xref>). Compared to its native range, this population occupies a climatic niche in Asia where, except for Bio10 (mean temperature of the warmest quarter) which has expanded towards lower levels, the other three variables (Bio4 (Temperature Seasonality), Bio16 (Precipitation of Wettest Quarter), Bio18 (Precipitation of Warmest Quarter)) have expanded towards higher levels (<xref ref-type="fig" rid="f6">
<bold>Figure&#xa0;6</bold>
</xref>).</p>
<table-wrap id="T3" position="float">
<label>Table&#xa0;3</label>
<caption>
<p>Climatic ecological niche similarity of <italic>Lissorhoptrus oryzophilus</italic> parthenogenetic populations in North America, Europe, and Asia (above the diagonal is the Sorensen index, below the diagonal is centroid distance).</p>
</caption>
<table frame="hsides">
<thead>
<tr>
<th valign="middle" rowspan="2" align="left"/>
<th valign="middle" colspan="3" align="left">Euclidean distance\Sorensen</th>
</tr>
<tr>
<th valign="middle" align="left">North America</th>
<th valign="middle" align="left">Europe</th>
<th valign="middle" align="left">Asia</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="middle" align="left">North America</td>
<td valign="middle" align="left"/>
<td valign="middle" align="left">0.1482</td>
<td valign="middle" align="left">0.0133</td>
</tr>
<tr>
<td valign="middle" align="left">Europe</td>
<td valign="middle" align="left">0.5495</td>
<td valign="middle" align="left"/>
<td valign="middle" align="left">0.0006</td>
</tr>
<tr>
<td valign="middle" align="left">Asia</td>
<td valign="middle" align="left">0.6727</td>
<td valign="middle" align="left">0.9319</td>
<td valign="middle" align="left"/>
</tr>
</tbody>
</table>
</table-wrap>
<fig id="f6" position="float">
<label>Figure&#xa0;6</label>
<caption>
<p>Based on the n-hypervolume and four key climatic variables to construct the climatic niche characteristics of <italic>Lissorhoptrus oryzophilus</italic> parthenogenetic populations across North America, Europe, and Asia (bio4 (Temperature Seasonality), bio10 (Mean Temperature of Warmest Quarter), bio16 (Precipitation of Wettest Quarter), bio18(Precipitation of Warmest Quarter)).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fpls-15-1506418-g006.tif"/>
</fig>
</sec>
<sec id="s3_6">
<label>3.6</label>
<title>The potential economic losses caused by <italic>L. oryzophilus</italic> parthenogenetic populations in China and their controlling benefit</title>
<p>Under the unmanaged scenario (F1), the potential economic losses of <italic>L. oryzophilus</italic> parthenogenetic populations on the rice industry were estimated to range from $5.44 billion to $32.46 billion USD at a 95% confidence level. Sensitivity analysis results showed that the ranking of the factors influencing these potential losses under unmanaged scenario include the rice yield loss rate (R), the damage rate of rice (I), the rice market price (Pa), and the yield of rice in suitable habitats (Q) (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S7A</bold>
</xref>).</p>
<p>Under the management scenario (F2), the potential economic loss of rice in China due to the populations range from $0.10 billion to $0.83 billion USD at a 95% confidence level, with a mean value of $0.47 billion USD. The potential economic loss from management costs (F3) ranges from $0.26 billion to $2.19 billion USD at a 95% confidence level, while the loss after management (F4) ranges from $0.36 billion to $3.02 billion USD, with mean values of $1.22 billion and $1.69 billion USD, respectively. Potential savings after management (F5) range from $4.41 billion to $30.68 billion USD at a 95% confidence level, with a mean value of $17.54 billion USD. Sensitivity analysis results showed that the ranking of the factors influencing these potential losses under the management scenario includes the loss rate after the unit prevention cost (C), the damage rate of rice by the populations (I), the area of rice plants in suitable habitats (S), the yield of rice in suitable habitats (Q), the rice market price (Pa), and the control effect of the populations (M) (<xref ref-type="supplementary-material" rid="SM1">
<bold>Supplementary Figure S7B</bold>
</xref>).</p>
</sec>
</sec>
<sec id="s4" sec-type="discussion">
<label>4</label>
<title>Discussion</title>
<p>Rice is the most important crop in the world because half of the global populations consume it daily. In some Asian countries, rice provides over 70% of the calorie supply (<xref ref-type="bibr" rid="B27">GRiSP, 2013</xref>). Therefore, rice is considered one of the most strategically significant commodities worldwide, closely intertwined with global food security, economic growth, employment, social stability, and regional peace (<xref ref-type="bibr" rid="B56">Mehrabi et&#xa0;al., 2018</xref>). However, the transport of pests beyond their native ranges by human actions is breaking down biogeographical barriers and threatening local rice production, and invasive alien pests also continually explore new climate characteristics during this process (<xref ref-type="bibr" rid="B11">Capinha et&#xa0;al., 2015</xref>; <xref ref-type="bibr" rid="B82">Vil&#xe0; et&#xa0;al., 2011</xref>). Indirectly, negative impact of climate change on rice yield by altering the suitable areas range of pests, increasing the occurrence of pests and diseases and exacerbating natural disasters, thus posing a threat to food security (<xref ref-type="bibr" rid="B78">Tilman et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B49">Lori, 2021</xref>; <xref ref-type="bibr" rid="B71">Rezaei et&#xa0;al., 2023</xref>).</p>
<sec id="s4_1">
<label>4.1</label>
<title>Humid and hot environments are favorable for the occurrence of the populations</title>
<p>Our results revealed that the effect of precipitation factors on the prevalence of <italic>L. oryzophilus</italic> parthenogenetic populations was significantly greater than that of temperature factors. Specifically, the precipitation of the warmest quarter (Bio18) and accounted for 57.9% and 13.7% of the contribution rate to the MaxEnt result and ranging from 685.19 to 753.33 mm for the precipitation of the warmest quarter were considered high suitability for the populations. Previous studies showed that the populations oviposits in the submerged portion of the rice seedlings in summer and the peak oviposition typically coincides with the establishment of a flood, fostering accelerated larval growth rates under these conditions (<xref ref-type="bibr" rid="B9">Bowling, 1972</xref>; <xref ref-type="bibr" rid="B79">Tindall et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B75">Stout et&#xa0;al., 2002</xref>). Previous studies indicate that most 1st-generation adults end diapause after exposure to 10&#xb0;C, 15&#xb0;C, and 20&#xb0;C, while diapause intensity is higher at 25&#xb0;C, possibly to avoid extreme high temperatures after emergence (<xref ref-type="bibr" rid="B38">Jiang et&#xa0;al., 2004</xref>). However, the 2nd-generation adults are less likely to face high temperatures, resulting in lower diapause intensity (<xref ref-type="bibr" rid="B38">Jiang et&#xa0;al., 2004</xref>). In our result, the mean temperature the warmest quarter (Bio10) maintained between 10&#xb0;C and 33&#xb0;C, the probability of presence for this populations will exceed 0. The previous results corroborate our findings indirectly.</p>
</sec>
<sec id="s4_2">
<label>4.2</label>
<title>Frequent invasion events of the populations concentrated in the Northern Hemisphere for over half a century</title>
<p>In the late 1950s, a parthenogenic populations of <italic>L. oryzophilus</italic> was first recorded in northern California (<xref ref-type="bibr" rid="B43">Lange and Grigarick, 1959</xref>). In the mid-1970s, the parthenogenetic populations of rice water weevils presumably &#x201c;hitchhiked&#x201d; across the Pacific into Aichi Prefecture, Japan (<xref ref-type="bibr" rid="B35">Iwata, 1979</xref>). After a decade of spreading, this populations quickly proliferated across the entire Japanese archipelago (<xref ref-type="bibr" rid="B55">Matsui, 1987</xref>). In Aichi Prefecture, Japan, the population is univoltine, with overwintered adults migrating to rice fields during daytime when temperatures exceed 20&#xb0;C in May and June. By late July, eggs and larvae are found in the rice fields (<xref ref-type="bibr" rid="B55">Matsui, 1987</xref>). In southern Japan, the population is bivoltine, with very low larval densities on late-planted rice seedlings (<xref ref-type="bibr" rid="B55">Matsui, 1987</xref>). Despite agricultural and chemical control measures targeting the parthenogenetic populations in Japan, some individuals among the 150 rice varieties planted still exhibit high tolerance (<xref ref-type="bibr" rid="B55">Matsui, 1987</xref>). In 1988, the populations were recorded in mainland China and the Korean Peninsula, while Taiwan first reported their presence in Taoyuan County in March 1990 (<xref ref-type="bibr" rid="B76">Sun et&#xa0;al., 1996</xref>). In Korea, the populations were primarily univoltine, with occasional second-generation appearances in some years (<xref ref-type="bibr" rid="B45">Li, 1993</xref>; <xref ref-type="bibr" rid="B76">Sun et&#xa0;al., 1996</xref>). The spread and velocity of the populations in Korea are influenced by wind, mountainous terrain, and ground transportation (<xref ref-type="bibr" rid="B80">Uhm et&#xa0;al., 1989</xref>). Since the 21st century began, the populations were detected for the first time in Europe in 2004 (<xref ref-type="bibr" rid="B10">Caldara et&#xa0;al., 2004</xref>). Since then, the pest has rapidly spread across northern Italy, where rice cultivation is prevalent and the interconnected rice fields create corridors that aid its spread (<xref ref-type="bibr" rid="B50">Lupi et&#xa0;al., 2010</xref>; <xref ref-type="bibr" rid="B83">Wang et&#xa0;al., 2011</xref>). By 2020, this populations had established widespread populations in rice-growing regions across Europe, including Macedonia, Greece, France, Spain (<xref ref-type="bibr" rid="B23">Giantsis et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B59">Montauban et&#xa0;al., 2021</xref>).</p>
</sec>
<sec id="s4_3">
<label>4.3</label>
<title>The establishment hotspot areas concentrated in East Asia for the populations</title>
<p>The suitable areas of <italic>L. oryzophilus</italic> parthenogenetic populations were predominantly concentrated in rice-planting areas of the United States, Brazil, Argentina, Italy, Spain, Bulgaria, China, Nepal, Myanmar, Laos, Vietnam, India, the Korean Peninsula and Japan under current and future climate scenarios. It&#x2019;s noteworthy that nearly all rice-growing areas in East Asia are covered by high-suitability areas for this populations, including China (northeastern, central and southern China), the Korean Peninsula, and Japan. Based on the results predicted by CLIMEX, <xref ref-type="bibr" rid="B54">Mao et&#xa0;al. (1997)</xref> found that the suitable areas are concentrated in Northeast, North, East, Central, South, and Southwest China. <xref ref-type="bibr" rid="B67">Qi et&#xa0;al. (2012)</xref> and <xref ref-type="bibr" rid="B87">Xie et&#xa0;al. (2022)</xref> used the MaxEnt model to analyze the suitable areas pattern of the populations in China reported high-suitability areas located primarily in northeastern, central and southern China. This also aligns with our results in China. Based on the analysis of climatic niche characteristics using the ecological niche hypervolume framework, the results indicate that compared to the native North American populations, the Asian populations occupied a larger climatic niche space, with significant climatic niche differentiation between the two populations. This isn&#x2019;t surprising, as populations of <italic>L. oryzophilus</italic> that reproduce through parthenogenesis possess allowing them to rapidly adapt to changing environments and establish a sustainable populations within a short timeframe (<xref ref-type="bibr" rid="B32">Huang et&#xa0;al., 2017</xref>). Populations genetic studies have shown that there is a certain degree of genetic differentiation within the parthenogenetic populations between populations from the United States, Europe, and Asia, and among different geographic subgroups within Asia (<xref ref-type="bibr" rid="B90">Yang, 2008</xref>). Additionally, species invasion depends on the availability of host plants and the extent to which intruders require specific host plant species or are able to adapt to new species (<xref ref-type="bibr" rid="B5">Aljaryian et&#xa0;al., 2016</xref>). The extensive rice-growing areas in Asia have indeed provided a conducive environment for the spread of this populations to a certain extent (<xref ref-type="bibr" rid="B32">Huang et&#xa0;al., 2017</xref>). Furthermore, human activities have contributed to the spread of this beetle in Asia, especially in China. Despite geographical barriers, transporting rice seedlings, straw, and soil contaminated by the beetle could inadvertently introduce it to neighboring villages and counties (<xref ref-type="bibr" rid="B32">Huang et&#xa0;al., 2017</xref>). Notably, it appears that countries in West Africa, despite being major rice-growing regions, do not seem to face potential invasion by this populations. The two climatically distinct rice growing periods &#x2013; dry and wet seasons &#x2013; are crucial for rice double cropping in West Africa (<xref ref-type="bibr" rid="B16">Dingkuhn and Miezan, 1995</xref>). During the dry season, the region experiences low air temperatures and minimal solar radiation due to dry and dusty conditions. In the late dry season, temperature gradually temperatures gradually rise. During the wet season, the region shows a climate gradient from hot, humid and rainy (Average annual rainfall of 1150&#x2009;mm) in the south to very hot and dry with low rainfall (Annual precipitation is about 200mm) in the north (<xref ref-type="bibr" rid="B34">Ibrahim et&#xa0;al., 2024</xref>). In Southeast Asia, the probability of extreme precipitation has increased from 1979 to 2019, with areas receiving over 2000 mm of annual rainfall accounting for 90.59% (<xref ref-type="bibr" rid="B89">Xu et&#xa0;al., 2022</xref>; <xref ref-type="bibr" rid="B39">Jin et&#xa0;al., 2023</xref>). This has contributed to a rise in flooding events, increasing the risk of waterlogging for the populations in this region (<xref ref-type="bibr" rid="B4">Aghaee and Godfrey, 2017</xref>). Therefore, extreme environmental changes have limited the occurrence of the rice weevil in West Africa to some extent. In the future, the establishment range of expansion will primarily be located in higher-altitude regions, such as the northeastern parts of Nepal and India. This is not surprising, as past studies have shown that global warming will further drive the beetles to expand into higher-altitude areas (<xref ref-type="bibr" rid="B58">Michael et&#xa0;al., 2022</xref>). This reflects the geographical response of insect to environmental changes, and it also indicates that the rice industry of these new regions will likely receive more attention in the future.</p>
</sec>
<sec id="s4_4">
<label>4.4</label>
<title>The potential economic loss of the populations is huge but recoverable in China</title>
<p>In recent decades, research on the potential economic impacts of IAPs on staple crop industry has significantly increased, focusing primarily on post-event impact assessments and evaluations of management effectiveness. For instance, <xref ref-type="bibr" rid="B68">Qin et&#xa0;al. (2020)</xref> utilized @RISK methodology to forecast the potential economic impact of <italic>Spodoptera frugiperda</italic> on maize industry in China. Without management measures, <italic>S. frugiperda</italic> is projected to cause potential economic losses ranging from 5.27 billion to 46.04 billion dollars (90% confidence level), while potential savings with management could amount to 3.57 billion to 40.93 billion dollars (90% confidence level).</p>
<p>In 1986, this species was classified as a national quarantine pest (<xref ref-type="bibr" rid="B92">Zhou, 1987</xref>). Two years later, a parthenogenetic population was first discovered in Tanghai, Hebei Province, and it rapidly spread along the coastal areas. Since the early 21st century, it has begun to move into central, southwestern, northwestern, and northeastern China (<xref ref-type="bibr" rid="B32">Huang et&#xa0;al., 2017</xref>). By July 2024, it had spread to 5/6 provinces in China (<ext-link ext-link-type="uri" xlink:href="http://www.moa.gov.cn/govpublic/ZZYGLS/202409/t20240902_6461580.htm">http://www.moa.gov.cn/govpublic/ZZYGLS/202409/t20240902_6461580.htm</ext-link>), becoming one of the most severe and rapidly spreading invasive pests in the country. Considering China is the largest producer of rice around the world, and the suitable areas of <italic>L. oryzophilus</italic> parthenogenetic populations cover nearly all rice-growing areas in China. Therefore, our study on potential economic losses focuses on China as a representative case. Based on @RISK software, the forecasted potential economic losses caused by <italic>L. oryzophilus</italic> parthenogenetic populations on rice industry show that the potential economic losses range from $5.44 billion to $32.46 billion USD (95% confidence level) under nil management scenario. However, the potential economic losses range from $0.10 billion to $0.83 billion USD (95% confidence level) after factoring in management costs, recovering over 90% of the potential economic losses. Sensitivity analysis reveals that the infestation rate of the populations and unit prevention cost is key input variable influencing potential economic losses under unmanaged scenario and managed scenario, respectively. Therefore, from an economic benefit perspective, implementing appropriate control measures in rice-growing regions affected by this global invasive pest is necessary and effective.</p>
</sec>
<sec id="s4_5">
<label>4.5</label>
<title>Better management of the establishment and spread of the populations</title>
<p>Since the initial discovery of <italic>L. oryzophilus</italic> parthenogenetic populations in the United States in 1958, the populations have rapidly spread across global rice-growing areas and establish stable populations. Our research highlights that East Asia contains extensive highly suitable areas for this populations, posing a significant threat to rice production in the region. Fortunately, a part of affected countries have implemented various control measures to mitigate the impact of the populations on local rice crops. In the U.S, as a semi-aquatic insect that relies on flooded conditions for larval development, the populations can be lower in a furrow irrigated rice system than the flooded field. Therefore, the furrow irrigated rice system may reduce the damage caused by this population (<xref ref-type="bibr" rid="B42">Kelly et&#xa0;al., 2021</xref>). During the fallow period, removing weeds from the rice field embankments and surrounding areas to reduce the abundance of host plants for the rice weevil may effectively lower its population density, thereby reducing the overall density in the rice fields (<xref ref-type="bibr" rid="B64">Palrang et&#xa0;al., 1994</xref>). This approach could be highly effective as it is easy for farmers to implement, making it suitable for promotion in China and other countries where the pest has become invasive (<xref ref-type="bibr" rid="B32">Huang et&#xa0;al., 2017</xref>). As a more efficient chemical control method, Chlorantraniliprole and its mixtures with other neonicotinoids chemicals (e.g., triazophos and thiamethoxam) are the primary chemical controls used in China (<xref ref-type="bibr" rid="B32">Huang et&#xa0;al., 2017</xref>). However, diamide seed treatments offer superior yield protection compared to neonicotinoids under high densities of the pest (<xref ref-type="bibr" rid="B62">Nicholas et&#xa0;al., 2024</xref>). Biological control and tolerance host plants breeding has shown applied promise. For instance, the highly resistant variety T03 was identified by comparing the adult feeding and oviposition preferences, egg hatching rate, larval survival rate among different rice varieties (<xref ref-type="bibr" rid="B47">Li et&#xa0;al., 2011</xref>). For potential but not yet realized suitable areas, it is crucial to establish official quarantine zones to prevent further spread. Strict quarantine on importing seedlings, straw, and soil from infected to non-infected areas, and avoiding the use of quarantine straw as packaging material, are essential (<xref ref-type="bibr" rid="B32">Huang et&#xa0;al., 2017</xref>).</p>
</sec>
</sec>
<sec id="s5" sec-type="conclusion">
<label>5</label>
<title>Conclusion</title>
<p>Based on the analysis using the MaxEnt model, the precipitation of the warmest quarter (Bio18) has been identified as the primary environmental factor influencing the habitat suitability of <italic>L. oryzophilus</italic> parthenogenetic populations. During its invasion process, the populations has explored new climatic conditions, particularly in East Asia. The results indicate that this populations pose the greatest threat to major rice-producing regions in Asia under current and future climate scenarios, particularly rice-growing areas in China, the Korean Peninsula, and Japan. Specially, the populations would cost the rice industry in China 18.95 billion US dollars under unmanaged measures. Fortunately, climate change has not significantly altered the current global distribution pattern of this populations within the rice-growing regions and it is possible to recover 93% of the economic losses in China through reasonable chemical control, such as the application of triazophos and thiamethoxam. Our research findings will support in monitoring, surveillance, and the development of early warning systems to control <italic>L. oryzophilus</italic> parthenogenetic populations worldwide. Policymakers and governments can utilize these findings to develop effective integrated pest management strategies to handle potential future outbreaks of this populations.</p>
</sec>
</body>
<back>
<sec id="s6" sec-type="data-availability">
<title>Data availability statement</title>
<p>The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.</p>
</sec>
<sec id="s7" sec-type="author-contributions">
<title>Author contributions</title>
<p>LL: Data curation, Writing &#x2013; original draft. ZJ: Conceptualization, Data curation, Methodology, Writing &#x2013; review &amp; editing. ML: Methodology, Writing &#x2013; review &amp; editing. YX: Conceptualization, Writing &#x2013; review &amp; editing. JG: Conceptualization, Writing &#x2013; review &amp; editing. DJ: Conceptualization, Writing &#x2013; review &amp; editing. RM: Conceptualization, Writing &#x2013; review &amp; editing. ZL: Conceptualization, Writing &#x2013; review &amp; editing. XX: Conceptualization, Writing &#x2013; review &amp; editing. WL: Conceptualization, Funding acquisition, Writing &#x2013; review &amp; editing.</p>
</sec>
<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 work was supported by the National Key R&amp;D Program of China (Grant No. 2022YFC2601400 and 2021YFC2600400) and the Innovation Program of the Chinese Academy of Agricultural Sciences (Grant No. caascx-2022-2025-IAS).</p>
</sec>
<sec id="s9" sec-type="COI-statement">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
<sec id="s10" sec-type="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/fpls.2024.1506418/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fpls.2024.1506418/full#supplementary-material</ext-link>
</p>
<supplementary-material xlink:href="DataSheet1.docx" id="SM1" mimetype="application/vnd.openxmlformats-officedocument.wordprocessingml.document"/>
<supplementary-material xlink:href="DataSheet2.csv" id="SM2" mimetype="text/csv"/>
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