{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T23:43:39Z","timestamp":1788479019007,"version":"build-2803163510"},"reference-count":53,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T00:00:00Z","timestamp":1747612800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100012149","name":"Environment and Natural Resources Trust Fund","doi-asserted-by":"crossref","award":["MAISRC Subproject 39: Increasing effectiveness of bigheaded carp deterrents by carbon dioxide integration"],"award-info":[{"award-number":["MAISRC Subproject 39: Increasing effectiveness of bigheaded carp deterrents by carbon dioxide integration"]}],"id":[{"id":"10.13039\/100012149","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"Invasive bigheaded carps (Hypophthalmichthys molitrix<\/jats:italic> and H. nobilis<\/jats:italic>) have caused substantial ecological and economic damage throughout the Mississippi River Basin and expanded their range threatening the Laurentian Great Lakes. Broadband acoustic deterrents have shown promise in repelling carp and are currently being assessed in navigational lock chambers on the Mississippi River. These nonphysical deterrents permit vessel navigation while reducing carp passage. However, no single deterrent is 100% effective and fish may habituate to the sound after repeated playback. Carp exhibit aversive behaviors to carbon dioxide, which suggests combining these two stimuli into one deterrent system could extend the effective duration of sound and reduce the frequency of carbon dioxide (C<\/mml:mi>O<\/mml:mi><\/mml:mrow>2<\/mml:mn><\/mml:mrow><\/mml:msub><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula>) application. We conditioned bigheaded carps to associate broadband sound from outboard boat motors (0.06\u20135\u2009kHz, ~<\/mml:mi><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula>150\u2009dB re. 1 \u03bc<\/mml:mi><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula>Pa) with C<\/mml:mi>O<\/mml:mi><\/mml:mrow>2<\/mml:mn><\/mml:mrow><\/mml:msub><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula> application (~<\/mml:mi><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula>35,000\u2009ppm) in small (80\u2009L) and large (3475\u2009L) two-choice shuttle tanks. We compared negative phonotaxis responses over one to four weeks between fish conditioned with sound and C<\/mml:mi>O<\/mml:mi><\/mml:mrow>2<\/mml:mn><\/mml:mrow><\/mml:msub><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula>, sound and air, or sound alone. Similar C<\/mml:mi>O<\/mml:mi><\/mml:mrow>2<\/mml:mn><\/mml:mrow><\/mml:msub><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula> avoidance thresholds were found across tank sizes and species. Conditioning treatment did not affect time to leave the sound chamber, confirming sound alone remains a deterrent for all fish. Carp conditioned with C<\/mml:mi>O<\/mml:mi><\/mml:mrow>2<\/mml:mn><\/mml:mrow><\/mml:msub><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula> took longer to return to the sound chamber than control treatments. Control fish were closer to the speaker during playback than during the pre-sound period, while fish conditioned with C<\/mml:mi>O<\/mml:mi><\/mml:mrow>2<\/mml:mn><\/mml:mrow><\/mml:msub><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula> were not significantly closer. Conditioning paradigms may extend the effective duration of nonphysical deterrents for bigheaded carps. Conditioning with C<\/mml:mi>O<\/mml:mi><\/mml:mrow>2<\/mml:mn><\/mml:mrow><\/mml:msub><\/mml:mrow><\/mml:math><\/jats:alternatives><\/jats:inline-formula> may also increase proactive flight-responses over reactive freeze-responses. Findings could be applied to increase nonphysical barrier effectiveness at locks along the Mississippi River and help protect the Laurentian Great Lakes from invasion.<\/jats:p>","DOI":"10.1371\/journal.pone.0320395","type":"journal-article","created":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T17:25:58Z","timestamp":1747675558000},"page":"e0320395","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["Conditioning invasive bigheaded carps (Hypophthalmichthys molitrix and H. nobilis)to enhance the efficacy of acoustic and CO2 deterrents"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2533-0802","authenticated-orcid":true,"given":"Jack A.","family":"Culotta","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie L.","family":"Ervin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brooke J.","family":"Vetter","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Allen F.","family":"Mensinger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,5,19]]},"reference":[{"key":"pone.0320395.ref001","first-page":"1","article-title":"Bigheaded carps: a biological synopsis and environmental risk assessment","volume":"33","author":"CS Kolar","year":"2007","journal-title":"Am Fish Soc Spec Publ"},{"issue":"1","key":"pone.0320395.ref002","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1139\/a2012-001","article-title":"Non-physical barriers to deter fish movements","volume":"20","author":"MR Noatch","year":"2012","journal-title":"Environ Rev"},{"key":"pone.0320395.ref003","unstructured":"Cudmore B, Mandrak NE, Dettmers JM, Chapman DC, Kolar CS. Binational ecological risk assessment of bigheaded carps (Hypophthalmichthys spp.) for the Great Lakes Basin. Report. Ottawa, ON; 2012. Report No.: 2011\/114."},{"key":"pone.0320395.ref004","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1007\/s11160-019-09583-x","article-title":"Acoustic deterrents to manage fish populations","volume":"29","author":"RL Putland","year":"2019","journal-title":"Rev Fish Biol Fisheries"},{"issue":"1","key":"pone.0320395.ref005","doi-asserted-by":"crossref","first-page":"220","DOI":"10.3391\/mbi.2022.13.1.13","article-title":"Evaluation of a broadband sound projected from the gates of a navigation lock in the Mississippi River shows it to be a weak deterrent for common carp and unable to block passage","volume":"13","author":"AT Riesgraf","year":"2022","journal-title":"Manage Biol Invasions"},{"issue":"6","key":"pone.0320395.ref006","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1577\/M10-053.1","article-title":"Introgressive hybridization between bighead carp and silver carp in the Mississippi and Illinois rivers","volume":"30","author":"JT Lamer","year":"2010","journal-title":"N Am J Fish Manag"},{"key":"pone.0320395.ref007","unstructured":"Kelly AM, Engle CR, Armstrong ML, Freeze M, Mitchell AJ, editors. History of introductions and governmental involvement in promoting the use of grass, silver, and bighead carps. In: Symposium on invasive Asian carps in North America: a forum to understand the biology and manage the problem; August 22\u201323, 2006; Peoria, IL. 2011."},{"issue":"6","key":"pone.0320395.ref008","doi-asserted-by":"crossref","first-page":"2035","DOI":"10.1890\/1051-0761(2006)016[2035:BIRFUP]2.0.CO;2","article-title":"Biological invasions: recommendations for U.S. policy and management","volume":"16","author":"DM Lodge","year":"2006","journal-title":"Ecol Appl"},{"issue":"7","key":"pone.0320395.ref009","doi-asserted-by":"crossref","first-page":"1512","DOI":"10.1139\/F08-099","article-title":"A management framework for preventing the secondary spread of aquatic invasive species","volume":"65","author":"MJ Vander Zanden","year":"2008","journal-title":"Can J Fish Aquat Sci"},{"issue":"3","key":"pone.0320395.ref010","first-page":"371","article-title":"Management implications of broadband sound in modulating wild silver carp (Hypophthalmichthys molitrix) behavior. Manag Biol Invasions","volume":"8","author":"BJ Vetter","year":"2017"},{"issue":"8","key":"pone.0320395.ref011","doi-asserted-by":"crossref","first-page":"2066","DOI":"10.1002\/eap.1795","article-title":"Selective fragmentation and the management of fish movement across anthropogenic barriers","volume":"28","author":"FJ Rahel","year":"2018","journal-title":"Ecol Appl"},{"issue":"8","key":"pone.0320395.ref012","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1002\/rra.3180","article-title":"Evaluating upstream passage and timing of approach by adult bigheaded carps at a gated dam on the Illinois River","volume":"33","author":"MV Lubejko","year":"2017","journal-title":"River Res Appl"},{"issue":"6","key":"pone.0320395.ref013","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1016\/j.jglr.2017.08.013","article-title":"Effects of tow transit on the efficacy of the Chicago sanitary and ship canal electric dispersal barrier system","volume":"43","author":"JJ Davis","year":"2017","journal-title":"J Great Lakes Res"},{"issue":"1","key":"pone.0320395.ref014","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/j.jglr.2016.11.009","article-title":"Acoustic deterrence of bighead carp (Hypophthalmichthys nobilis) to a broadband sound stimulus","volume":"43","author":"BJ Vetter","year":"2017","journal-title":"J Great Lakes Res"},{"issue":"12","key":"pone.0320395.ref015","doi-asserted-by":"crossref","first-page":"3383","DOI":"10.1007\/s10530-015-0964-6","article-title":"Acoustical deterrence of Silver Carp (Hypophthalmichthys molitrix)","volume":"17","author":"BJ Vetter","year":"2015","journal-title":"Biol Invasions"},{"issue":"3","key":"pone.0320395.ref016","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1111\/fme.12220","article-title":"Potential implications of acoustic stimuli as a non-physical barrier to silver carp and bighead carp","volume":"24","author":"KA Murchy","year":"2017","journal-title":"Fish Manage Ecol"},{"issue":"3","key":"pone.0320395.ref017","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0192561","article-title":"Reexamining the frequency range of hearing in silver (Hypophthalmichthys molitrix) and bighead (H. nobilis) carp","volume":"13","author":"BJ Vetter","year":"2018","journal-title":"PLoS One"},{"key":"pone.0320395.ref018","article-title":"Fish hearing \u201cspecialization\u201d\u2014-a re-evaluation","author":"AN Popper","year":"2021","journal-title":"Hear Res"},{"issue":"3","key":"pone.0320395.ref019","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.cbpa.2005.07.018","article-title":"The inner ear morphology and hearing abilities of the Paddlefish (Polyodon spathula) and the Lake Sturgeon (Acipenser fulvescens)","volume":"142","author":"JM Lovell","year":"2005","journal-title":"Comp Biochem Physiol A Mol Integr Physiol"},{"issue":"3","key":"pone.0320395.ref020","article-title":"Behavioral responses of native and invasive fishes of the Upper Mississippi River to 100 hp boat motor acoustic stimulus","volume":"13","author":"KA Murchy","year":"2022","journal-title":"Manage Biol Invasions"},{"issue":"3","key":"pone.0320395.ref021","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1002\/jez.10129","article-title":"Sensing and transfer of respiratory gases at the fish gill","volume":"293","author":"SF Perry","year":"2002","journal-title":"J Exp Zool"},{"key":"pone.0320395.ref022","doi-asserted-by":"crossref","first-page":"3133","DOI":"10.1007\/s10530-015-0941-0","article-title":"Molecular and behavioral responses of early-life stage fishes to elevated carbon dioxide","volume":"17","author":"CE Dennis","year":"2015","journal-title":"Biol Invasions"},{"issue":"3","key":"pone.0320395.ref023","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1080\/00028487.2016.1143397","article-title":"Carbon dioxide as a tool to deter the movement of invasive bigheaded carps","volume":"145","author":"MR Donaldson","year":"2016","journal-title":"Trans Am Fish Soc"},{"issue":"11","key":"pone.0320395.ref024","first-page":"1748","article-title":"Responses of native and invasive fishes to carbon dioxide: potential for a nonphysical barrier to fish dispersal. Can J Fish Aquatic Sci","volume":"69","author":"D Kates","year":"2012"},{"issue":"1","key":"pone.0320395.ref025","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.jglr.2020.10.004","article-title":"Telemetry evaluation of carbon dioxide as a behavioral deterrent for invasive carps","volume":"47","author":"AR Cupp","year":"2021","journal-title":"J Great Lakes Res"},{"issue":"6","key":"pone.0320395.ref026","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1139\/cjfas-2018-0026","article-title":"Avoidance of carbon dioxide in flowing water by bighead carp","volume":"76","author":"CT Hasler","year":"2019","journal-title":"Can J Fish Aquatic Sci"},{"issue":"3","key":"pone.0320395.ref027","first-page":"297","article-title":"Responses of invasive silver and bighead carp to a carbon dioxide barrier in outdoor ponds. Can J Fish Aquatic Sci","volume":"74","author":"AR Cupp","year":"2017"},{"issue":"4","key":"pone.0320395.ref028","article-title":"Emerging control strategies for integrated pest management of invasive carps","volume":"70","author":"AR Cupp","year":"2021","journal-title":"J Vertebr Biol"},{"key":"pone.0320395.ref029","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/s40462-023-00396-z","article-title":"Movement and behavioral states of common carp (Cyprinus carpio) in response to a behavioral deterrent in a navigational lock","volume":"11","author":"M Raboin","year":"2023","journal-title":"Mov Ecol"},{"issue":"4","key":"pone.0320395.ref030","doi-asserted-by":"crossref","DOI":"10.1061\/(ASCE)EE.1943-7870.0001987","article-title":"Performance of a Carbon Dioxide Injection System at a Navigation Lock to Control the Spread of Aquatic Invasive Species","volume":"148","author":"TJ Zolper","year":"2022","journal-title":"J Environ Eng"},{"issue":"3","key":"pone.0320395.ref031","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.jglr.2013.05.004","article-title":"Acoustical conditioning and retention in the common carp (Cyprinus carpio)","volume":"39","author":"JL Sloan","year":"2013","journal-title":"J Great Lakes Res"},{"key":"pone.0320395.ref032","doi-asserted-by":"crossref","first-page":"1505","DOI":"10.1007\/978-3-031-50256-9_36","article-title":"Acoustic and Carbon Dioxide Deterrents for Invasive Bigheaded Carps (Hypophthalmichthys molitrix and H. nobilis).","volume-title":"The effects of noise on aquatic life: principles and practical considerations","author":"J Culotta","year":"2024"},{"issue":"4","key":"pone.0320395.ref033","doi-asserted-by":"crossref","first-page":"1230","DOI":"10.1093\/icesjms\/fsw003","article-title":"Combined impacts of elevated CO2 and anthropogenic noise on European sea bass (Dicentrarchus labrax)","volume":"74","author":"DA Poulton","year":"2016","journal-title":"ICES J Mar Sci"},{"issue":"1875","key":"pone.0320395.ref034","first-page":"20172650","article-title":"Effect of elevated CO2 and small boat noise on the kinematics of predator-prey interactions","volume":"285","author":"MI McCormick","year":"2018","journal-title":"Proc Biol Sci"},{"issue":"3","key":"pone.0320395.ref035","first-page":"25","volume":"5","author":"CD Suski","year":"2020","journal-title":"Development of carbon dioxide barriers to deter invasive fishes: insights and lessons learned from bigheaded carp. Fishes"},{"issue":"6","key":"pone.0320395.ref036","doi-asserted-by":"crossref","first-page":"3073","DOI":"10.1121\/1.1515799","article-title":"Empirical refinements applicable to the recording of fish sounds in small tanks","volume":"112","author":"T Akamatsu","year":"2002","journal-title":"J Acoust Soc Am"},{"key":"pone.0320395.ref037","first-page":"933","article-title":"Parvulescu revisited: small tank acoustics for bioacousticians.","volume-title":"Effects of noise on aquatic life II. Advances in experimental medicine and biology","author":"PH Rogers","year":"2016"},{"key":"pone.0320395.ref038","first-page":"363","article-title":"\u201cLarge\u201d tank acoustics: how big is big enough? In: Popper AN, Hawkins A, editors. Effects of noise on aquatic life II","volume":"016","author":"MD Gray","year":"8752","journal-title":"Advances in experimental medicine and biology"},{"issue":"7","key":"pone.0320395.ref039","doi-asserted-by":"crossref","first-page":"2325","DOI":"10.1093\/icesjms\/fsab115","article-title":"Fish hearing and how it is best determined","volume":"78","author":"AN Popper","year":"2021","journal-title":"ICES J Mar Sci"},{"issue":"2","key":"pone.0320395.ref040","doi-asserted-by":"crossref","first-page":"948","DOI":"10.1121\/1.5120185","article-title":"Examining the hearing abilities of fishes","volume":"146","author":"AN Popper","year":"2019","journal-title":"J Acoust Soc Am"},{"issue":"3","key":"pone.0320395.ref041","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1016\/j.neubiorev.2006.10.006","article-title":"Evolutionary background for stress-coping styles: Relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates","volume":"31","author":"\u00d8 \u00d8verli","year":"2007","journal-title":"Neurosci Biobehav Rev"},{"issue":"2","key":"pone.0320395.ref042","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1007\/s10530-018-1842-9","article-title":"Glucocorticoid and behavioral variation in relation to carbon dioxide avoidance across two experiments in freshwater teleost fishes","volume":"21","author":"EK Tucker","year":"2019","journal-title":"Biol Invasions"},{"key":"pone.0320395.ref043","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.anbehav.2019.10.002","article-title":"Presence of conspecifics reduces between-individual variation and increases avoidance of multiple stressors in bluegill","volume":"158","author":"EK Tucker","year":"2019","journal-title":"Anim Behav"},{"issue":"1","key":"pone.0320395.ref044","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1006\/hbeh.2002.1796","article-title":"Effects of cortisol on aggression and locomotor activity in rainbow trout","volume":"42","author":"O Overli","year":"2002","journal-title":"Horm Behav"},{"key":"pone.0320395.ref045","doi-asserted-by":"crossref","DOI":"10.1016\/j.jenvman.2021.112720","article-title":"Exploring how vessel activity influences the soundscape at a navigation lock on the Mississippi River","volume":"296","author":"RL Putland","year":"2021","journal-title":"J Environ Manage"},{"key":"pone.0320395.ref046","volume-title":"Fishing down the bighead and silver carps: Reducing the risk of invasion to the Great Lakes","author":"JE Garvey","year":"2012"},{"issue":"7","key":"pone.0320395.ref047","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.1111\/j.1095-8649.2010.02585.x","article-title":"Salinity selection and preference of the grey snapper Lutjanus griseus: field and laboratory observations","volume":"76","author":"X Serrano","year":"2010","journal-title":"J Fish Biol"},{"key":"pone.0320395.ref048","volume-title":"Chemotaxis and phonotaxis in a two-choice shuttle tank by bigheaded carps","author":"J Culotta","year":"2023"},{"issue":"11","key":"pone.0320395.ref049","doi-asserted-by":"crossref","first-page":"2247","DOI":"10.1002\/etc.4855","article-title":"Toxicity of carbon dioxide to freshwater fishes: implications for aquatic invasive species management","volume":"39","author":"AR Cupp","year":"2020","journal-title":"Environ Toxicol Chem"},{"issue":"11","key":"pone.0320395.ref050","doi-asserted-by":"crossref","first-page":"3095","DOI":"10.1007\/s10530-018-1761-9","article-title":"Temperature dependent effects of carbon dioxide on avoidance behaviors in bigheaded carps","volume":"20","author":"JA Tix","year":"2018","journal-title":"Biol Invasions"},{"issue":"9","key":"pone.0320395.ref051","article-title":"Quantifying p CO2 in biological ocean acidification experiments: a comparison of four methods","volume":"12","author":"S-A Watson","year":"2017","journal-title":"PLoS One"},{"issue":"1","key":"pone.0320395.ref052","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1002\/eco.95","article-title":"Direct and continuous measurement of dissolved carbon dioxide in freshwater aquatic systems-method and applications","volume":"3","author":"MS Johnson","year":"2010","journal-title":"Ecohydrology"},{"issue":"3","key":"pone.0320395.ref053","first-page":"234","article-title":"Use of avoidance response by rainbow trout to carbon dioxide for fish self-transfer between tanks. 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