{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,20]],"date-time":"2026-08-20T05:23:32Z","timestamp":1787203412153,"version":"build-2736575974"},"reference-count":38,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T00:00:00Z","timestamp":1787011200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100005825","name":"USDA National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["1019561"],"award-info":[{"award-number":["1019561"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]},{"award":["1019561"],"award-info":[{"award-number":["1019561"]}],"id":[{"id":"https:\/\/ror.org\/05qx3fv49","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/100026154","name":"Cherokee Nation of Oklahoma","doi-asserted-by":"crossref","award":["PO272913"],"award-info":[{"award-number":["PO272913"]}],"id":[{"id":"10.13039\/100026154","id-type":"DOI","asserted-by":"crossref"}]},{"award":["PO272913"],"award-info":[{"award-number":["PO272913"]}],"id":[{"id":"https:\/\/ror.org\/00p23dy23","id-type":"ROR","asserted-by":"publisher"}]},{"name":"Oklahoma Military Department Directorate of Facility Management Cooperative Agreement","award":["#0259007642"],"award-info":[{"award-number":["#0259007642"]}]},{"name":"Neustadt\u2013Sarkeys Endowed Professorship"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Most species within the genus Nicrophorus (Staphylinidae: Silphinae: Necrophorini) overwinter as adults during cold months. However, species that were once widely distributed, such as the American burying beetle, Nicrophorus americanus Olivier, experience different overwintering conditions, altered by increasing climate variability, making cold periods less predictable. In this study, we determined the mean super-cooling point of Oklahoma N. americanus to be \u22121.98 \u00b0C, a value that suggests that beetles rely on behavioral avoidance of freezing soils rather than on physiological freeze tolerance or super-cooling. We conducted a series of field experiments in Oklahoma to test the effects of habitat and burial depth on the overwintering survival of N. americanus. Correlations were found between burial depth and the survival of beetles. Highly fluctuating winter temperatures and periods without precipitation increased mortality rates, with adults emerging from overwintering much earlier than previously documented. As climates become warmer and more variable, with temperature fluctuations and altered precipitation patterns, populations of the federally designated threatened N. americanus are at risk of extirpation.<\/jats:p>","DOI":"10.3390\/biology15161417","type":"journal-article","created":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T08:08:41Z","timestamp":1787040521000},"page":"1417","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Super-Cooling Point and Effects of Temperature, Moisture, and Habitat on Overwintering Survival of the Threatened American Burying Beetle Nicrophorus americanus"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8927-9102","authenticated-orcid":false,"given":"William Wyatt","family":"Hoback","sequence":"first","affiliation":[{"name":"Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amelea","family":"Jones","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leonardo Vieira","family":"Santos","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5821-0153","authenticated-orcid":false,"given":"Rafael","family":"Hayashida","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2836-8398","authenticated-orcid":false,"given":"Michael","family":"Cavallaro","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,18]]},"reference":[{"key":"ref_1","unstructured":"Leather, S.R., Walters, K.F.A., and Bale, J.S. (1995). The Ecology of Insect Overwintering, Cambridge University Press."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1098\/rstb.1990.0035","article-title":"Cold Tolerance of Insects and Other Arthropods","volume":"326","author":"Block","year":"1990","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_3","first-page":"751","article-title":"Classes of Insect Cold Hardiness","volume":"7","author":"Bale","year":"1993","journal-title":"Funct. Ecol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"308","DOI":"10.2307\/1311113","article-title":"Insect Cold-Hardiness: To Freeze or Not to Freeze","volume":"39","author":"Lee","year":"1989","journal-title":"BioScience"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1016\/0022-1910(87)90001-1","article-title":"Insect Cold Hardiness: Freezing and Supercooling\u2014An Ecophysiological Perspective","volume":"33","author":"Bale","year":"1987","journal-title":"J. Insect Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Denlinger, D.L., and Lee, R.E. (2010). Low Temperature Biology of Insects, Cambridge University Press.","DOI":"10.1017\/CBO9780511675997"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1146\/annurev.en.06.010161.000415","article-title":"Principles of Insect Cold-Hardiness","volume":"6","author":"Salt","year":"1961","journal-title":"Annu. Rev. Entomol."},{"key":"ref_8","first-page":"73","article-title":"Loss of Supercooling Ability in Cryptopygus antarcticus (Collembola: Isotomidae) Associated with Water Uptake","volume":"6","author":"Cannon","year":"1985","journal-title":"CryoLetters"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Franks, F. (1982). Supercooled Water. Water and Aqueous Solutions at Subzero Temperatures, Springer.","DOI":"10.1007\/978-1-4757-6952-4"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"983","DOI":"10.4039\/Ent103983-7","article-title":"Physiological Classification of Dormancies in Insects","volume":"103","author":"Mansingh","year":"1971","journal-title":"Can. Entomol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1017\/S1464793102006024","article-title":"Climatic Variability and Insect Freeze Tolerance","volume":"78","author":"Sinclair","year":"2003","journal-title":"Biol. Rev."},{"key":"ref_12","first-page":"157","article-title":"Insect Cold Tolerance: How Many Kinds of Frozen?","volume":"96","author":"Sinclair","year":"1999","journal-title":"Eur. J. Entomol."},{"key":"ref_13","unstructured":"Tauber, M.J., Tauber, C.A., and Masaki, S. (1986). Seasonal Adaptations of Insects, Oxford University Press."},{"key":"ref_14","first-page":"144","article-title":"Evolutionary Adaptation to Temperature","volume":"57","author":"Bennett","year":"2003","journal-title":"Evolution"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1146\/annurev.ento.43.1.595","article-title":"The Ecology and Behavior of Burying Beetles","volume":"43","author":"Scott","year":"1998","journal-title":"Annu. Rev. Entomol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1007\/s10841-007-9086-5","article-title":"Provisioning Effects on Overwinter Survival of the American Burying Beetle","volume":"12","author":"Schnell","year":"2008","journal-title":"J. Insect Conserv."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1588","DOI":"10.1139\/z02-151","article-title":"Effect of Larval Body Size on Overwinter Survival and Emerging Adult Size in the Burying Beetle, Nicrophorus investigator","volume":"80","author":"Smith","year":"2002","journal-title":"Can. J. Zool."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1023\/A:1009684926873","article-title":"Distribution, Ecology, and Population Dynamics of the American Burying Beetle [Nicrophorus americanus Olivier (Coleoptera, Silphidae)] in South-Central Nebraska, USA","volume":"3","author":"Bedick","year":"1999","journal-title":"J. Insect Conserv."},{"key":"ref_19","first-page":"362","article-title":"Causes of Rapid Carrion Beetle (Coleoptera: Silphidae) Death in Flooded Pitfall Traps, Response to Soil Flooding, Immersion Tolerance, and Swimming Behavior","volume":"46","author":"Cavallaro","year":"2017","journal-title":"Environ. Entomol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s10841-017-9955-5","article-title":"Distribution and Habitat of Endangered American Burying Beetle in Northern and Southern Regions","volume":"21","author":"Leasure","year":"2017","journal-title":"J. Insect Conserv."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"McMurry, R.S., Cavallaro, M.C., Shufran, A., and Hoback, W.W. (2023). Establishing Age-Based Color Changes for the American Burying Beetle, Nicrophorus americanus Olivier, with Implications for Conservation Efforts. Insects, 14.","DOI":"10.3390\/insects14110844"},{"key":"ref_22","unstructured":"U.S. Fish and Wildlife Service (2019). Species Status Assessment Report for the American Burying Beetle (Nicrophorus americanus)."},{"key":"ref_23","unstructured":"Hoback, W.W., and Conley, A. (2014). Overwintering Biology and Tests of Trap and Relocate as a Conservation Measure for Burying Beetles, University of Nebraska. Nebraska Department of Transportation Research Reports."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1242\/jeb.037911","article-title":"Insect Overwintering in a Changing Climate","volume":"213","author":"Bale","year":"2010","journal-title":"J. Exp. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1007\/s10841-010-9372-5","article-title":"Combined Effects of Overwintering Temperature and Habitat Degradation on the Survival of Boreal Wood Ant","volume":"15","author":"Sorvari","year":"2011","journal-title":"J. Insect Conserv."},{"key":"ref_26","first-page":"155","article-title":"A Simple Method to Adjust Cooling Rates for Supercooling Point Determination","volume":"25","author":"Carrillo","year":"2004","journal-title":"Cryoletters"},{"key":"ref_27","unstructured":"Systat Software, Inc. (2014). SigmaPlot, Systat Software, Inc."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1111\/een.13201","article-title":"A Test of the Competitive Ability\u2013Cold Tolerance Trade-off Hypothesis in Seasonally Breeding Beetles","volume":"48","author":"Wettlaufer","year":"2022","journal-title":"Ecol. Entomol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1111\/1744-7917.12321","article-title":"Impact of Cold on the Immune System of Burying Beetle, Nicrophorus vespilloides (Coleoptera: Silphidae)","volume":"24","author":"Czarniewska","year":"2017","journal-title":"Insect Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"104063","DOI":"10.1016\/j.jtherbio.2025.104063","article-title":"The Role of Life Stage and Season in Critical Thermal Limits of Carrion Beetles","volume":"127","author":"Garfinkel","year":"2025","journal-title":"J. Therm. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1134\/S0013873817050025","article-title":"Overwintering Ecology of Philonthus rotundicollis (Coleoptera, Staphylinidae) in the Nest of the Carpenter Ant Camponotus herculeanus on the Coast of the Sea of Okhotsk","volume":"97","author":"Zhigulskaya","year":"2017","journal-title":"Entmol. Rev."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.cois.2020.06.003","article-title":"Evolutionary Impacts of Winter Climate Change on Insects","volume":"41","author":"Marshall","year":"2020","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_33","unstructured":"Pipino, J.A. (2024). Factors Impacting the Post Release Viability of American Burying Beetle (Nicrophorus americanus Oliver) to New York. [Master\u2019s Thesis, State University of New York at Oneonta]."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1111\/brv.12105","article-title":"Cold Truths: How Winter Drives Responses of Terrestrial Organisms to Climate Change","volume":"90","author":"Williams","year":"2015","journal-title":"Biol. Rev."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.jtherbio.2014.07.007","article-title":"Linking Energetics and Overwintering in Temperate Insects","volume":"54","author":"Sinclair","year":"2015","journal-title":"J. Therm. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1151","DOI":"10.1111\/1365-2435.14037","article-title":"Longer and Warmer Prewinter Periods Reduce Post-winter Fitness in a Diapausing Insect","volume":"36","author":"Nielsen","year":"2022","journal-title":"Funct. Ecol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/s00114-011-0866-0","article-title":"Threshold Temperatures Mediate the Impact of Reduced Snow Cover on Overwintering Freeze-Tolerant Caterpillars","volume":"99","author":"Marshall","year":"2012","journal-title":"Naturwissenschaften"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/S0167-8809(99)00130-9","article-title":"Overwintering of Arthropods in Soils of Arable Fields and Adjacent Semi-Natural Habitats","volume":"78","author":"Pfiffner","year":"2000","journal-title":"Agric. Ecosyst. Environ."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/16\/1417\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,20]],"date-time":"2026-08-20T04:25:45Z","timestamp":1787199945000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/16\/1417"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,18]]},"references-count":38,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["biology15161417"],"URL":"https:\/\/doi.org\/10.3390\/biology15161417","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,18]]}}}