{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,2]],"date-time":"2026-01-02T07:39:04Z","timestamp":1767339544615,"version":"build-2065373602"},"reference-count":56,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2022,8,11]],"date-time":"2022-08-11T00:00:00Z","timestamp":1660176000000},"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":["32060307","31872241"],"award-info":[{"award-number":["32060307","31872241"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"National Natural Science Foundation Surface Project of China","award":["32060307","31872241"],"award-info":[{"award-number":["32060307","31872241"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Remote Sensing"],"abstract":"<jats:p>Global warming is deeply influencing various ecological processes, especially regarding the phenological synchronization pattern between species, but more cases around the world are needed to reveal it. We report how the forest leaf phenology and ungulate molting respond differently to climate change, and investigate whether it will result in a potential phenology mismatch. Here, we explored how climate change might alter phenological synchronization between forest leaf phenology and Siberian roe deer (Capreolus pygargus) molting in northeast China based on a camera-trapping dataset of seven consecutive years, analyzing forest leaf phenology in combination with records of Siberian roe deer molting over the same period by means of wavelet analysis. We found that the start of the growing season of forest leaf phenology was advanced, while the end of the growing season was delayed, so that the length of the growing season was prolonged. Meanwhile, the start and the end of the molting of Siberian roe deer were both advanced in spring, but in autumn, the start of molting was delayed while the end of molting was advanced. The results of wavelet analysis also suggested the time lag of synchronization fluctuated slightly from year to year between forest leaf phenology and Siberian roe deer molting, with a potential phenology mismatch in spring, indicating the effect of global warming on SRD to forest leaf phenology. Overall, our study provides new insight into the synchronization between forest leaf phenology and ungulate molting, and demonstrates feasible approaches to data collection and analysis using camera-trapping data to explore global warming issues.<\/jats:p>","DOI":"10.3390\/rs14163901","type":"journal-article","created":{"date-parts":[[2022,8,11]],"date-time":"2022-08-11T21:15:05Z","timestamp":1660252505000},"page":"3901","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Wavelet Analysis Reveals Phenology Mismatch between Leaf Phenology of Temperate Forest Plants and the Siberian Roe Deer Molting under Global Warming"],"prefix":"10.3390","volume":"14","author":[{"given":"Heqin","family":"Cao","sequence":"first","affiliation":[{"name":"Forestry College, Guizhou University, Guiyang 550025, China"},{"name":"Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin 150040, China"},{"name":"Research Center for Bio-Diversity and Nature Conservation, Guizhou University, Guiyang 550025, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yan","family":"Hua","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou 510520, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xin","family":"Liang","sequence":"additional","affiliation":[{"name":"Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin 150040, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zexu","family":"Long","sequence":"additional","affiliation":[{"name":"Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin 150040, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jinzhe","family":"Qi","sequence":"additional","affiliation":[{"name":"Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin 150040, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dusu","family":"Wen","sequence":"additional","affiliation":[{"name":"Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin 150040, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8299-4499","authenticated-orcid":false,"given":"Nathan James","family":"Roberts","sequence":"additional","affiliation":[{"name":"Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin 150040, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2123-0660","authenticated-orcid":false,"given":"Haijun","family":"Su","sequence":"additional","affiliation":[{"name":"Forestry College, Guizhou University, Guiyang 550025, China"},{"name":"Research Center for Bio-Diversity and Nature Conservation, Guizhou University, Guiyang 550025, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guangshun","family":"Jiang","sequence":"additional","affiliation":[{"name":"Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin 150040, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1126\/science.1173004","article-title":"Phenology feedbacks on climate change","volume":"324","author":"Penuelas","year":"2009","journal-title":"Science"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.foreco.2012.09.006","article-title":"Mapping asynchrony between gypsy moth egg-hatch and forest leaf-out: Putting the phenological window hypothesis in a spatial context","volume":"287","author":"Foster","year":"2013","journal-title":"For. Ecol. Manag."},{"key":"ref_3","unstructured":"Lai, J.Y. (2020). Seasonal Hair Change of Siberian Roe Deer (Capreolus pygargus) Based on Automatic Camera Technology, Northeast Forestry University."},{"key":"ref_4","first-page":"110","article-title":"Seasonal variation of pelage characteristics in Siberian weasel (Mustela sibirica) of Xiaoxing\u2019 anling area, Heilongjiang, China","volume":"30","author":"Hua","year":"2010","journal-title":"Acta Theriol. Sin."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"20140029","DOI":"10.1098\/rspb.2014.0029","article-title":"Snowshoe hares display limited phenotypic plasticity to mismatch in seasonal camouflage","volume":"281","author":"Zimova","year":"2014","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"7360","DOI":"10.1073\/pnas.1222724110","article-title":"Camouflage mismatch in seasonal coat color due to decreased snow duration","volume":"110","author":"Mills","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1126\/science.aan8097","article-title":"Winter color polymorphisms identify global hot spots for evolutionary rescue from climate change","volume":"359","author":"Mills","year":"2018","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1146\/annurev.ecolsys.37.091305.110100","article-title":"Ecological and evolutionary responses to recent climate change","volume":"37","author":"Parmesan","year":"2006","journal-title":"Annu. Rev. Ecol. Evol. Syst."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.cois.2016.07.002","article-title":"Complex responses of insect phenology to climate change","volume":"17","author":"Forrest","year":"2016","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"800","DOI":"10.1126\/science.1157174","article-title":"Adaptive Phenotypic Plasticity in Response to Climate Change in a Wild Bird Population","volume":"320","author":"Charmantier","year":"2008","journal-title":"Science"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1038\/35019151","article-title":"Avian phenology: Climate change and constraints on breeding","volume":"406","author":"Stevenson","year":"2000","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"20180318","DOI":"10.1098\/rspb.2018.0318","article-title":"Convergence of biannual moulting strategies across birds and mammals","volume":"285","author":"Roxanne","year":"2018","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"S74","DOI":"10.1086\/687530","article-title":"Is There a Temperate Bias in Our Understanding of How Climate Change Will Alter Plant-Herbivore Interactions? A Meta-analysis of Experimental Studies","volume":"188","author":"Mundim","year":"2016","journal-title":"Am. Nat."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1038\/416389a","article-title":"Ecological responses to recent climate change","volume":"416","author":"Walther","year":"2002","journal-title":"Nature"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/s00442-006-0657-z","article-title":"Use of digital webcam images to track spring green-up in a deciduous broadleaf forest","volume":"152","author":"Richardson","year":"2007","journal-title":"Oecologia"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1071\/AM17016","article-title":"Identification of threatened rodent species using infrared and white-flash camera traps","volume":"40","author":"Burns","year":"2018","journal-title":"Aust. Mammal."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"13488","DOI":"10.1002\/ece3.6954","article-title":"Using community photography to investigate phenology: A case study of coat molt in the mountain goat (Oreamnos americanus) with missing data","volume":"10","author":"Nowak","year":"2020","journal-title":"Ecol. Evol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.agrformet.2016.01.006","article-title":"Phenopix: A R package for image-based vegetation phenology","volume":"220","author":"Filippa","year":"2016","journal-title":"Agricutural Meteorol."},{"key":"ref_19","first-page":"1","article-title":"Moult: An R package to analyses moult in birds","volume":"52","author":"Erni","year":"2012","journal-title":"J. Stat. Softw."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1111\/j.1474-919X.1988.tb08810.x","article-title":"A model for avian primary moult-data types based on migration strategies and an example using the Redshank Tringatotanus","volume":"130","author":"Underhill","year":"1990","journal-title":"IBIS"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1007\/s00484-013-0679-2","article-title":"The spatial pattern of leaf phenology and its response to climate change in China","volume":"58","author":"Dai","year":"2014","journal-title":"Int. J. Biometeorol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1007\/s00442-008-0993-2","article-title":"Wavelet analysis of ecological time series","volume":"156","author":"Cazelles","year":"2008","journal-title":"Oecologia"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"205","DOI":"10.2307\/2261007","article-title":"Characterizing canopy gap structure in forests using wavelet analysis","volume":"80","author":"Spies","year":"1992","journal-title":"J. Ecol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1038\/414716a","article-title":"Travelling waves and spatial hierarchies in measles epidemics","volume":"414","author":"Grenfell","year":"2001","journal-title":"Nature"},{"key":"ref_25","first-page":"1","article-title":"Wavelet methods reveal big cat activity patterns and synchrony of activity with prey","volume":"17","author":"Qi","year":"2021","journal-title":"Integr. Zool."},{"key":"ref_26","unstructured":"Roschand, A., and Schmidbauer, H. (2020, May 09). WaveletComp: A Guide Tour through the R-Package. Online Version Paper, 2014. Available online: https:\/\/cran.r-project.org\/package=WaveletComp."},{"key":"ref_27","unstructured":"Li, M. (2011). The Responses of Forest Phenology on Climate Change in Changbai Mountains. [Ph.D. Thesis, Northeast Normal University]."},{"key":"ref_28","first-page":"23","article-title":"Comparative study of vegetation phenology extraction methods based on digital images","volume":"37","author":"Zhou","year":"2018","journal-title":"Prog. Geogr."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Bothmann, L., Menzel, A., Menze, B.H., Schunk, C., and Kauermann, G. (2017). Automated processing of webcam images for phenological classification. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0171918"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e02826","DOI":"10.1002\/ecy.2826","article-title":"Shifts in phenological mean and synchrony interact to shape competitive outcomes","volume":"100","author":"Carter","year":"2019","journal-title":"Ecology"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"De Sassi, C., and Tylianakis, J.M. (2012). Climate change disproportionately increases herbivore over plant or parasitoid biomass. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0040557"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1017\/S0007485317000062","article-title":"Robustness of plant-insect herbivore interaction networks to climate change in a fragmented temperate forest landscape","volume":"107","author":"Bahner","year":"2017","journal-title":"Bull. Entomol. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1874","DOI":"10.1111\/2041-210X.13024","article-title":"Using archived television video footage to quantify phenology responses to climate change","volume":"9","author":"Bertrand","year":"2018","journal-title":"Methods Ecol. Evol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1927","DOI":"10.1007\/s00484-015-0999-5","article-title":"Five years of phenological monitoring in a mountain grassland: Inter-annual patterns and evaluation of the sampling protocol","volume":"59","author":"Filippa","year":"2015","journal-title":"Int. J. Biometeorol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1111\/gcb.12023","article-title":"A plant\u2019s perspective of extremes: Terrestrial plant responses to changing climatic variability","volume":"19","author":"Reyer","year":"2012","journal-title":"Glob. Chang. Biol."},{"key":"ref_36","first-page":"5280","article-title":"Relationships between Leymus chinensis phenology and meteorological factors in Inner Mongolia grasslands","volume":"29","author":"Chen","year":"2009","journal-title":"Acta Ecol. Sin."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Deng, L.J. (2017). Response of Plant Phenology to Climate Change in North China and Surveillance Camera-Based Monitoring of Plant Flowering Phenology. [Master\u2019s Thesis, China University of Geosciences].","DOI":"10.1007\/978-981-10-3966-9_31"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1007\/s00376-010-9219-8","article-title":"The response of first flowering dates to abrupt climate change in Beijing","volume":"28","author":"Bai","year":"2011","journal-title":"Adv. Atmos. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1038\/nature15402","article-title":"Declining global warming effects on the phenology of spring leaf unfolding","volume":"526","author":"Fu","year":"2015","journal-title":"Nature"},{"key":"ref_40","first-page":"258","article-title":"Study on the molt sequence of captive sable in spring in Dalian China","volume":"37","author":"Gu","year":"2016","journal-title":"Chin. J. Wildl."},{"key":"ref_41","first-page":"6","article-title":"The regularity of seasonal molting of Mustelasibirica","volume":"2","author":"Yang","year":"1980","journal-title":"J. Econ. Anim."},{"key":"ref_42","first-page":"101","article-title":"Coat changes and hair morphology of musk deer (Moschus berezovskii) fawn","volume":"26","author":"Xu","year":"2006","journal-title":"Acta Theriol. Sin."},{"key":"ref_43","first-page":"840","article-title":"Measurement method of molt sequence of Siberian roe deer (Capreolus Pygargus) in northeast China based on camera-trapping","volume":"40","author":"Hua","year":"2019","journal-title":"Chin. J. Wildl."},{"key":"ref_44","unstructured":"Zhang, D. (2020). Study on the Environmental Factors Driving the Seasonal Molting Characteristics of Siberian Roe Deer (Capreolus Pygargus). [Master\u2019s Thesis, Northeast Forestry University]."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1139\/as-2016-0023","article-title":"Effects of changing permafrost and snow conditions on tundra wildlife: Critical places and times","volume":"3","author":"Berteaux","year":"2016","journal-title":"Arct. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/0016-6480(71)90034-7","article-title":"Seasonal changes of pelage in the vole (Microtus agrestis): The effect of daylength","volume":"16","author":"Johnson","year":"1971","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1126\/science.89.2314.418","article-title":"Shortening daylight periods between May 15 and September 12 and the pelt cycle of the mink","volume":"89","author":"Bissonnette","year":"1939","journal-title":"Science"},{"key":"ref_48","first-page":"27","article-title":"Effects of light on reproduction and molting of Matres zibellina","volume":"6","author":"Song","year":"1988","journal-title":"Chin. J. Ecol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1959","DOI":"10.1139\/z83-257","article-title":"Regulation in pregnant mink (Mustela vison) of plasma progesterone and prolactin and regulation of the onset of the spring moult by daylight ratio and melatonin injections","volume":"61","author":"Martinet","year":"1983","journal-title":"Can. J. Zool."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/j.ecolmodel.2012.11.022","article-title":"Host plant-mediated effects of climate change on the occurrence of the Alcon blue butterfly (Phengaris alcon)","volume":"250","author":"Cormont","year":"2013","journal-title":"Ecol. Model."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1596","DOI":"10.1111\/j.1365-2486.2007.01400.x","article-title":"Predicting adaptation of phenology in response to climate change, an insect herbivore example","volume":"13","author":"Holleman","year":"2007","journal-title":"Glob. Chang. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"3843","DOI":"10.1098\/rspb.2012.1051","article-title":"Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change","volume":"279","author":"Anderson","year":"2012","journal-title":"Proc. R. Soc. B-Biol. Sci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1530\/jrf.0.0730241","article-title":"Effect of constant-release implants of melatonin on seasonal cycles in reproduction, prolactin secretion and molting in rams","volume":"73","author":"Lincoln","year":"1985","journal-title":"J. Reprod. Fertil."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1111\/j.1748-7692.2000.tb00952.x","article-title":"Do photoperiod and temperature influence the molt cycle of Phoca vitulina","volume":"16","author":"Mo","year":"2006","journal-title":"Mar. Mammal Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1017\/S0021859600048863","article-title":"A field study of coat shedding in cattle under conditions of equal day-length but different temperatures","volume":"65","author":"Murray","year":"1965","journal-title":"J. Agric. Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1478","DOI":"10.1111\/brv.12405","article-title":"Function and underlying mechanisms of seasonal colourmolting in mammals and birds: What keeps them changing in a warming world?","volume":"93","author":"Zimova","year":"2018","journal-title":"Biol. Rev."}],"container-title":["Remote Sensing"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-4292\/14\/16\/3901\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:07:25Z","timestamp":1760141245000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-4292\/14\/16\/3901"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,11]]},"references-count":56,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["rs14163901"],"URL":"https:\/\/doi.org\/10.3390\/rs14163901","relation":{},"ISSN":["2072-4292"],"issn-type":[{"type":"electronic","value":"2072-4292"}],"subject":[],"published":{"date-parts":[[2022,8,11]]}}}