{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T18:03:57Z","timestamp":1789581837941,"version":"build-2803163510"},"reference-count":49,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T00:00:00Z","timestamp":1789516800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>\n                    Advancements in thermal management systems often rely on incorporating novel design features which can be effectively influenced through bioinspiration. A major gap in applying bioinspired concepts to thermal design is the identification of morphological structures of interest due to the multimodal nature of most energy transfer systems. Investigating species along an operative temperature gradient\u2014which incorporates convective and radiative heat transfer\u2014offers a more comprehensive view of environmental heat load than traditional ambient air temperature or latitude, providing better granularity to identify phenotypic plasticity driven by heat load. This study refined a thermally oriented bioinspiration search method by clustering species spatial group locations based on growing season operative temperature distributions. Focusing on the North American tree species\n                    <jats:italic>Populus heterophylla<\/jats:italic>\n                    , thermal clines were developed using a density-based cluster analysis utilizing ERA5-Land climate data to evaluate both 2-meter air temperatures and calculated operative temperatures. To evaluate phenotypic trends across these thermal regimes, 2D leaf margins from 103 herbarium specimens were analyzed for aspect ratio, leaf width, and non-dimensionalized characteristic edge radius. While ambient air temperature clustering yielded only two broad regional groups, operative temperature mapping provided greater environmental granularity, resolving four distinct spatial groups, including unique mid-latitude and coastal sub-populations. Specimen analysis revealed that cooler-climate groups exhibited smaller edge radii (higher margin dissection) than warmer-climate groups, with intermediate clusters displaying transitional values between the extreme ranges. These results demonstrate that operative temperature space offers an improved framework for identifying candidate morphological features associated with regional thermal environments, laying a foundation to test potential heat-transfer adaptations for engineering design.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0358463","type":"journal-article","created":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T17:36:46Z","timestamp":1789580206000},"page":"e0358463","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Beyond air temperature: An examination of leveraging operative temperature space for the discovery of bioinspired thermal design features"],"prefix":"10.1371","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0009-0005-9450-3040","authenticated-orcid":true,"given":"Thomas N.","family":"Slavens","sequence":"first","affiliation":[{"name":"College of Aerospace and Mechanical Engineering, University of Oklahoma","place":["Norman, Oklahoma, United States of America"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hamid","family":"Shabgard","sequence":"additional","affiliation":[{"name":"College of Aerospace and Mechanical Engineering, University of Oklahoma","place":["Norman, Oklahoma, United States of America"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,9,16]]},"reference":[{"key":"pone.0358463.ref001","unstructured":"Yeh FCaSFS. Review and status of heat-transfer technology for internal passages of air-cooled turbine blades. 1984."},{"key":"pone.0358463.ref002","unstructured":"Blake M, Osborne L, Slavens T, inventors. Gas turbine engine component having curved turbulator. United States patent 10316668. 2019."},{"key":"pone.0358463.ref003","unstructured":"Lee CP, inventor. Turbine airfoil with an internal cooling system having vortex forming turbulators. United States patent 8920122. 2014."},{"key":"pone.0358463.ref004","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-84628-319-2","volume-title":"Engineering Design: A Systematic Approach","author":"G Pahl","year":"2007"},{"key":"pone.0358463.ref005","doi-asserted-by":"crossref","unstructured":"Slavens T, Shabgard H. Development of a Bioinpsiration Search Method in Thermal Design. In Proceedings of the 10th World Congress on Momentum, Heat and Mass Transfer. Barcelona, Spain; 2025.","DOI":"10.11159\/enfht25.179"},{"issue":"4","key":"pone.0358463.ref006","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1007\/s10798-010-9132-6","article-title":"Introducing students to bio-inspiration and biomimetic design: a workshop experience","volume":"21","author":"C Santulli","year":"2011","journal-title":"Int J Technol Des Educ"},{"key":"pone.0358463.ref007","first-page":"408","article-title":"Beautiful and Functional: A Review of Biomimetic Design in Additive Manufacturing","volume":"27","author":"A du Plessis","year":"2019","journal-title":"Addit Manuf"},{"issue":"2","key":"pone.0358463.ref008","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1680\/jbibn.16.00010","article-title":"Biomimetics and its tools","volume":"6","author":"K Wanieck","year":"2017","journal-title":"Bioinspired Biomim Nanobiomaterials"},{"issue":"2","key":"pone.0358463.ref009","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.destud.2009.10.003","article-title":"The effects of biological examples in idea generation","volume":"31","author":"JO Wilson","year":"2010","journal-title":"Des Stud"},{"issue":"3","key":"pone.0358463.ref010","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1017\/S0094837300019746","article-title":"When are leaves good thermometers? A new case for Leaf Margin Analysis","volume":"23","author":"P Wilf","year":"1997","journal-title":"Paleobiology"},{"issue":"2","key":"pone.0358463.ref011","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1669\/0883-1351(2004)019<0129:PEULAI>2.0.CO;2","article-title":"Paleotemperature Estimation Using Leaf-Margin Analysis: Is Australia Different?","volume":"19","author":"DR Greenwood","year":"2004","journal-title":"Palaios"},{"issue":"5","key":"pone.0358463.ref012","doi-asserted-by":"crossref","first-page":"498","DOI":"10.2110\/palo.2004.P04-58","article-title":"Leaf Margin Analysis: Taphonomic Constraints","volume":"20","author":"DR Greenwood","year":"2005","journal-title":"Palaios"},{"issue":"3","key":"pone.0358463.ref013","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1111\/j.1469-8137.2010.03615.x","article-title":"Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications","volume":"190","author":"DJ Peppe","year":"2011","journal-title":"New Phytol"},{"issue":"5","key":"pone.0358463.ref014","doi-asserted-by":"crossref","first-page":"915","DOI":"10.3732\/ajb.1100428","article-title":"Roles of climate and functional traits in controlling toothed vs. untoothed leaf margins","volume":"99","author":"DL Royer","year":"2012","journal-title":"Am J Bot"},{"issue":"10","key":"pone.0358463.ref015","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0007653","article-title":"Phenotypic plasticity of leaf shape along a temperature gradient in Acer rubrum","volume":"4","author":"DL Royer","year":"2009","journal-title":"PLoS One"},{"issue":"1","key":"pone.0358463.ref016","first-page":"208747","article-title":"Plant phenotypic plasticity in response to environmental factors","volume":"2014","author":"L Gratani","year":"2014","journal-title":"Adv Bot"},{"issue":"3","key":"pone.0358463.ref017","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1007\/BF00389024","article-title":"Convective heat transfer characteristics of toothed leaves","volume":"53","author":"DE Gottschlich","year":"1982","journal-title":"Oecologia"},{"issue":"2","key":"pone.0358463.ref018","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1093\/jxb\/27.2.231","article-title":"The Boundary Layer over aPopulusLeaf","volume":"27","author":"J Grace","year":"1976","journal-title":"J Exp Bot"},{"issue":"1","key":"pone.0358463.ref019","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1086\/497995","article-title":"Why Do Toothed Leaves Correlate with Cold Climates? Gas Exchange at Leaf Margins Provides New Insights into a Classic Paleotemperature Proxy","volume":"167","author":"DL Royer","year":"2006","journal-title":"Int J Plant Sci"},{"issue":"6","key":"pone.0358463.ref020","doi-asserted-by":"crossref","first-page":"723","DOI":"10.3390\/atmos12060723","article-title":"ECLand: The ECMWF Land Surface Modelling System","volume":"12","author":"S Boussetta","year":"2021","journal-title":"Atmosphere"},{"key":"pone.0358463.ref021","volume-title":"Heat Transmission","author":"WH McAdams","year":"1954","edition":"3"},{"key":"pone.0358463.ref022","doi-asserted-by":"crossref","unstructured":"Marshall JL, Williams P, Rheault JP, Prochaska T, Allen RD, DePoy DL. Characterization of the reflectivity of various black materials. In: Ground-based and Airborne Instrumentation for Astronomy V. 2014;9147:1459\u201366.","DOI":"10.1117\/12.2056729"},{"key":"pone.0358463.ref023","author":"EL Little","year":"1971","journal-title":"Atlas of United States Trees"},{"key":"pone.0358463.ref024","unstructured":"Ester M, Kriegel HP, Sander J, Xiaowei X. A density-based algorithm for discovering clusters in large spatial databases with noise. In: Proceedings of the Second International Conference on Knowledge Discovery in Databases and Data Mining. Portland (OR); 1996. p. 226\u201331."},{"issue":"5","key":"pone.0358463.ref025","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.tree.2022.11.015","article-title":"The herbarium of the future","volume":"38","author":"CC Davis","year":"2023","journal-title":"Trends Ecol Evol"},{"issue":"209","key":"pone.0358463.ref026","doi-asserted-by":"crossref","first-page":"7","DOI":"10.3897\/zookeys.209.3313","article-title":"Mass digitization of scientific collections: New opportunities to transform the use of biological specimens and underwrite biodiversity science","author":"RS Beaman","year":"2012","journal-title":"Zookeys"},{"issue":"7","key":"pone.0358463.ref027","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1016\/j.tree.2017.03.015","article-title":"Old Plants, New Tricks: Phenological Research Using Herbarium Specimens","volume":"32","author":"CG Willis","year":"2017","journal-title":"Trends Ecol Evol"},{"issue":"4","key":"pone.0358463.ref028","doi-asserted-by":"crossref","first-page":"512","DOI":"10.3732\/ajb.93.4.512","article-title":"A new herbarium-based method for reconstructing the phenology of plant species across large areas","volume":"93","author":"C Lavoie","year":"2006","journal-title":"Am J Bot"},{"issue":"1","key":"pone.0358463.ref029","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.ppees.2012.10.002","article-title":"Biological collections in an ever changing world: herbaria as tools for biogeographical and environmental studies","volume":"15","author":"C Lavoie","year":"2013","journal-title":"Perspect Plant Ecol Evol Syst"},{"issue":"1","key":"pone.0358463.ref030","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1111\/nph.15401","article-title":"Using herbaria to study global environmental change","volume":"221","author":"PLM Lang","year":"2019","journal-title":"New Phytol"},{"key":"pone.0358463.ref031","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1080\/23818107.2018.1451775","article-title":"On the use of herbarium specimens for morphological and anatomical research","volume":"165","author":"F Espinosa","year":"2018","journal-title":"Bot Lett"},{"issue":"3","key":"pone.0358463.ref032","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1007\/s00442-017-3964-7","article-title":"Drier climate shifts leaf morphology in Amazonian trees","volume":"185","author":"J Stropp","year":"2017","journal-title":"Oecologia"},{"issue":"7","key":"pone.0358463.ref033","doi-asserted-by":"crossref","DOI":"10.1111\/njb.04211","article-title":"Dressed for the occasion! Ecotypic divergence, phenotypic plasticity and taxonomic value of capitulum characters of Scorzoneroides autumnalis (Asteraceae)","volume":"2024","author":"GV Ingimundard\u00f3ttir","year":"2024","journal-title":"Nordic J Bot"},{"issue":"7","key":"pone.0358463.ref034","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1046\/j.1365-2699.2003.00897.x","article-title":"Reconstructing the spread of invasive plants: taking into account biases associated with herbarium specimens","volume":"30","author":"F Delisle","year":"2003","journal-title":"J Biogeogr"},{"key":"pone.0358463.ref035","unstructured":"TORCH Portal. The Texas Oklahoma Regional Consortium of Herbaria [Online]. 2025 [cited 2025 October 20. Available from: http\/\/:portal.torcherbaria.org\/portal\/index.php"},{"key":"pone.0358463.ref036","unstructured":"KANU Vascular Plants Collection. R. L. McGregor Herbarium Vascular Plants Collection [Online]. 2025 [cited 2025 October 20]. Available from: https:\/\/biodiversity.ku.edu\/botany\/vascular-plant-collection"},{"key":"pone.0358463.ref037","unstructured":"Connecticut Uo. Biodiversity Research Collections [Online]. 2026 [cited 2025 October]. Available from: https:\/\/search.biodiversity.uconn.edu\/SimpleSearch.html"},{"key":"pone.0358463.ref038","volume-title":"The complete trees of North America. Field guide and natural history","author":"TS Elias","year":"1981"},{"key":"pone.0358463.ref039","volume-title":"Fundamentals of Computer Numerical Control","author":"WW Luggen","year":"1994","edition":"3"},{"key":"pone.0358463.ref040","unstructured":"Martin TJ, Staroselsky A, Zelesky MF, Slavens TN, inventors. United States of America patent 9,091,176. 2015."},{"key":"pone.0358463.ref041","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/j.crme.2011.11.004","article-title":"Control of the separated flow around an airfoil using a wavy leading edge inspired by humpback whale flippers","volume":"340","author":"J Favier","year":"2012","journal-title":"Comptes Rendus M\u00e9canique"},{"key":"pone.0358463.ref042","article-title":"Numerical simulation of the effect of leading-edge tubercles on the flow characteristics around an airfoil.","author":"AFA Gawad","year":"2012","journal-title":"International Mechnaical Engineering Congresss & Exposition"},{"issue":"5","key":"pone.0358463.ref043","doi-asserted-by":"crossref","DOI":"10.1063\/1.1688341","article-title":"Leading-edge tubercles delay stall on humpback whale (Megaptera novaeangliae) flippers","volume":"16","author":"DS Miklosovic","year":"2004","journal-title":"Phys Fluids"},{"key":"pone.0358463.ref044","article-title":"Optimal Configuration of Integrated Bio-Inspired Humpback Whale Flippers Shaped Metallic Plates in a Cross-Flow Heat Exchanger: A CFD based Comparative Analysis.","volume-title":"3rd International Conference on Mechanical, Manufacturing and Process Engineering","author":"S Rahman","year":"2026"},{"key":"pone.0358463.ref045","volume-title":"Populus heterophylla L., Swamp cottonwood. Consveration and Research Plan","author":"RT McMaster","year":"2003"},{"issue":"12","key":"pone.0358463.ref046","doi-asserted-by":"crossref","first-page":"1869","DOI":"10.1111\/ddi.12815","article-title":"Plant niche breadths along environmental gradients and their relationship to plant functional traits","volume":"24","author":"D Schellenberger Costa","year":"2018","journal-title":"Divers Distrib"},{"issue":"3","key":"pone.0358463.ref047","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/j.1469-8137.1990.tb00404.x","article-title":"Tansley Review No. 22 What becomes of the transpiration stream?","volume":"114","author":"MJ Canny","year":"1990","journal-title":"New Phytol"},{"key":"pone.0358463.ref048","unstructured":"Martin TJ, Staroselsky A, Slavens TN, Zelesky MF, Wagner JH, inventors. United States of America patent US9109452B2. 2015."},{"issue":"1","key":"pone.0358463.ref049","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1146\/annurev.pp.19.060168.001235","article-title":"Transpiration and Leaf Temperature","volume":"19","author":"DM Gates","year":"1968","journal-title":"Annu Rev Plant Physiol"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0358463","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T17:36:58Z","timestamp":1789580218000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0358463"}},"subtitle":[],"editor":[{"given":"Mohammad","family":"Zuber","sequence":"first","affiliation":[{"name":"Manipal Academy of Higher Education","place":["INDIA"]}],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,9,16]]},"references-count":49,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,9,16]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0358463","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,16]]}}}