{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,5]],"date-time":"2026-02-05T10:43:33Z","timestamp":1770288213330,"version":"3.49.0"},"reference-count":69,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2022,2,8]],"date-time":"2022-02-08T00:00:00Z","timestamp":1644278400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["42001373"],"award-info":[{"award-number":["42001373"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Remote Sensing"],"abstract":"<jats:p>Climate change is transforming winter environmental conditions rapidly. Shifts in snow regimes and freeze\/thaw cycles that are unique to the harsh winter season can strongly influence ecological processes and biodiversity patterns of mammals and birds. However, the role of the winter environment in structuring a species richness pattern is generally downplayed, especially in temperate regions. Here we developed a suite of winter habitat indices at 500 m spatial resolution by fusing MODIS snow products and NASA MEaSUREs daily freeze\/thaw records from passive microwave sensors and tested how these indices could improve the explanation of species richness patterns across China. We found that the winter habitat indices provided unique and mutually complementary environmental information compared to the commonly used Dynamic Habitat Indices (DHIs). Winter habitat indices significantly increased the explanatory power for species richness of all mammal and bird groups. Particularly, winter habitat indices contributed more to the explanation of bird species than mammals. Regarding the independent contribution, winter season length made the largest contributions to the explained variance of winter birds (30%), resident birds (27%), and mammals (18%), while the frequency of snow-free frozen ground contributed the most to the explanation of species richness for summer birds (23%). Our research provides new insights into the interpretation of broad-scale species diversity, which has great implications for biodiversity assessment and conservation.<\/jats:p>","DOI":"10.3390\/rs14030794","type":"journal-article","created":{"date-parts":[[2022,2,8]],"date-time":"2022-02-08T23:42:20Z","timestamp":1644363740000},"page":"794","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Remotely Sensed Winter Habitat Indices Improve the Explanation of Broad-Scale Patterns of Mammal and Bird Species Richness in China"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4777-4129","authenticated-orcid":false,"given":"Likai","family":"Zhu","sequence":"first","affiliation":[{"name":"Shandong Provincial Key Laboratory of Water and Soil Conservation and Environmental Protection, College of Resources and Environment, Linyi University, Linyi 276000, China"}]},{"given":"Yuanyuan","family":"Guo","sequence":"additional","affiliation":[{"name":"Shandong Provincial Key Laboratory of Water and Soil Conservation and Environmental Protection, College of Resources and Environment, Linyi University, Linyi 276000, China"}]}],"member":"1968","published-online":{"date-parts":[[2022,2,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1038\/35012241","article-title":"Consequences of changing biodiversity","volume":"405","author":"Chapin","year":"2000","journal-title":"Nature"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e1400253","DOI":"10.1126\/sciadv.1400253","article-title":"Accelerated modern human-induced species loss: Entering the sixth mass extinction","volume":"1","author":"Ceballos","year":"2015","journal-title":"Sci. Adv."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nature11148","article-title":"Biodiversity loss and its impact on humanity","volume":"486","author":"Cardinale","year":"2012","journal-title":"Nature"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1038\/nature19092","article-title":"Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality","volume":"536","author":"Soliveres","year":"2016","journal-title":"Nature"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1038\/s41559-019-0826-1","article-title":"Essential biodiversity variables for mapping and monitoring species populations","volume":"3","author":"Jetz","year":"2019","journal-title":"Nat. Ecol. Evol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Wu, J., and Liang, S. (2018). Developing an integrated remote sensing based biodiversity index for predicting animal species richness. Remote Sens., 10.","DOI":"10.3390\/rs10050739"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3105","DOI":"10.1890\/03-8006","article-title":"Energy, water and broad-scale geographic patterns of species richness","volume":"84","author":"Hawkins","year":"2003","journal-title":"Ecology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1016\/j.rse.2018.12.009","article-title":"The Dynamic Habitat Indices (DHIs) from MODIS and global biodiversity","volume":"222","author":"Radeloff","year":"2019","journal-title":"Remote Sens. Environ."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Luo, Z., Tang, S., Li, C., Fang, H., Hu, H., Yang, J., Ding, J., and Jiang, Z. (2012). Environmental effects on vertebrate species richness: Testing the energy, environmental stability and habitat heterogeneity hypotheses. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0035514"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2241","DOI":"10.1890\/11-1861.1","article-title":"What is the form of the productivity\u2013animal-species-richness relationship? A critical review and meta-analysis","volume":"93","author":"Currie","year":"2012","journal-title":"Ecology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1147","DOI":"10.1111\/ecog.02813","article-title":"Disentangling vegetation and climate as drivers of Australian vertebrate richness","volume":"41","author":"Coops","year":"2018","journal-title":"Ecography"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1111\/j.1461-0248.2004.00671.x","article-title":"Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness","volume":"7","author":"Currie","year":"2004","journal-title":"Ecol. Lett."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1016\/j.rse.2008.11.012","article-title":"Exploring the relative importance of satellite-derived descriptors of production, topography and land cover for predicting breeding bird species richness over Ontario, Canada","volume":"113","author":"Coops","year":"2009","journal-title":"Remote Sens. Environ."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Zhang, C., Cai, D., Li, W., Guo, S., Guan, Y., Bian, X., and Yao, W. (2017). Effect of the Long-Term Mean and the Temporal Stability of Water-Energy Dynamics on China\u2019s Terrestrial Species Richness. ISPRS Int. J. Geo-Inf., 6.","DOI":"10.3390\/ijgi6030058"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1329","DOI":"10.1111\/geb.12365","article-title":"A global, remote sensing-based characterization of terrestrial habitat heterogeneity for biodiversity and ecosystem modelling","volume":"24","author":"Tuanmu","year":"2015","journal-title":"Glob. Ecol. Biogeogr."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1016\/j.ecolind.2017.09.055","article-title":"Remotely sensed spatial heterogeneity as an exploratory tool for taxonomic and functional diversity study","volume":"85","author":"Rocchini","year":"2018","journal-title":"Ecol. Indic."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4302","DOI":"10.1002\/joc.5086","article-title":"WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas","volume":"37","author":"Fick","year":"2017","journal-title":"Int. J. Climatol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"170078","DOI":"10.1038\/sdata.2017.78","article-title":"MERRAclim, a high-resolution global dataset of remotely sensed bioclimatic variables for ecological modelling","volume":"4","author":"Vega","year":"2017","journal-title":"Sci. Data"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"112309","DOI":"10.1016\/j.rse.2021.112309","article-title":"Winter Habitat Indices (WHIs) for the contiguous US and their relationship with winter bird diversity","volume":"255","author":"Keyser","year":"2021","journal-title":"Remote Sens. Environ."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.rse.2017.04.018","article-title":"A comparison of Dynamic Habitat Indices derived from different MODIS products as predictors of avian species richness","volume":"195","author":"Hobi","year":"2017","journal-title":"Remote Sens. Environ."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.ecoinf.2014.10.006","article-title":"Advancing species diversity estimate by remotely sensed proxies: A conceptual review","volume":"25","author":"Rocchini","year":"2015","journal-title":"Ecol. Inform."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1111\/2041-210X.12545","article-title":"How do we want Satellite Remote Sensing to support biodiversity conservation globally?","volume":"7","author":"Pettorelli","year":"2016","journal-title":"Methods Ecol. Evol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1086\/285144","article-title":"Energy and large-scale patterns of animal and plant species richness","volume":"137","author":"Currie","year":"1991","journal-title":"Am. Nat."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"105567","DOI":"10.1016\/j.ecolind.2019.105567","article-title":"Untangling multiple species richness hypothesis globally using remote sensing habitat indices","volume":"107","author":"Coops","year":"2019","journal-title":"Ecol. Indic."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"111306","DOI":"10.1016\/j.rse.2019.111306","article-title":"Tropical bird species richness is strongly associated with patterns of primary productivity captured by the Dynamic Habitat Indices","volume":"232","author":"Suttidate","year":"2019","journal-title":"Remote Sens. Environ."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Zhang, C., Cai, D., Guo, S., Guan, Y., Fraedrich, K., Nie, Y., Liu, X., and Bian, X. (2016). Spatial-Temporal Dynamics of China\u2019s Terrestrial Biodiversity: A Dynamic Habitat Index Diagnostic. Remote Sens., 8.","DOI":"10.3390\/rs8030227"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1939","DOI":"10.1890\/09-1160.1","article-title":"Winter climate change: A critical factor for temperate vegetation performance","volume":"91","author":"Kreyling","year":"2010","journal-title":"Ecology"},{"key":"ref_28","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_29","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.fooweb.2017.02.006","article-title":"Winter is changing: Trophic interactions under altered snow regimes","volume":"13","author":"Penczykowski","year":"2017","journal-title":"Food Webs"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1038\/s41558-019-0588-4","article-title":"Climate change causes functionally colder winters for snow cover-dependent organisms","volume":"9","author":"Zhu","year":"2019","journal-title":"Nat. Clim. Chang."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1890\/120222","article-title":"The subnivium: A deteriorating seasonal refugium","volume":"11","author":"Pauli","year":"2013","journal-title":"Front. Ecol. Environ."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.rse.2017.01.020","article-title":"Characterizing global patterns of frozen ground with and without snow cover using microwave and MODIS satellite data products","volume":"191","author":"Zhu","year":"2017","journal-title":"Remote Sens. Environ."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"21480","DOI":"10.1073\/pnas.2001254117","article-title":"Decreasing snow cover alters functional composition and diversity of Arctic tundra","volume":"117","author":"Niittynen","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1242\/jeb.076331","article-title":"Real-time measurement of metabolic rate during freezing and thawing of the wood frog, Rana sylvatica: Implications for overwinter energy use","volume":"216","author":"Sinclair","year":"2013","journal-title":"J. Exp. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1038\/s41558-018-0311-x","article-title":"Snow cover is a neglected driver of Arctic biodiversity loss","volume":"8","author":"Niittynen","year":"2018","journal-title":"Nat. Clim. Chang."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7549","DOI":"10.1002\/ece3.5286","article-title":"Seasonality in spatial distribution: Climate and land use have contrasting effects on the species richness of breeding and wintering birds","volume":"9","author":"Kawamura","year":"2019","journal-title":"Ecol. Evol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3926","DOI":"10.1038\/s41467-018-06157-6","article-title":"Quantifying climate sensitivity and climate-driven change in North American amphibian communities","volume":"9","author":"Miller","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1038\/35002501","article-title":"Biodiversity hotspots for conservation priorities","volume":"403","author":"Myers","year":"2000","journal-title":"Nature"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"eabd0952","DOI":"10.1126\/sciadv.abd0952","article-title":"Spatial variation in biodiversity loss across China under multiple environmental stressors","volume":"6","author":"Lu","year":"2021","journal-title":"Sci. Adv."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"133","DOI":"10.5194\/essd-9-133-2017","article-title":"An extended global Earth system data record on daily landscape freeze\u2013thaw status determined from satellite passive microwave remote sensing","volume":"9","author":"Kim","year":"2017","journal-title":"Earth Syst. Sci. Data"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Riggs, G., and Hall, D. (2020). Continuity of MODIS and VIIRS Snow Cover Extent Data Products for Development of an Earth Science Data Record. Remote Sens., 12.","DOI":"10.3390\/rs12223781"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1007\/BF02837505","article-title":"Delineation of eco-geographic regional system of China","volume":"13","author":"Wu","year":"2003","journal-title":"J. Geogr. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/S0034-4257(02)00095-0","article-title":"MODIS snow-cover products","volume":"83","author":"Hall","year":"2002","journal-title":"Remote Sens. Environ."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"791","DOI":"10.5194\/essd-9-791-2017","article-title":"A global satellite environmental data record derived from AMSR-E and AMSR2 microwave Earth observations","volume":"9","author":"Du","year":"2017","journal-title":"Earth Syst. Sci. Data"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1016\/j.tree.2007.09.006","article-title":"The use of \u2018altitude\u2019 in ecological research","volume":"22","author":"Korner","year":"2007","journal-title":"Trends Ecol. Evol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1038\/nature25794","article-title":"Global elevational diversity and diversification of birds","volume":"555","author":"Quintero","year":"2018","journal-title":"Nature"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"9586","DOI":"10.1002\/ece3.5483","article-title":"Altitudinal biodiversity patterns of seed plants along Gongga Mountain in the southeastern Qinghai-Tibetan Plateau","volume":"9","author":"Zu","year":"2019","journal-title":"Ecol. Evol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"180040","DOI":"10.1038\/sdata.2018.40","article-title":"A suite of global, cross-scale topographic variables for environmental and biodiversity modeling","volume":"5","author":"Amatulli","year":"2018","journal-title":"Sci. Data"},{"key":"ref_49","unstructured":"Jiang, Z., Ma, Y., Wu, Y., Wang, Y., Zhou, K., Liu, S., and Feng, Z. (2015). China\u2019s Mammal Diversity and Geographic Distribution, Science Press."},{"key":"ref_50","unstructured":"China Wildlife Conservation Association (2005). Atlas of Mammalia of China, Henan Science and Technology Press."},{"key":"ref_51","unstructured":"Smith, A.T., and Xie, Y. (2009). A Guide to the Mammals of China, Hunan Education Press."},{"key":"ref_52","unstructured":"Zheng, G. (2018). A Checklist on the Classification and Distribution of the Birds of China, Science Press. [3rd ed.]."},{"key":"ref_53","unstructured":"Zhao, X. (2018). A Photographic Guide to the Birds of China, The Commercial Press."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"E2602","DOI":"10.1073\/pnas.1302251110","article-title":"Global patterns of terrestrial vertebrate diversity and conservation","volume":"110","author":"Jenkins","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1246752","DOI":"10.1126\/science.1246752","article-title":"The biodiversity of species and their rates of extinction, distribution, and protection","volume":"344","author":"Pimm","year":"2014","journal-title":"Science"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1657\/AAAR0016-009","article-title":"Climatology of the Timing and Duration of the Near-Surface Soil Freeze-Thaw Status Across China","volume":"48","author":"Wang","year":"2018","journal-title":"Arct. Antarct. Alp. Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"755","DOI":"10.5194\/hess-20-755-2016","article-title":"Variability in snow cover phenology in China from 1952 to 2010","volume":"20","author":"Ke","year":"2016","journal-title":"Hydrol. Earth Syst. Sci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1007\/s10584-016-1688-z","article-title":"Distribution, attribution, and radiative forcing of snow cover changes over China from 1982 to 2013","volume":"137","author":"Chen","year":"2016","journal-title":"Clim. Chang."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"2867","DOI":"10.1007\/s00382-020-05422-z","article-title":"Ground observed climatology and trend in snow cover phenology across China with consideration of snow-free breaks","volume":"55","author":"Ma","year":"2020","journal-title":"Clim. Dyn."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"084004","DOI":"10.1088\/1748-9326\/10\/8\/084004","article-title":"New satellite climate data records indicate strong coupling between recent frozen season changes and snow cover over high northern latitudes","volume":"10","author":"Kim","year":"2015","journal-title":"Environ. Res. Lett."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1111\/ecog.03531","article-title":"Where the wild birds go: Explaining the differences in migratory destinations across terrestrial bird species","volume":"42","author":"Somveille","year":"2018","journal-title":"Ecography"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1007\/s00442-019-04389-x","article-title":"Snow roosting reduces temperature-associated stress in a wintering bird","volume":"190","author":"Shipley","year":"2019","journal-title":"Oecologia"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1111\/j.1466-8238.2011.00737.x","article-title":"Broad-scale ecological implications of ectothermy and endothermy in changing environments","volume":"21","author":"Buckley","year":"2012","journal-title":"Glob. Ecol. Biogeogr."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1198","DOI":"10.1038\/s41467-021-21263-8","article-title":"The evolution of critical thermal limits of life on Earth","volume":"12","author":"Bennett","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1086\/345459","article-title":"The effect of energy and seasonality on avian species richness and community composition","volume":"161","author":"Hurlbert","year":"2003","journal-title":"Am. Nat."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1111\/geb.12298","article-title":"Why do birds migrate? A macroecological perspective","volume":"24","author":"Somveille","year":"2015","journal-title":"Glob. Ecol. Biogeogr."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"12897","DOI":"10.1073\/pnas.2000299117","article-title":"Migratory behavior and winter geography drive differential range shifts of eastern birds in response to recent climate change","volume":"117","author":"Rushing","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1111\/ddi.13036","article-title":"Differential winter and breeding range shifts: Implications for avian migration distances","volume":"26","author":"Curley","year":"2020","journal-title":"Divers. Distrib."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1111\/cobi.13091","article-title":"Conserving and managing the subnivium","volume":"32","author":"Zuckerberg","year":"2018","journal-title":"Conserv. Biol."}],"container-title":["Remote Sensing"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-4292\/14\/3\/794\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:16:19Z","timestamp":1760134579000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-4292\/14\/3\/794"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,8]]},"references-count":69,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2022,2]]}},"alternative-id":["rs14030794"],"URL":"https:\/\/doi.org\/10.3390\/rs14030794","relation":{},"ISSN":["2072-4292"],"issn-type":[{"value":"2072-4292","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,8]]}}}