成果展示材料

成果展示材料项目名称：迁地保护生境中鸟类功能特征对濒危植物更新的影响申请人：金柏慧吕婷婷刘好好蒋佩月王业迪指导老师：王征鲁长虎项目周期：2018.7-2020.5录用通知吕婷婷同志：您好！你的文章《三种食果鸟类对植物果实的取食和肠道消化时间研究》已通过审核，拟定于2020年7月刊登。请勿一稿多投,谢谢配合。国内统一出版物号：CN：50-1186/S国际标准连续出版物号：ISSN：1673-890X2020月三种食果鸟类对植物果实的取食和肠道消化时间研究吕婷婷 王业迪 蒋佩月 金柏慧 刘好好王征1南京林业大学南方现代林业协同创新中心，生物与环境学院 南京 210037摘要（对种子的有效传播距离。于2018年7-8月，以白头鹎（Pycnonotussinensis）、红耳鹎（Pycnonotusjocosus）和灰树鹊（Dendrocittaformosae）为对象，研究三种鸟类对八角枫（Alangiumchinense）（Cayratiajaponica）（Sambucuswilliamsii）果实（关键词：食果鸟类、植物果实、取食、肠道消化时间（Seeddispersal）[1]。在热带和亚热带原始森林中，70%–95%的植物依靠鸟类传播种子，它们能为种子提供较远的传[2][3]20187-8（PcnonousnensPycnnotusjoosu（endctafo（Alagimchinns、（Cayratiajaponica）（Sambucuswilliamsii）1基金项目江苏省高等学校大学生创新创业训练计划项目“迁地保护生境中鸟类功能特征对濒危植物更新的影响”（201810298044Z）通讯作者：王征；Email:zhengw1028@163.com第一作者介绍：吕婷婷（1999-），女，本科生；研究方向：动植物关系；Email:1659756718@材料与方法Passeriformes、鹎科Regulidae20Corvidae38cm[8]7-1117-102-47-92-355240×30×40长×宽×高2-320180.1mm0.0001g。实验前1天将鸟类禁食，仍供以足够的水。每天固定时间（上午8:00-11:00，下午SPSSStatistics20.0Excel2007ologoroirnov（A、LSD0.05。结果与分析450540775颗。单因素方差分析显示，三种植物果实的长径（F2,1762=3212.1,P<0.001）（F2,1762=3459.2,>>F1,95=17.,<0001表1。果实类型数量（颗）八角枫450乌蔹莓540接骨木775表1果实类型数量（颗）八角枫450乌蔹莓540接骨木775长径（mm）短径（mm）重量/颗（g）8.84±0.057.56±0.050.300±0.01(6.310.9)(5.19.8)(0.1340.520)9.39±0.048.24±0.040.488±0.01(6.212.8)(5.410.8)(0.2500.860)注：表中数据用平均值±标准误表示。

6.09±0.01(5.07.1)

0.122±0.01—(0.0900.160)352头鹎最大、灰树鹊其次、红耳鹎最小。表2三种食果鸟类对植物果实的取食果实类型

白头鹎投喂/次

白头鹎

红耳鹎投喂/次

红耳鹎

灰树鹊投喂/次

灰树鹊取食率（%）接骨木98.75 98.6780 75 — —（395/400接骨木98.75 98.6780 75 — —（395/400） （370/375）八角枫90.67 77.3375 75 — —（204/225） （174/225）乌蔹莓90.22 75.56 81.1175 75 30

（170/225）

（73/90）3-5（F2,221=0.80P=0.451）（F2,193=0.88,P=0.415）F2,4476571,<0001，即灰树鹊显著大于另两种，但两种鹎类无差异。表3三种食果鸟类取食果实后的肠道消化时间果实类型/消化时间（m）

白头鹎 红耳鹎 灰树鹊接骨木 19.0±0.89八角枫 20.2±0.83乌蔹莓 19.0±0.60

20.9±0.66(12.538.3)20.4±0.95(9.546.0)19.3±0.59(13.029.0)

——74.6±3.42(46.5134.0)结论与讨论[7][9]（20c（38c[10,11]。]。本文研究结果为了解食果鸟类对植参考文献HoweSmallwoodJ.1982.Ecologyofseeddispersal[J].AnnualReviewofEcology,EvolutionandSystematics,13:201-228.McConkeyKR,PrasadS,Corlettetal.2011.Seeddispersalinchanginglandscapes[J].BiologicalConservation,146:1-13.GarcíaC,KleinE,Jordano2017.Dispersalprocessesdrivingplantmovement:challengesforunderstandingandpredictingrangeshiftsinachangingworld[J].JournalofEcology,105:1-5.段琼,权锐昌.2012.西双版纳食果鸟对植物果实颜色的取食选择[J].动物学研究,33(5427-432.李新华,尹晓明,贺善安.2001.南京中山植物园秋冬季鸟类对植物种子的传播作用,9(1):68-72.BrochetAL,MatthieuMichelGC,etal.2010.EndozoochoryofMediterraneanaquaticplantseedsbytealafteraperiodofdesiccation:Determinantsofseedsurvivalandinfluenceofretentiontimeongerminabilityandviability[J].AquaticBotany,93:99-106.鲁为华,万娟娟,杨洁晶.2013.草食动物对植物种子的消化道传播研究进展[J].草业学报,22(3):306-313.约翰.马敬能,卡伦.菲利普斯,何芬奇.中国鸟类野外手册:中文版[M].湖南教育出版社,2000.彭红元,文清华,黄捷,等.2008.3种鹎科鸟类春季食性的分析和比较[J].四川动物,27(1):99-101.LordJM.2010.Frugivoregapesizeandtheevolutionoffruitsizeandshapeinsouthernhemispherefloras[J].AustralEcology,29(4):430-436.SimmonsBI,SutherlandWJ,Dicksetal.2018.Movingfromfrugivorytoseeddispersal:incorporatingthefunctionaloutcomesofinteractionsinplant-frugivorenetworks[J].JournalofAnimalEcology,87(4):995-1007.[12],2000.[J].,42(10):1096-1100.四川动物0年第9卷第2期 nlfyl．9o．20江苏省无锡发现赤红山椒鸟9年2月1日4∶5在江苏省无锡市梅园(0°2'.6″E1°4'.3″N海拔6m)进行鸟类观测时发现2只体Campephagidae雌鸟在树林间活动并拍摄到其中1只的清晰照片(1)。该雌鸟背部多灰色胸腹部、腰尾羽羽缘及翼上的2道斑纹为黄色且黄色延至喉颏耳羽及额头。中国鸟类野外手册(约翰·马敬能等，2000Pericrocotusflammeus雌性成鸟。赤红山椒鸟隶属雀形目s山椒鸟科(郑光美7)是一种体型略大(9m)且色彩浓艳的鸟类主要分布于印度东南亚菲律宾及中国南方等(约翰·马敬能等0)。全世界赤红山椒鸟共有9个亚种(r0)中国有3个亚种:..s分布于西藏东部和云南..s分布于海南..s分布于贵州湖南南部江西浙江福建中部和北部广东北部香港澳门和广西(郑光美7)。因此判断此次发现的雌性成鸟为..s。本次发现地梅园是当地著名的观鸟点之一拍摄到的雌性赤红山椒鸟正停歇在树枝上。在观察和拍摄的过程中2只雌鸟身体状况良好活动灵敏且具有较高警惕性应不是逃逸个体。继本次记录之后0年1月7日上午苏州鸟类调查员在同里国家湿地公园的生态保育区内观测到1群山椒鸟其中亦发现1只雌性赤红山椒鸟并拍摄到照片次日姑苏晚报(http//.0.m/c/0/1/8/.l)。经与历史分布记录和中国观鸟记录相比对赤红山椒鸟为江苏省鸟类分布新记录本次发现为了解该物种的分布现状提供了基础资料。图1江苏无锡发现赤红山椒鸟Pericrocotusflammeus(任旭清摄)金柏慧1，任旭清2，刘好好1，王征1*，鲁长虎11.南京林业大学南方现代林业协同创新中心生物与环境学院210037;2.江苏省苏南猛禽调查组214000)基金项目:江苏省高等学校大学生创新创业训练计划项目“迁地保护生境中鸟类功能特征对濒危植物更新的影响”(201810298044Z);江苏省高校优势学科建设工程项目(PAPD)作者简介:金柏慧女本科生研究方向:鸟类生态学El:4@.m*通信作者El:8@.m196南京中ft植物园食果鸟类对宜昌润楠果实的取食和传播金柏慧，刘好好，吕婷婷，王业迪，蒋佩月，王征1，*南京林业大学南方现代林业协同创新中心，生物与环境学院，南京210037摘要（Machilusichangensis）（Lauraceae）20196-8ft14mandarinus）erythrorhyncha）43.83%17.90%；总取食量较高的鸟类依次有乌鸫、红嘴蓝鹊、黑脸噪鹛（xperpiilaus、灰树鹊（ndctafoeCanopiacau5（F4,24=1.08,<0.01（6.1±3颗F7,29=3.81,P.0054.63%关键词食果鸟类；取食行为；种子传播；宜昌润楠FruitsforaginganddispersalofMachilusichangensisbyfrugivorousbirdsinNanjingBotanicalGardenMem.SunYat-SenJINBai-hui,LIUHaohao,LVTingting,WANGYedi,JIANGPeiyue,WANGZheng*（Co-InnovationCenterforSustainableForestryinSouthernChina,CollegeofBiologyandtheEnvironment,NanjingForestryUniversity,Nanjing210037,China）AbstractsFrugivorousbirdsareimportantdispersalmediaofplantseeds,andtheirmorphologicalandbehaviouraltraitsarethemainfactorsaffectingseeddispersal.Machilusichangensisisanevergreenbroad-leavedtreespeciesbelongedtoLauraceae,whichdependsonbirdstoforageand1基金项目的影响”（201810298044Z（P）作者简介：金柏慧(1999—)，女，浙江温州人，本科生，研究方向为野生动植物保护，Email:297136954@通讯作者：王征，女，博士，副教授，主要从事野生动物生态学研究，E-mail:zhengw1028@163.comdisperseseeds.Inthesummerof2019,fruitsforaginganddispersingofM.ichangensisbyfrugivorousbirdshavebeenresearchedinNanjingBotanicalGardenMem.SunTheresultsshowedthatM.ichangensisattracted14speciesoffrugivorousbirdstofeedonfruits.ChineseBlackbirdmandarinus)andRed-billedBlueMagpie(Urocissaerythrorhyncha)withthemostforagingfrequencyandforagingamountoffruitswereconsideredtheprimaryseeddispersersofM.ichangensis,accountingfor43.83%and17.90%ofthetotalforagingfrequencyrespectively.ChineseBlackbird,Red-billedBlueMagpie,MaskedLaughingthrush(Garrulaxperspicillatus),GreyTreepie(Dendrocittaformosae)andAzure-wingedMagpie(Cyanopicacyanus)werethefivebirdspecieswithhightotalforagingamountoffruits.Thereweresignificantdifferencesinforagingamountamongthefivebirdspecies(F4,247=11.08,P<0.001),andtheforagingamountofChineseBlackbird(6.1±0.3)wassignificantlyhigherthantheotherbirds.Thereweresignificantdifferencesinthedispersaldistanceamongtheeightbirdspecieswithmoreforagingfrequency(F7,294=3.881,P<0.001),andbirdspecieswithlargerbodysizefromCorvidaeandTurdidaehadrelativelylongerdispersaldistance.Themainhabitattypesofbirdsafterforagingwerearborforest,shrubandgrassland,andarborforestwasthemainpreferredrestinghabitatoffrugivorousbirds.Therewerethelargestnumberofrestingbirdspeciesinarborforest,andtherestingfrequencyofbirdsinarborforestaccountingfor54.63%ofthetotalrestingThestudyshowedthatfrugivorousbirdsmightplayanimportantroleinseeddispersalofM.ichangensis,andalsoprovidedsomeimportantsuggestionsfortheprotectionofthisspecies.Keywordsfrugivorousbirds;foragingbehavior;seeddispersal;Machilusichangensis前言[1]。在热带和亚70-95%[2-3]（）（）[6-7]。其[5,8][9]；体型大小亦与取食方式[12]。（Machilusichangensis）（Lauraceae）[13]ft材料与方法研究地概况ftftft186hm2，1000.4ft8000（）1970[14]。6hm2300兼有草地、灌木及水域等；周边主要树种有香樟（Cinnmcora、冬青（IexpurpuPotniaerulaf（Elaearpusyves7151cm0.4-0.6g68鸟类调查于2019年6-8月间，采用样线法[15]调查鸟类群落多样性以确定环境中鸟类分布和宜昌润2122km，生06:00-10:00（10×4230m9鸟类取食观测20196-8806:30-18:00（10×42倍（、（（数据分析（[17]1%-10%1%Shannon-WienerPielouSimpsonSPSS20.0Kolmogorov-Smirnov标准误表示，显著性水平设置在0.05。结果鸟类物种组成428192661.90%2969.05%13种，30.95%2（Accipiter（Falcotnnuncuuniner3.6Pilou082，pson优势度指数为0.07。172161卷尾（uslcopaus、八哥（Acrdothesatlus）和小灰ft椒鸟（Percocous14172（uusarnuxperpiilau（oceryhohyncha、灰喜鹊（Cynopiacanus）等10种；偶见种有灰ft椒鸟（Perccousdiarcaualusglandaiu等5种87.90（表1（Dendrocittaformosae）5F4,24=.0,P0.01（61±0.）颗/只次，显著大于其他鸟类，另4种鸟类取食量无显著差异。（Streptopelia（PicapiaffAegihalosglanogulai、大ftParuscnereuCopsyhusa表1食果鸟类对宜昌润楠果实的取食Table1ForagingonthefruitsofMachilusichangensisbyfrugivorousbirds体型 取食

平均取食

平均停留时 取食鸟种 大

频次 （颗次

间（秒次） 方式（cm）乌鸫Turdusmandarinus291426.1±0.3179.8±7.7整吞红嘴蓝鹊Urocissaerythrorhyncha68583.2±0.2142.8±11.7整吞黑脸噪鹛Garrulaxperspicillatus30203.2±0.3129.0±17.6整吞银喉长尾ft雀16182.3±0.1140.0±13.7啄食Aegithalosglancogularis红头长尾ft雀10171.6±0.2127.1±4.8啄食Aegithalosconcinnus灰树鹊Dendrocittaformosae38163.8±0.9180.0±35.1整吞灰喜鹊Cyanopicacyanus35163.5±0.4161.3±14.2整吞大ft雀Paruscinereus14151.8±0.3200.03±25.3啄食鹊鸲Copsychussaularis2071.6±0.3145.7±17.8整吞/啄食白头鹎Pycnonotussinensis1954.0±0.6132.0±29.4整吞喜鹊Picapica4543.0±0.4135.0±15.0整吞灰ft椒鸟Pericrocotusdivaricatus2041.5±0.3120.0±34.6整吞ft斑鸠Streptopeliaorientalis3214300.0整吞松鸦Garrulusglandarius3514120.0整吞注：表中数据用平均值±标准误表示(DataareexpressedasmeanSE)图1食果鸟类与宜昌润楠果实间的的取食关系Figure1AforagingnetworkbetweenfrugivorousbirdsandthefruitsofMachilusichangensis14（表210次的8F7,294=3.81,P<.00，平（13.4±2.2）ftft（5.5±1.1）mft雀（3.7±0.2）mftft表2（14种最多，（9种（6种31.79%（Sloananens（Sabinachnens表2食果鸟类取食后的飞行距离和停歇地类型2 Thedispersaldistanceandhabitattypeoffrugivorousbirdsafterforaging取食后飞行距离 取食后停歇地类型<10m10-30m<10m10-30m>30m乔木灌丛草地乌鸫64744561472红嘴蓝鹊25249231421黑脸噪鹛6131128–银喉长尾ft雀18––18––红头长尾ft雀152–17––灰树鹊115–1114灰喜鹊511–1222大ft雀96–141–鹊鸲34–412白头鹎13141–喜鹊31–2–2灰ft椒鸟22–22–ft斑鸠1––1––松鸦––11––总计1631451617744103讨论宜昌润楠分布区及周围的鸟类多样性决定了植物的潜在访问和传播鸟类，其中取食鸟类对于植物的种子传播和更新至关重要。一般认为，传播种子的鸟类种类越多，则鸟类与植物之间的种子传播关系越趋于稳定，故拥有较多的传播鸟类多样性对植物种群的更新更为有利[18]。在鸟类和植物形成的种子传播系统中，一种植物和一种食果鸟类之间的互利关系很少见，）[20-22][23]（27种[24]（18（14种42-3月，ftftft[9,25][10]。鸟类的取食行为特征是影响种子传播的重要因素[5]。鸟类的取食频次与取食量影响了种[12]ftftft6，ft[14,26][24][27][28]。鸟类取食后的行为特征，如传播距离、种子排放地等，决定了有多少种子能够到达适宜生境并萌发和更新[11]。不同鸟类取食宜昌润楠果实后的传播距离差异显著，体型较大、活动范围较广的鸦科、鸫科鸟类具有相对较大的飞行距离，故能为种子提供较大的传播距离，以促进植物占据新的生境。鸟类取食后的停歇地选择具有一定的偏好，导致潜在的种子排放和萌发地生境不同[12]。研究结果显示，阔叶乔木林是鸟类取食宜昌润楠后选择的主要停歇地，其总利用频次高于灌木和草地，这可能与乔木林具有更高的隐蔽性和安全性有关。取食后偏好利用乔木林生境这一行为特征在鸟类对其他植物的种子传播中亦常见[23,27]。植物园内阔叶林和宜昌润楠母树周围可见许多幼苗，显示迁地保护生境中该树种可以自然更新。本研究表明食果鸟类对宜昌润楠种子具有潜在传播作用，尤以乌鸫和红嘴蓝鹊为主要的取食传播者，研究结果为阐明其种子传播机制提供了基础数据，亦为该物种的保护提供参考建议。参考文献HOWEHJ.Ecologyofseeddispersal[J].AnnualReviewofEvolutionandSystematics,1982,13:201-228.JORDANOFORGETPM,JE,etal.Frugivoresandseeddispersal:mechanismsandconsequencesforbiodiversityofakeyecologicalinteraction[J].BiologyLetters,2011,7(3):321-323.CORLETTRFrugivoryandseeddispersalbyvertebratesintropicalandsubtropicalAsia:anupdate[J].GlobalEcologyandConservation,2017,11(1):1-22.王静,闫巧玲.干扰对动物传播森林植物种子有效性影响的研究进展[J].应用生态学报,2017,28(51716-1726.LiN,Z,ZhANGS,etal.Importanceofbirdtraitsforseeddispersalpatternsofco-fruitingtreesinapatchyforest.IntegrativeZoology,2019,14(5):470-478.BURNSKC,B.Fruit–frugivoreinteractionsintwosouthernhemisphereforests:phylogenyandbodysize[J].Oikos,2009,118(12):1901-1907.李宁,钟明,,等.[J].,2015,34(7):2041-2047.MUÑOZMC,SCHAEFERHM,BÖHNING-GAESEK,etal.Importanceofanimalandplanttraitsforfruitremovalandseedlingrecruitmentinatropicalforest[J].Oikos,2017,126(6):823-832.DONOSOI,SCHLEUNINGM,GARCÍAD,etal.Defaunationeffectsonplantrecruitmentdependonsizematchingandsizetrade-offsinseeddispersalnetworks[J].ProceedingsoftheRoyalSocietyB:BiologicalSciences,2017,284(1855):20162664.MOHAMMEDM,LANDIMINOARIVELOHO,etal.Frugivoryandseeddispersal:Extendedbi-stablepersistenceandreducedclusteringofplants[J].Ecologicalmodelling,2018,380:31-39.SCHLEUNINGM,FRÜNDJ,GARCÍAD.Predictingecosystemfunctionsfrombiodiversityandmutualisticnetworks:anextensionoftrait-basedconceptstoplant–animalinteractions[J].2015,38(4):380-392.SCHUPPEJORDANOGÓMEZJM.Seeddispersaleffectivenessrevisited:aconceptualreview[J].NewPhytologist,2010,188(2):333-353..[M].北京:,2004.李新华,尹晓明.南京中ft植物园春夏季节鸟类对植物种子的传播作用[J].生态学报,2004,24(7):1452-1458.BIBBYCJ,BURGESSND,HILLDA,etal.Birdcensustechniques[M].SanDiego:AcademicPress,2000.(M].北京:,2017约翰·马敬能,卡伦·菲利普斯,何芬奇.中国鸟类野外手册[M].长沙:湖南教育出版社,2000N,BÖHNING-GAESEK,BLEHERB.EnhancedseeddispersalofPrunusafricanainfragmentedanddisturbedforests?[J].Oecologia,2006,147(2):238-252.HERRERACM.Plant-vertebrateseeddispersalsystemsintheMediterranean:ecological,evolutionaryandhistoricaldeterminants[J].AnnualReviewofEcology＆Systematics,1995,26(1):705-727.FRANCISCOMR,LUNARDIVO,GALETTIM.Birdattributes,plantcharacteristicsandseeddispersalofPeraglabrata(Schott,1858),(Euphorbiaceae)inadisturbedcerradoarea[J].BrazilianJournalof2007,67(4):627-634.DUSNQ,GOODALEE,QUANRC.TheeffectofcoloronfruitselectioninsixtropicalAsianbirds[J].TheCondor,2013,115(3):623-629.TIRIBELLIAMICOGC,SASALetal.Theeffectofspatialcontextandplantcharacteristicsonfruitremoval[J].ActaOecologica,2017,82:69-74.,.ft（的取食[J].,2019,54(6):784-792.潘扬,徐丹,鲁长虎,等.食果鸟类对红楠种子的传播作用[J].生态科学,2017,36(2):63-67.GONZÁLEZ-CASTROA,M,NOGALESM.Comparingseeddispersaleffectivenessbyfrugivoresatthecommunitylevel[J].Ecology,2015,96(3):808-818.[26]ARUNAR,BALASUBRAMANIANP,RADHAKRISHNANP.Roleoffrugivorousbirdsinseeddispersalinthemixeddrydeciduousforestsofattappadyandanaikatty,WesternGhats[J].TheIndianForester,2009,135(10):1308-1316.,,,等.[J].28(1):32–37.,.[J].,1998,17(1):61-64.Responseofwinteringwaterbirddiversitytoreclamationhistoryandpost-reclamationhabitatalongYellowseacoastZhengWang1,Bai-huiJin1,ShuaiGao1,NingLi2,,Shu-QingAn3Co-InnovationCenterforSustainableForestryinSouthernChina,CollegeofBiologyandtheEnvironment,NanjingForestryUniversity,Nanjing,Jiangsu,ChinaInstituteofAppliedEcology,CollegeofFoodScience,NanjingXiaozhuangUniversity,Nanjing,Jiangsu,ChinaSchoolofLifeScienceandInstituteofWetlandEcology,NanjingUniversity,Nanjing,Jiangsu,ChinaNingLi(Correspondingauthor)E-mail:lining196@126.com;Tel:+86-25-86178307;Fax:+86-25-86178307Abstracts:Waterbirddiversityisoneofmostimportantindicatorformonitoringwetlandquality.However,theincreasingintensityofreclamationactivitiesinrecentdecadescausedthechangeofhabitatlandscapealongcoasts,whichcouldaffectthediversityofwinteringwaterbirds.Ourstudytriedtoinvestigatehowreclamationhistoryandpost-reclamationhabitatsinfluencethespeciesrichness,speciesabundance,andShannon-WienerdiversityofwinteringwaterbirdsalongYanchengcoastalwetlands.Atotalof68waterbirdspecieswererecordedandtheabundancepatternofwinteringbirdschangedfrom2009to2013.Speciesrichnessandabundanceofwinteringwaterbirdsvariedinthedifferentreclamationhistories.Mostimportantly,theGenerallinermixedmodelhighlightedtheimportanceofreclamationhistory,post-reclamationhabitattypeandtheirinteractionsforshapingbothspeciesabundanceandShannon-Wienerdiversityofwinteringwaterbirds,butthesevariablesdidnotaffectthespeciesrichnessofwaterbirds.Furthermore,therandomforestresultsalsoshowedapositiveassociationbetweenreclamationhistorywithspeciesrichness,speciesabundanceandShannon-Wienerdiversityofwinteringwaterbirds.Moreover,threepost-reclamationhabitattype,Suaedaglauca,Bareflatandfishpondplayedimportantrolesforwinteringbirds.Ourresultshighlightedreclamationhistory,post-reclamationhabitatsandtheirinteractionsdeterminedwaterbirddiveristy.Giventhegrowingthreatstowetlandecosystemsfromreclamationactivities,furtherresearchshouldfindabalancebetweencoastalreclamationandwaterbirdbiodiversityconservation.Keywords:Reclamationhistory;Post-reclamationhabitat;Winteringwaterbirds;YanchengwetlandsIntroductionRecently,coastalwetlandshavebeenfacingthreatsresultingfromthelandreclamation,whichisperformedtoalleviatelandpressureandgenerateaseriesofeconomicbenefitsunderthebackgroundofincreasinghumanspeciesabundanceandrapidurbanization(Mengetal.2017).Asaresult,coastalwetlandsareundergoingdevastatingexploitationonaglobalscale,withcoastalreclamationbeingmostprevalentinEuropeandAsia(Halpernetal.2008).Form1949,China’scoastalregionshaveexperiencedfourwavesforreclamation:seasaltproduction,agriculturalfarming,theconstructionofindustrialdevelopmentzones,andthedevelopmentoftouristandotherlargeinfrastructures(Mengetal.2017).Lossofnaturalwetlandscausechangesintheirecologicalprocessesandpatterns,whichhaveexertedasignificantinfluenceonthehydrology,waterquality,andbiodiversityofcoastalwetlands(Liuetal.2006;Mooresetal.2016;Chenetal.2017).Duetothesensitivitytoenvironmentalchange,waterbirddiversitywereoftenusedasindicatorspeciesforestimatingtheecologicalhealthyofcoastalwetlands(Reisetal.2012;Maetal.2014).Mostconservationbiologistshaveconsideredstudiesonwaterbirdpopulationecologytobeessentialformeasuringeffectiveconservation.Thesestudiesshouldincludeanalysisofhowwaterbirdsrespondtoreclamationintermsofhabitatutilizationandspeciesabundance(Owenetal.2017).Regardinghabitatutilization,reclamationcausedsomewaterbirdstouseconstructedwetlandsassupplementaryhabitats(Louise&Susan1996).OntheeasterntidalflatsofChongmingIsland,forexample,reclamationhasenabledtheinvasionofSpartinaalterniflora,whichinturnledtoadecreaseinsuitablewaterbirdhabitatssuchasbreedingpondsandScirpusmariquetermarshes.Asaresult,waterbirdhabitatshavegraduallyshiftedfromnaturaltoconstructedwetlands(Fanetal.2010).Reclamationalsoleadstothedestructionofenvironments,resultinginthesmotheringofmostbenthicorganismsandreducingtheirsurvivalratebymorethan50%(Nase2011).Studieshaveshownthatthenumberoffamiliesandabundanceofbenthicfaunaaresignificantlyreducedinthevicinityofreclaimedareas,butthattheysignificantlyincreasewithdistancefromtheseareas(Luetal.2002);thisisalsoakeyexplanationtowhywaterbirdstendtochooseunreclaimedareasashabitats(Evansetal.1979).However,lessattentionhasbeenpaidtotheeffectsofreclamationhistoryandpost-reclamationhabitats.Astheecologicalconsequenceofreclamation,thequalityofpost-reclamationhabitatsandreclamationhistorycouldaffecthabitatutilizationofwaterbirds,buttherelativestudieswerelacked.TheYanchengNatureReservedistributedintheyellowseacoasts.ItwasdesignatedasaUNESCOBiosphereReservein1993andaWetlandofInternationalImportanceundertheRamsarConventionin2002.So,itisimportanttoexplorehowreclamationhistoryandpost-reclamationhabitatsaffectswinteringwaterbirds.Inthisstudy,wecombinedfielddataofwinteringwaterbirds(2009-2013)relatedtoreclamationhistoryandpost-reclamationhabitatstoelucidatetheinfluenceoflong-termcoastalreclamationontheconservationandmanagementofwinteringwaterbirds.Wehypothesizedthatcoastalreclamationhistoryandpost-reclamationhabitatscouldaffectspeciesrichnessandspeciesabundanceofwaterbirdsinthecoastlineYellowSea,thusaffectingtheShannon-Wienerdiversityofwaterbirds.MethodsStudyareaandhabitatvariablesThestudysite,locatedat32°35′–34°28′N,119°37′–120°53′E,liesalongthecoastoftheYellowSeainEastChina.Thesimplevegetationcommunityalongthecoastisdistributedwithastratifiedpattern,fromthecoasttoinland,withthebaretidalflatsorsupportingcommunitiessuchasthosedominatedbySpartinaalternifloraLoisel.,SuaedaglaucaBge.,Imperatacylindrical(Linn.)Beauv.orPhragmitesaustralis(Cav.)Trin.exSteud.,andlastlybyotherxeromorphicvegetation.Humanlandusealongthiscoastalregionincludesmainlyagriculture/farming,aquaculture,andsaltproductionusingsolardryingtechniques.Inrecenttimes,humanactivitiessuchasharborbuilding,windpowergeneration,andtourismhaveincreased(Maetal.2014).Twonationalnaturalwetlandsreserves,theRed-crownCraneNationalReserve,andtheDafengMiluNationalNaturalReserve,havebeendesignatedalongtheyellowseacoasts(Fig.1).TakingintoconsiderationofhabitatchangesintheYanchengwetlandsfrom1975to2016,thenorthernbufferandcorezonesoftheYanchengNatureReservewereclassifiedintofourcategoriesbasedontheirreclamationhistory:unreclaimedareas,andareasreclaimedfor1–10,15–25,and30–40years.Wealsodefinedthepost-reclaimedhabitatstoeighttypes:urbanhabitat,bareflat,Suaedaglauca,reedhabitat,Spartinaalterniflora,farmland,saltpanandfishpond(Lietal.2019).BirdsurveyInthisstudy,birdsurveyswerecarriedoutinthenorthexperimentalareaandcoreareaofYanchengnationalreservebasedonpointcounting,whichthesitescontainedfourreclamationhistoriesandeightpost-reclaimedhabitats(Lietal.2019).SamplingswereconductedfromNovembertonextFebruarytorecordwinteringwaterbirdspeciesfrom2009to2013.Basedonourlongtermexperience,tencountingpointswitha1kmradiuswererandomlyestablishedinthesitesofeachreclamationhistory.Toexcludeyear-toyearvariationinbirdpattern,werecordedthesamesamplingsitebysamemethodeveryyear.Thebirdsurveyswerecarriedoutwithinaradius1kmofsamplingsiteeachyearonfineweatherwithoutrainorsignificantwind.BirdspeciesandpopulationnumberwererecordedbyOLYMPUSbinoculars(10×42)andZeiss85monoculars(30×60).Usingthemaximumof2countsisknowntoyieldbiasedestimateofanimalabundanceandbiasedcovariaterelationshipswithabundance,duetoimperfectdetectionofspecies(Zouetal.2016).So,thesurveyofeachpointinourstudywasperformedtwiceduringthe14-dayinvestigationperiodinastudyingyearandnumberofspecieswithmaxcountingwereusedforfutureanalysis.DataanalysisWefirstcomparedthespeciesrichnessandspeciesabundanceofwaterbirds.TheKolmogorov–SmirnovtestwasperformedusingSPSS19.0(SPSS,Inc.,Chicago,IL)todeterminewhetherdataonbirdabundancewerenormallydistributed.Thesemivariogramfunctionwasusedtoexplainthespatialpatternofbirdabundancepattern.BlockkrigingwasappliedtointerpolatethisvariableintoaspatialsurfacemapusingGS+3.1.Moreover,speciesrichness,population,andShannon-Wienerindexofwinteringwaterbirdscouldbeexplainedbythegeneralizedlinermixedmodel(GLMM),wherereclamationhistory(Orderedvariable.1:unreclaimedareas,2:areasreclaimedfor1–10years,3:areasreclaimedfor15–25years,and4:areasreclaimedfor30–40years),post-reclamationhabitattypes(Orderedvariable.1:urbanhabitat,2:bareflat,3:Suaedaglauca,4:reedhabitat,5:Spartinaalterniflora,6:farmland,7:saltpanand8:fishpond)werethefactorsandthestudyyears,samplingpointsandtheirinteractiontermwastreatedastherandomfactors.Wealsousedtherandomforestmodeltoplotthepartialeffectofsurveyingyears,reclamationhistory,post-reclamationhabitattypeontheonthespeciesrichness,population,andShannon-Wienerdiversityofwinteringwaterbirds(RpackageRandomForest;Breiman2001).ResultsFrom2009to2013,atotalof68waterbirdspeciesbelongingto6orders,16families,and39generawererecorded.30specieswith12657individuals,20specieswith9502individuals,23specieswith9657individuals,31specieswith8718individualsand22specieswith7376individualswererecordedin2009,2010,2011,2012and2013respectively.ThemostimportantdominatespeciesduringfiveyearswereGrusgrus,AnserfabalisandAnasplatyrhynchos.Moreover,theabundancepatternofwinteringbirdsalsochangedduringfiveyears,whichthemiddleandsouthpartofstudyingsitessuppliedhotspotsitesforwinteringbirds(Fig.2).Species,speciesabundanceofwinteringwaterbirdsvariedinthedifferentreclamationhistoriesandpost-reclamationhabitats.Thenumberofwaterbirdspeciesinthehabitatsreclaimedfor1–10yearswassignificantlylowerthanthoseinhabitatswithotherreclamationhistories(P<0.05).Speciesabundanceofwaterbirdswassignificantlyhigherinfourhabitats(unreclaimedS.sylvestris,fishpond,andreedhabitatsreclaimedfor15–25years,andbare-flathabitatsreclaimedfor30–40years)thantheothers(P<0.05).Whenquantifyinghowcoastalreclamationaffectedspeciesrichness,speciesabundanceandShannon-Wienerdiversityofwinteringwaterbirds,theGLMMhighlightedtheroleofreclamationhistory,post-reclamationhabitattypeandtheirinteractionsinbothspeciesabundanceandShannon-Wienerdiversityofwinteringwaterbirds,butthesevariablesdidnotaffectthespeciesrichnessofwaterbirds(GLMM,ALLP>0.05)(Table1).Furthermore,therandomforestresultsclearlyshowedapositiveassociationbetweenreclamationhistorywithspeciesrichness,speciesabundanceandShannon-Wienerdiversityofwinteringwaterbirds.Moreover,threepost-reclamationhabitattype,Suaedaglauca,Bareflatandfishpondplayedimportantrolesforwinteringbirds(Fig.3).DiscussionChangesinlandusetypecausedbyreclamationresultinhabitatchange,whichinturnmayleadwaterbirdstoselectotherhabitatsforinhabitationandfood.Therefore,theinfluenceofreclamationonwaterbirddiversityismainlyreflectedontheutilizationofreclaimedareasbywaterbirdsassupplementaryhabitats;thisisaffectedbythelengthofreclamationhistoryandthequalityofseasonalchangesinpost-reclamationhabitats.Ourresultsshowedthatbothreclamationhistoryandpost-reclamationhabitatsandtheirinteractionsweremainfactorsforshapingspeciesrichness,speciesabundance,andShannon-Wienerdiversityofwinteringwaterbirds.Thenumberofbirdspeciesinhabitatsreclaimedfor15–25yearswashigherthaninhabitatsreclaimedfor1–10years.Thiscouldbeattributedtoanincreasedlengthofreclamationhistoryleadingtoanincreaseandstabilizationofhabitatdiversity(Maetal.2014),therebyresultinginalargernumberofbirdspecies.Sucharesultisalsoconsistentwiththeintermediatedisturbancehypothesis,whichpredictsadecreaseinwaterbirddiversitywhendisturbanceincreasesbyacertaindegree,duetotheparabolicrelationshipbetweendiversityandthedegreeofdisturbance.Therefore,themaximumvalueforbirddiversityoccurswhent