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Waterbird Composition and Changes With Wetland ParkConstruction at Lake Dianchi YunnanndashGuizhou Plateau
Authors Wang Rong-Xing and Yang Xiao-Jun
Source Mountain Research and Development 41(1)
Published By International Mountain Society
URL httpsdoiorg101659MRD-JOURNAL-D-19-000551
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Waterbird Composition and Changes With WetlandPark Construction at Lake Dianchi YunnanndashGuizhouPlateauRong-Xing Wang12 and Xiao-Jun Yang1 Corresponding author yangxjmailkizaccn1 State Key Laboratory of Genetic Resources and Evolution Kunming Institute of Zoology Kunming 650223 Yunnan China2 Institute of Eastern-Himalaya Biodiversity Research Dali University Dali 671003 Yunnan China
2021 Wang and Yang This open access article is licensed under a Creative Commons Attribution 40 International License (httpcreativecommonsorglicensesby40) Please credit the authors and the full source
Establishing effectivelyprotected and managedecosystems with highbiodiversity is the broad aimof the Aichi initiativeAssessing the biodiversity of aspecific ecosystem is the firststep in estimating its
conservation value Most lakes on the YunnanndashGuizhou Plateauare formed by mountain faulting and are surrounded by humansettlements Lake ecosystems are fragile and frequently disturbedby pollution agricultural activities and tourism The currentlakeside wetland parks are intended to abate pollution andpromote tourism However the composition of the monthly andyearly waterbird population and the impacts of the parks onwaterbirds are unclear Using direct observation and spot mapcensus methods we conducted 104 field surveys across 4consecutive years at Lake Dianchi to fill the gaps in currentknowledge The results showed that Dianchi could provide habitats
for more than 60000 individual birds of 105 species including
residents summer visitors migrants and winter visitors The
current oxidation ponds in wetland parks created for water
purification and tourism were not suitable for most shorebirds
Consequently we suggest that plans for the construction of
artificial wetlands or wetland parks in this region should consider
the habitat requirements of different waterbirds in different
seasons Particular attention should be given to protecting the
marshlands and mudflats that wading birds require We also
suggest that increased waterbird monitoring in different seasons
across different years is needed around Lake Dianchi and other
wetlands on the YunnanndashGuizhou Plateau for effective
conservation
Keywords waterbird composition shorebirds wetland park Lake
Dianchi wetland management Ramsar convention
Received 19 August 2019 Accepted 21 January 2021
Introduction
Effectively maintained and managed ecosystems with highbiodiversity are among the International Union forConservation of Naturersquos Aichi targets drawn up at theConvention on Biological Diversity (CBD 2010) In line withthis successful conservation of global waterbird populationsdepends on effective governance (Amano et al 2018)Assessing waterbird biodiversity is the first step in estimatingits conservation value and planning suitable managementstrategies In China 84 out of 260 waterbird species are indecline (Wang et al 2018) This is a warning to humans toprotect waterbirds and their habitats Appropriate action isneeded to investigate the environmental factors affectingwaterbird distribution and identify more wetlands with highwaterbird biodiversity For the former Ma et al (2010)reviewed the available literature and found that variousfactors influence waterbirds and that these are regionspecific They suggested that management should be timedto meet the specific needs of breeding stopover andwintering periods based on species diversity and seasonaldynamics For the latter more research has focused oncoastal wetlands than inland wetlands (reviewed by Wang et
al 2016) and only 4 wetlands on the YunnanndashGuizhou (YGP)have been listed as Wetlands of International Importance(Ramsar sites) Dashanbao Bitahai Napahai and Lashihai(Ramsar Convention Secretariat 2020) The YGP is 1 of 6major lake zones in China and includes 13 lakes covering anarea exceeding 10 km2 (Ma et al 2011) However no lakesamong these 13 have been listed as Ramsar sites (RamsarConvention Secretariat 2020) probably because their valuefor waterbird conservation is still unclear
The YGP lies in Southwest China and mainly consists ofmountainous land Most of the lakes are tectonic in origin(caused by deformation of the Earthrsquos crust) and aresurrounded by human settlements (Wang and Dou 1998)Lake ecosystems are fragile and often overburdened byexcessive discharge of domestic and industrial sewage theoverdevelopment of tourism and other factors Many lakesare heavily polluted Lake Dianchi for example is one of themost severely polluted lakes in China (Jin 2003) Of the 13lakes in the YGP 9 are well-known tourist attractions inYunnan Province (Liu et al 2012) To minimize pollutionwhile providing suitable sites for tourism many lakesidewetlands and other facilities have been built near lakes suchas Lake Dianchi Lake Erhai and Lake Yilong Usually these
Mountain Research and Development (MRD)An international peer-reviewed open access journalpublished by the International Mountain Society (IMS)wwwmrd-journalorg
MountainResearchSystems knowledge
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artificial wetlands are oxidation ponds appended to leisureand entertainment functions such as the pond-trail systemsin the lakeside areas of Lake Dianchi and Lake Erhai Theseponds are surrounded by dry grasslands trees and shrubs(Figure 1)
Waterbird population composition changes seasonallyand yearly as a result of climate change (Zhao et al 2019) TheYGP wetlands have always been regarded as a winteringplace for waterbirds Thus field surveys have mainly focusedon the winter months (eg Quan et al 2002 Yang et al 2010Cui et al 2014 Li and Yang 2015 Yang Liu He and Li 2020Yang Liu and Tian 2020) However few studies have focusedon the waterbird population composition across consecutivemonths and years To assess the waterbird biodiversity of theYGP lakes for the Aichi targets and then provide scientificguidance for lake management especially the constructionof lakeside wetlands it is essential to first ascertain theintegrated waterbird composition Related issues can then beconsidered In this study we used Lake Dianchi the largestin YGP as an example to (1) determine the speciescomposition and habitat requirements of waterbirds at LakeDianchi and (2) test the changes before and after theconstruction of lakeside wetland parks to propose targetedstrategies for subsequent wetland restoration and wetlandpark construction
Methods
Study area
Lake Dianchi (248400ndash258020N 1028370ndash1028480E hereafterDianchi) is a permanent freshwater lake located in KunmingCity Yunnan Province Southwest China The water area is281 km2 and the manually controlled water level has beenstable at 18875 masl over the past decade (Wu et al 2016Kunming Dianchi Administration Bureau 2018) The averagewater depth is ~43 m (Jin et al 2006) The lake is a crescent-shaped water body extending from north to south Dianchi isdivided into 2 parts Caohai in the north and Waihai in thesouth by a traffic dam The average length of the lake is~404 km the width is ~70 km and the shoreline is ~150km (Wang and Dou 1998) Dianchi is situated in thesubtropical climatic zone with an average annualtemperature of 1448C an average annual rainfall of 10361
mm and an annual frost-free period of 227 days (Wang andDou 1998)
Dianchi plays an important role in regulating themicroclimate of the surrounding area It contributes to theproductivity of the local industry agriculture husbandry andfisheries and it provides recreation for humans (Jin et al2006) However Dianchi is a relatively closed lake with a slowwater-exchange rate and low self-purification capacity A lakereclamation campaign carried out from 1966 to 1970 causedsevere damage to marsh wetlands in the Caohai area Inaddition large amounts of urban sewage and industrialwastewater have been discharged into the lake exceeding itsself-purification capacity and causing serious pollution It hasalso been badly affected by cyanobacteria outbreaks in recentdecades (Luo et al 2017) To control the pollution of Dianchithe Chinese government listed it as a national sewagetreatment project in the lsquolsquoThree Rivers and Three Lakesrsquorsquo(Liaohe Huaihe Haihe Taihu Chaohu and Dianchi) schemelaunched in 1995 (Liu and Qiu 2007) As a result somewetland parks have been constructed in the lakeside zone topurify the water and create leisure areas for citizens Wetlandparks are mainly in the form of oxidation ponds They aresmall water bodies with such aquatic plants as Phragmitesaustralis Typha orientalis Acorus calamus Eichhornia crassipesLemna minor and Pistia stratiotes (Wang et al 2016) outside theponds there are trails trees and lawns (Figure 1)
Selection of observation sites and sample plots
We surveyed all the lake surface and adjacent lakesidewetlands for Caohai For Waihai we used systematicsampling (every 5ndash7 km on the lakeshore) to set 22 fixedobstruction-free sites of approximately 1-km radius tosurvey the lake surface (Bibby et al 2000 Cao et al 2011)Adjacent sample plots were set on the outside of the lakeshoreline and the inner side of the lake road at eachobservation site Non-wetlands (village land farmland orgardens) with a width of at least 05 km were established asisolation belts to ensure that each plot was independent(Figure 2)
Selection of wetland parks
During our survey artificial lakeside wetlands were underconstruction Some wetland parks had already been built
FIGURE 1 A schematic model of lakeside wetland parks at Lake Dianchi The design includes 2 subsystems the central water purification system and the surrounding
leisure system The former consists of deep ponds and aquatic vegetation the latter consists of xerophytic vegetation (trees shrubs herbs) roads and trails
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before our survey and some started after This meant that wecould not obtain complete annual waterbird datasets forbefore and after construction for all of the wetland parksTherefore based on the completeness of our data collectionwe selected 2 representative sample plots S5 (Wangguanwetland park impact 1) and S8 (Ancient Dian Kingdomwetland park impact 2) for which there was annualwaterbird composition data for both before and afterconstruction (Figure 2) We integrated all the lakeside plotsof Dianchi into 1 large plot to act as a control plot (control)
Waterbird counts
We carried out a total of 104 surveys A preliminary surveyfor the selection of observation sites and plots wasconducted during 1 week in February 2013 Three surveyseach month (early middle and late) were conducted from
March 2013 to May 2015 One survey was conducted in themiddle of each month from June 2015 to May 2017 Therewere no surveys in April and November 2016 due tocontinued unfavorable weather (rainy foggy or windy) Eachsurvey lasted for 3 consecutive days from dawn to dusk Inthe case of unfavorable weather the survey was advanced orpostponed 1ndash2 days
For the lake surface we used a direct observation methodto count the rare birds (fewer than 1000 individuals perspecies) For the more common species (more than 1000individuals) such as Chroicocephalus ridibundus (black-headedgull) we used the component counts method to estimate theflock population (Bibby et al 2000 Cao et al 2011) Forconstructed wetlands and wetland parks we divided eachplot into several patches according to vegetation type andadopted a spot map census method to mark the species andtheir individuals on prepared maps (Bibby et al 2000) In
FIGURE 2 Study area and observation sites The upper inner graph shows the location of Lake Dianchi in the mountainous area of Asia shaded in gray (Keuroorner et al
2016)
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addition to obtain integrated information on thecomposition of the waterbird population of Dianchi inrecent years we obtained other waterbird distributioninformation from the literature and experiencedbirdwatchers
Statistical analysis
Species diversity estimation We used species accumulationcurves to assess our surveys and estimate species richness(Ugland et al 2003) We defined the cumulative number ofindividuals in a survey as the abundance of each species Inaddition we used the maximum abundance of each speciesto determine the population of waterbirds at Dianchi
Division of season and residence type According to thephenology and the seasonal classification method widelyused in China we set the seasons as spring (March to May)summer (June to August) autumn (September to November)and winter (December to February) We determined theresident types of waterbirds according to our continuousobservations and reference to The Avifauna of Yunnan ChinaVol I Non-Passeriformes (Yang et al 1995)
Ecological guilds classification Morphological form relates toecological function in birds (cf Ma et al 2010 Pigot et al2020) thus we divided the waterbirds into wading birds andswimming birds For the former we subdivided the birdsinto large shorebirds (herons storks godwits and others)which mainly rely on lakeside marshlands and smallshorebirds (sandpipers plovers and knots) which mainlyrely on mudflats We subdivided the latter into dabblingbirds (dabbling ducks and gulls) which mainly rely onshallow water and diving birds (diving ducks grebes andcormorants) which mainly rely on deep water
Changes in vegetation types We obtained satellite images ofthe 2 parks from Google Earth before and after wetlandconstruction and corrected habitat information (such asvegetation type) according to the field surveys We calculatedthe vegetation area of each patch before and afterconstruction in ArcGIS 93 (ESRI Inc) According to the typeof aquatic vegetation we classified each patch as high
emerging plant type (HE) high floating plant type (HF) lowemerging plant type (LE) low floating plant type (LF) mixedvegetation type (Mix) pond type (Pond) and mudflat type(Mudflat) (see Wang et al 2016) Changes in vegetation typemainly showed an increase in impervious surface and pondand a decrease in aquatic vegetation (Table 1 Figure 3)
Changes in waterbirds before and after the wetland parks Weused an asymmetric before-after-control-impact method toevaluate how wetland park construction affected waterbirds(Underwood 1994 Smith 2002) The species richness andShannonndashWiener diversity index (H0) of each plot (impact 1impact 2 and control) in a single survey were used asindicators of waterbird diversity In addition we used theaverage value of the aforementioned diversity to representlsquolsquobefore and after constructionrsquorsquo of impact 1 impact 2 andcontrol We used a general linear model to test differences inspecies diversity before and after wetland park constructionsusing IBM SPSS Statistics software (version 23) H0 andspecies richness were respectively used as dependentvariables survey sites (controlimpact CI) and the period(beforeafter BA) were used as fixed factors and survey yearswere used as random factors
We verified that the diversity and variance of eachguildmdashexcept for the H0 of Podicipediformes andLariformesmdashwere normally distributed and we used apaired t-test based on the monthly survey(s) to evaluatechanges in the diversity of each guild before and afterwetland park construction
Results
Species composition
We detected 67385 individuals belonging to 7 orders 15families and 99 species in all surveys from February 2013 toMay 2017 The species cumulation (rarefaction) curveshowed that our survey represented the waterbirdcomposition (Figure 4) The total number of species atDianchi was 105 including 6 species from recent referencesor birdwatchers Anser anser (greylag goose) (Xinhuanet 2017)Porzana cinerea (white-browed crake) (CBR 2020) Calidris
TABLE 1 Areas (ha) and their changing ratio () of different habitat types before and after the construction of 2 wetland parks at Lake Dianchi
Habitat type
S5 S8 Total
Be Af CR () Be Af CR () Be Af CA CR ()
HE 435 352 ndash196 959 000 ndash2393 1394 352 ndash1043 ndash1258
HF 935 000 ndash2184 230 1557 3313 1165 1557 392 473
LE 000 066 153 000 000 000 000 066 066 079
LF 1370 000 ndash3201 182 148 ndash087 1553 148 ndash1405 ndash1696
Mix 999 000 ndash2334 2059 000 ndash5141 3058 000 ndash3058 ndash3691
Mudflat 409 000 ndash955 000 000 000 409 000 ndash409 ndash494
Pond 132 2476 5476 576 1577 2499 708 4053 3345 4037
Total 4281 2893 ndash3242 4005 3281 ndash1809 8286 6174 ndash2112 ndash2549
Note S5 Wangguan wetland park S8 Ancient Dian Kingdom wetland park Be before wetland construction Af after wetland construction CR changing percentage
area () CA change area (ha) HE high emerging plant habitat HF high floating plant habitat LE low emerging plant habitat LF low floating plant habitat mix
mixed vegetation habitat mudflat mudflat habitat pond pond habitat
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melanotos (pectoral sandpiper) (Wang et al 2017) C alba(sanderling) (Wang et al 2017) Larus vegae (Vega gull) (Tu etal 2017) and L canus (mew gull) (Tu et al 2017) Three specieswere globally threatened (IUCN 2020) Aythya baeri (Baerrsquos
pochard) was listed as critically endangered Calidristenuirostris (great knot) was listed as endangered and Rissatridactyla (black-legged kittiwake) was listed as vulnerable(Appendix S1 Supplemental material httpsdoiorg101659MRD-JOURNAL-D-19-000551S1)
Ecological guilds and resident types
We found more wading species (69 species) than swimmingspecies (36 species) in all survey periods The formerincluded 33 large shorebirds and 36 small shorebirds andthe latter included 25 dabbling birds and 11 diving birdsShorebirds mainly comprised spring and autumn migrants(38 species) and resident birds (16 species) Swimming birdsmainly comprised winter visitors (29 species) (Figure 5A)The winter visitors which included more than 60000dabbling and large wading individuals were the dominantguilds at Dianchi These were followed by resident birdsmainly comprising large shorebirds (such as herons)Moreover more than 1000 migratory shorebirds usedDianchi as a stopover site (Figure 5B)
FIGURE 3 Changes in vegetation types before and after construction of 2 wetland parks Wangguan wetland park (A B) and Ancient Dian Kingdom wetland park (C D)
Habitat type HE high emerging plants type HF high floating plants type LE low emerging plants type LF low floating plants type Mix mixed vegetation type
Mudflat mudflat type Pond pond type
FIGURE 4 Rarefaction curves based on species and individuals of waterbirds
between February 2013 and May 2017 at Lake Dianchi China
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Impacts of wetland parks on waterbirds
The construction of wetland parks resulted in a significantdecrease in species richness and H0 (Table 2) For the controlplot the whole lakeside wetland held a mean (6 SD) of 20186 587 species and 1965 6 377 species before and after the
wetland parks were constructed respectively There were nosignificant differences (F frac14 013 P frac14 072) between the 2periods For the impact plots S5 held 579 6 547 speciesand 208 6 200 species before and after the construction ofthe wetland park respectively There were significantdifferences (F frac14 1085 P 001) between the 2 periods S8supported 400 6 221 species and 030 6 129 species beforeand after wetland park construction respectively Therewere significant differences (Ffrac14 8228 P 001) between the2 periods (Figure 6A) H0 showed the same patterns as speciesrichness (Figure 6B)
Except for the Lariformes and Anseriformes the speciesrichness of other guilds decreased significantly afterconstruction of the wetland parks Except for Gruiformesand Anseriformes the H0 of other guilds decreasedsignificantly after construction of the wetland parks(Figure 7 Table 3)
Discussion
High waterbird diversity needs adequate protection andmanagement
In this study we found more than 60000 individuals from105 waterbird species accounting for 4038 of the totalnumber of waterbirds in China (Wang et al 2018) Inparticular we found that the species richness of the migrantswas high Most of the species were small shorebirds whichrely strongly on mudflats and marshlands This findingsuggests that continuous monitoring throughout consecutivemonths and years is important to collect complete data onwaterbird population composition and propose timelymanagement measures
However only 4 wetlands (Dashanbao Napahai Bitahaiand Lashihai) on the YGP have been listed as internationallyimportant sites (Ramsar Convention Secretariat 2020) Usingthe data from our field surveys over the past decadeliterature and the website of BirdReport of China (httpwwwbirdreportcn) we analyzed the species composition ofDianchi and the 4 Ramsar wetlands We found that the
FIGURE 5 Species diversity of waterbirds in Lake Dianchi from March 2013 to
May 2017 Indicates the species richness (A) and abundance (B) of each
residence type in different ecological guilds
TABLE 2 Asymmetrical analysis of variance comparing waterbird diversity (species richness and H0e) before and after wetland park construction at 2 affected sites and
1 control site using a lsquolsquobeyond before-after-control-impactrsquorsquo design Significant differences are marked in bold type
Source
Species richness H0e
SS df MS F Sig SS df MS F Sig
CI Hypothesis 248947 100 248947 13199 000 979 100 979 5306 000
Error 26855 1424 18861 957 5191 0184
BA Hypothesis 12769 100 12769 758 009 429 100 429 952 008
Error 3942 234 16847 097 215 0451
Year Hypothesis 10452 200 5226 146 034 038 200 019 039 072
Error 14237 397 35845 095 198 0480
BA3CI Hypothesis 9670 100 9670 7360 000 598 100 598 6674 000
Error 31742 24160 1314 027 298 0090
BA3CI3year Hypothesis 009 200 004 000 100 016 200 008 033 072
Error 480229 25700 18686 6099 25700 0237
Note SS sum of squares df degrees of freedom MS mean square Sig significance C control I impact B before A after
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waterbird species richness of Dianchi was higher than that ofany of the Ramsar sites (Table 4) Furthermore in recentyears Dianchi has supported 3 species consideredendangered according to the International Union forConservation of Nature (Appendix S1 Supplemental materialhttpsdoiorg101659MRD-JOURNAL-D-19-000551S1)According to the Ramsar Convention Manual lsquolsquoA wetlandshould be considered internationally important if itregularly supports 20000 or more waterbirdsrsquorsquo (RamsarConvention Secretariat 2013) Dianchi has recently met this
criterion every year (see Wang et al 2016 Wang and Yang2020) Therefore we suggest that monitoring and protectionfor Dianchi should be strengthened in the future
Wetland park construction needs to consider the habitat
requirements of waterbirds
The zones adjacent to mountainous lakes on the YGP arenarrow and disturbed by human activities (such as grazingand tourism) Our study found that the lakeside zone around
FIGURE 6 Differences in species richness (A) and H0e (B) before and after the
construction of 2 wetland parks at Lake Dianchi The control represented the
entire lakeside wetlands of Lake Dianchi impact 1 represented the Wangguan
wetland Park (S5) and impact 2 represented the Ancient Dian Kingdom wetland
park (S8)
FIGURE 7 Comparisons of species richness (A) and H0e (B) for different waterbird
guilds before and after the construction of 2 wetland parks at Lake Dianchi PODI
Podicipediformes CICO Ciconiiformes GRUI Gruiformes CHAR
Charadriiformes LARI Lariformes ANSE Anseriformes The H0e of
Podicipediformes and Lariformes were not compared because each had just 1
species P 005 P 001 P 0001
TABLE 3 Waterbird diversity differences before and after the wetland parks by paired t-test The H0e of Podicipediformes
and Lariformes were not tested because each had just 1 species Significant differences are marked in bold type
Order
Diversity
index Mean SD SE t df P
Podicipediformes SR 046 059 012 382 2300 0001
Ciconiiformes H0e 030 055 011 271 2300 0013
SR 158 228 047 340 2300 0002
Gruiformes H0e 002 027 005 030 2300 0767
SR 063 092 019 331 2300 0003
Charadriiformes H0e 062 107 022 286 2300 0009
SR 433 710 145 299 2300 0007
Lariformes SR 017 056 012 145 2300 0162
Anseriformes H0e 005 018 004 145 2300 0162
SR 017 064 013 128 2300 0213
Note df degrees of freedom SR species richness H0e ShannonndashWiener diversity index
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Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
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Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
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Waterbird Composition and Changes With WetlandPark Construction at Lake Dianchi YunnanndashGuizhouPlateauRong-Xing Wang12 and Xiao-Jun Yang1 Corresponding author yangxjmailkizaccn1 State Key Laboratory of Genetic Resources and Evolution Kunming Institute of Zoology Kunming 650223 Yunnan China2 Institute of Eastern-Himalaya Biodiversity Research Dali University Dali 671003 Yunnan China
2021 Wang and Yang This open access article is licensed under a Creative Commons Attribution 40 International License (httpcreativecommonsorglicensesby40) Please credit the authors and the full source
Establishing effectivelyprotected and managedecosystems with highbiodiversity is the broad aimof the Aichi initiativeAssessing the biodiversity of aspecific ecosystem is the firststep in estimating its
conservation value Most lakes on the YunnanndashGuizhou Plateauare formed by mountain faulting and are surrounded by humansettlements Lake ecosystems are fragile and frequently disturbedby pollution agricultural activities and tourism The currentlakeside wetland parks are intended to abate pollution andpromote tourism However the composition of the monthly andyearly waterbird population and the impacts of the parks onwaterbirds are unclear Using direct observation and spot mapcensus methods we conducted 104 field surveys across 4consecutive years at Lake Dianchi to fill the gaps in currentknowledge The results showed that Dianchi could provide habitats
for more than 60000 individual birds of 105 species including
residents summer visitors migrants and winter visitors The
current oxidation ponds in wetland parks created for water
purification and tourism were not suitable for most shorebirds
Consequently we suggest that plans for the construction of
artificial wetlands or wetland parks in this region should consider
the habitat requirements of different waterbirds in different
seasons Particular attention should be given to protecting the
marshlands and mudflats that wading birds require We also
suggest that increased waterbird monitoring in different seasons
across different years is needed around Lake Dianchi and other
wetlands on the YunnanndashGuizhou Plateau for effective
conservation
Keywords waterbird composition shorebirds wetland park Lake
Dianchi wetland management Ramsar convention
Received 19 August 2019 Accepted 21 January 2021
Introduction
Effectively maintained and managed ecosystems with highbiodiversity are among the International Union forConservation of Naturersquos Aichi targets drawn up at theConvention on Biological Diversity (CBD 2010) In line withthis successful conservation of global waterbird populationsdepends on effective governance (Amano et al 2018)Assessing waterbird biodiversity is the first step in estimatingits conservation value and planning suitable managementstrategies In China 84 out of 260 waterbird species are indecline (Wang et al 2018) This is a warning to humans toprotect waterbirds and their habitats Appropriate action isneeded to investigate the environmental factors affectingwaterbird distribution and identify more wetlands with highwaterbird biodiversity For the former Ma et al (2010)reviewed the available literature and found that variousfactors influence waterbirds and that these are regionspecific They suggested that management should be timedto meet the specific needs of breeding stopover andwintering periods based on species diversity and seasonaldynamics For the latter more research has focused oncoastal wetlands than inland wetlands (reviewed by Wang et
al 2016) and only 4 wetlands on the YunnanndashGuizhou (YGP)have been listed as Wetlands of International Importance(Ramsar sites) Dashanbao Bitahai Napahai and Lashihai(Ramsar Convention Secretariat 2020) The YGP is 1 of 6major lake zones in China and includes 13 lakes covering anarea exceeding 10 km2 (Ma et al 2011) However no lakesamong these 13 have been listed as Ramsar sites (RamsarConvention Secretariat 2020) probably because their valuefor waterbird conservation is still unclear
The YGP lies in Southwest China and mainly consists ofmountainous land Most of the lakes are tectonic in origin(caused by deformation of the Earthrsquos crust) and aresurrounded by human settlements (Wang and Dou 1998)Lake ecosystems are fragile and often overburdened byexcessive discharge of domestic and industrial sewage theoverdevelopment of tourism and other factors Many lakesare heavily polluted Lake Dianchi for example is one of themost severely polluted lakes in China (Jin 2003) Of the 13lakes in the YGP 9 are well-known tourist attractions inYunnan Province (Liu et al 2012) To minimize pollutionwhile providing suitable sites for tourism many lakesidewetlands and other facilities have been built near lakes suchas Lake Dianchi Lake Erhai and Lake Yilong Usually these
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artificial wetlands are oxidation ponds appended to leisureand entertainment functions such as the pond-trail systemsin the lakeside areas of Lake Dianchi and Lake Erhai Theseponds are surrounded by dry grasslands trees and shrubs(Figure 1)
Waterbird population composition changes seasonallyand yearly as a result of climate change (Zhao et al 2019) TheYGP wetlands have always been regarded as a winteringplace for waterbirds Thus field surveys have mainly focusedon the winter months (eg Quan et al 2002 Yang et al 2010Cui et al 2014 Li and Yang 2015 Yang Liu He and Li 2020Yang Liu and Tian 2020) However few studies have focusedon the waterbird population composition across consecutivemonths and years To assess the waterbird biodiversity of theYGP lakes for the Aichi targets and then provide scientificguidance for lake management especially the constructionof lakeside wetlands it is essential to first ascertain theintegrated waterbird composition Related issues can then beconsidered In this study we used Lake Dianchi the largestin YGP as an example to (1) determine the speciescomposition and habitat requirements of waterbirds at LakeDianchi and (2) test the changes before and after theconstruction of lakeside wetland parks to propose targetedstrategies for subsequent wetland restoration and wetlandpark construction
Methods
Study area
Lake Dianchi (248400ndash258020N 1028370ndash1028480E hereafterDianchi) is a permanent freshwater lake located in KunmingCity Yunnan Province Southwest China The water area is281 km2 and the manually controlled water level has beenstable at 18875 masl over the past decade (Wu et al 2016Kunming Dianchi Administration Bureau 2018) The averagewater depth is ~43 m (Jin et al 2006) The lake is a crescent-shaped water body extending from north to south Dianchi isdivided into 2 parts Caohai in the north and Waihai in thesouth by a traffic dam The average length of the lake is~404 km the width is ~70 km and the shoreline is ~150km (Wang and Dou 1998) Dianchi is situated in thesubtropical climatic zone with an average annualtemperature of 1448C an average annual rainfall of 10361
mm and an annual frost-free period of 227 days (Wang andDou 1998)
Dianchi plays an important role in regulating themicroclimate of the surrounding area It contributes to theproductivity of the local industry agriculture husbandry andfisheries and it provides recreation for humans (Jin et al2006) However Dianchi is a relatively closed lake with a slowwater-exchange rate and low self-purification capacity A lakereclamation campaign carried out from 1966 to 1970 causedsevere damage to marsh wetlands in the Caohai area Inaddition large amounts of urban sewage and industrialwastewater have been discharged into the lake exceeding itsself-purification capacity and causing serious pollution It hasalso been badly affected by cyanobacteria outbreaks in recentdecades (Luo et al 2017) To control the pollution of Dianchithe Chinese government listed it as a national sewagetreatment project in the lsquolsquoThree Rivers and Three Lakesrsquorsquo(Liaohe Huaihe Haihe Taihu Chaohu and Dianchi) schemelaunched in 1995 (Liu and Qiu 2007) As a result somewetland parks have been constructed in the lakeside zone topurify the water and create leisure areas for citizens Wetlandparks are mainly in the form of oxidation ponds They aresmall water bodies with such aquatic plants as Phragmitesaustralis Typha orientalis Acorus calamus Eichhornia crassipesLemna minor and Pistia stratiotes (Wang et al 2016) outside theponds there are trails trees and lawns (Figure 1)
Selection of observation sites and sample plots
We surveyed all the lake surface and adjacent lakesidewetlands for Caohai For Waihai we used systematicsampling (every 5ndash7 km on the lakeshore) to set 22 fixedobstruction-free sites of approximately 1-km radius tosurvey the lake surface (Bibby et al 2000 Cao et al 2011)Adjacent sample plots were set on the outside of the lakeshoreline and the inner side of the lake road at eachobservation site Non-wetlands (village land farmland orgardens) with a width of at least 05 km were established asisolation belts to ensure that each plot was independent(Figure 2)
Selection of wetland parks
During our survey artificial lakeside wetlands were underconstruction Some wetland parks had already been built
FIGURE 1 A schematic model of lakeside wetland parks at Lake Dianchi The design includes 2 subsystems the central water purification system and the surrounding
leisure system The former consists of deep ponds and aquatic vegetation the latter consists of xerophytic vegetation (trees shrubs herbs) roads and trails
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before our survey and some started after This meant that wecould not obtain complete annual waterbird datasets forbefore and after construction for all of the wetland parksTherefore based on the completeness of our data collectionwe selected 2 representative sample plots S5 (Wangguanwetland park impact 1) and S8 (Ancient Dian Kingdomwetland park impact 2) for which there was annualwaterbird composition data for both before and afterconstruction (Figure 2) We integrated all the lakeside plotsof Dianchi into 1 large plot to act as a control plot (control)
Waterbird counts
We carried out a total of 104 surveys A preliminary surveyfor the selection of observation sites and plots wasconducted during 1 week in February 2013 Three surveyseach month (early middle and late) were conducted from
March 2013 to May 2015 One survey was conducted in themiddle of each month from June 2015 to May 2017 Therewere no surveys in April and November 2016 due tocontinued unfavorable weather (rainy foggy or windy) Eachsurvey lasted for 3 consecutive days from dawn to dusk Inthe case of unfavorable weather the survey was advanced orpostponed 1ndash2 days
For the lake surface we used a direct observation methodto count the rare birds (fewer than 1000 individuals perspecies) For the more common species (more than 1000individuals) such as Chroicocephalus ridibundus (black-headedgull) we used the component counts method to estimate theflock population (Bibby et al 2000 Cao et al 2011) Forconstructed wetlands and wetland parks we divided eachplot into several patches according to vegetation type andadopted a spot map census method to mark the species andtheir individuals on prepared maps (Bibby et al 2000) In
FIGURE 2 Study area and observation sites The upper inner graph shows the location of Lake Dianchi in the mountainous area of Asia shaded in gray (Keuroorner et al
2016)
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addition to obtain integrated information on thecomposition of the waterbird population of Dianchi inrecent years we obtained other waterbird distributioninformation from the literature and experiencedbirdwatchers
Statistical analysis
Species diversity estimation We used species accumulationcurves to assess our surveys and estimate species richness(Ugland et al 2003) We defined the cumulative number ofindividuals in a survey as the abundance of each species Inaddition we used the maximum abundance of each speciesto determine the population of waterbirds at Dianchi
Division of season and residence type According to thephenology and the seasonal classification method widelyused in China we set the seasons as spring (March to May)summer (June to August) autumn (September to November)and winter (December to February) We determined theresident types of waterbirds according to our continuousobservations and reference to The Avifauna of Yunnan ChinaVol I Non-Passeriformes (Yang et al 1995)
Ecological guilds classification Morphological form relates toecological function in birds (cf Ma et al 2010 Pigot et al2020) thus we divided the waterbirds into wading birds andswimming birds For the former we subdivided the birdsinto large shorebirds (herons storks godwits and others)which mainly rely on lakeside marshlands and smallshorebirds (sandpipers plovers and knots) which mainlyrely on mudflats We subdivided the latter into dabblingbirds (dabbling ducks and gulls) which mainly rely onshallow water and diving birds (diving ducks grebes andcormorants) which mainly rely on deep water
Changes in vegetation types We obtained satellite images ofthe 2 parks from Google Earth before and after wetlandconstruction and corrected habitat information (such asvegetation type) according to the field surveys We calculatedthe vegetation area of each patch before and afterconstruction in ArcGIS 93 (ESRI Inc) According to the typeof aquatic vegetation we classified each patch as high
emerging plant type (HE) high floating plant type (HF) lowemerging plant type (LE) low floating plant type (LF) mixedvegetation type (Mix) pond type (Pond) and mudflat type(Mudflat) (see Wang et al 2016) Changes in vegetation typemainly showed an increase in impervious surface and pondand a decrease in aquatic vegetation (Table 1 Figure 3)
Changes in waterbirds before and after the wetland parks Weused an asymmetric before-after-control-impact method toevaluate how wetland park construction affected waterbirds(Underwood 1994 Smith 2002) The species richness andShannonndashWiener diversity index (H0) of each plot (impact 1impact 2 and control) in a single survey were used asindicators of waterbird diversity In addition we used theaverage value of the aforementioned diversity to representlsquolsquobefore and after constructionrsquorsquo of impact 1 impact 2 andcontrol We used a general linear model to test differences inspecies diversity before and after wetland park constructionsusing IBM SPSS Statistics software (version 23) H0 andspecies richness were respectively used as dependentvariables survey sites (controlimpact CI) and the period(beforeafter BA) were used as fixed factors and survey yearswere used as random factors
We verified that the diversity and variance of eachguildmdashexcept for the H0 of Podicipediformes andLariformesmdashwere normally distributed and we used apaired t-test based on the monthly survey(s) to evaluatechanges in the diversity of each guild before and afterwetland park construction
Results
Species composition
We detected 67385 individuals belonging to 7 orders 15families and 99 species in all surveys from February 2013 toMay 2017 The species cumulation (rarefaction) curveshowed that our survey represented the waterbirdcomposition (Figure 4) The total number of species atDianchi was 105 including 6 species from recent referencesor birdwatchers Anser anser (greylag goose) (Xinhuanet 2017)Porzana cinerea (white-browed crake) (CBR 2020) Calidris
TABLE 1 Areas (ha) and their changing ratio () of different habitat types before and after the construction of 2 wetland parks at Lake Dianchi
Habitat type
S5 S8 Total
Be Af CR () Be Af CR () Be Af CA CR ()
HE 435 352 ndash196 959 000 ndash2393 1394 352 ndash1043 ndash1258
HF 935 000 ndash2184 230 1557 3313 1165 1557 392 473
LE 000 066 153 000 000 000 000 066 066 079
LF 1370 000 ndash3201 182 148 ndash087 1553 148 ndash1405 ndash1696
Mix 999 000 ndash2334 2059 000 ndash5141 3058 000 ndash3058 ndash3691
Mudflat 409 000 ndash955 000 000 000 409 000 ndash409 ndash494
Pond 132 2476 5476 576 1577 2499 708 4053 3345 4037
Total 4281 2893 ndash3242 4005 3281 ndash1809 8286 6174 ndash2112 ndash2549
Note S5 Wangguan wetland park S8 Ancient Dian Kingdom wetland park Be before wetland construction Af after wetland construction CR changing percentage
area () CA change area (ha) HE high emerging plant habitat HF high floating plant habitat LE low emerging plant habitat LF low floating plant habitat mix
mixed vegetation habitat mudflat mudflat habitat pond pond habitat
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melanotos (pectoral sandpiper) (Wang et al 2017) C alba(sanderling) (Wang et al 2017) Larus vegae (Vega gull) (Tu etal 2017) and L canus (mew gull) (Tu et al 2017) Three specieswere globally threatened (IUCN 2020) Aythya baeri (Baerrsquos
pochard) was listed as critically endangered Calidristenuirostris (great knot) was listed as endangered and Rissatridactyla (black-legged kittiwake) was listed as vulnerable(Appendix S1 Supplemental material httpsdoiorg101659MRD-JOURNAL-D-19-000551S1)
Ecological guilds and resident types
We found more wading species (69 species) than swimmingspecies (36 species) in all survey periods The formerincluded 33 large shorebirds and 36 small shorebirds andthe latter included 25 dabbling birds and 11 diving birdsShorebirds mainly comprised spring and autumn migrants(38 species) and resident birds (16 species) Swimming birdsmainly comprised winter visitors (29 species) (Figure 5A)The winter visitors which included more than 60000dabbling and large wading individuals were the dominantguilds at Dianchi These were followed by resident birdsmainly comprising large shorebirds (such as herons)Moreover more than 1000 migratory shorebirds usedDianchi as a stopover site (Figure 5B)
FIGURE 3 Changes in vegetation types before and after construction of 2 wetland parks Wangguan wetland park (A B) and Ancient Dian Kingdom wetland park (C D)
Habitat type HE high emerging plants type HF high floating plants type LE low emerging plants type LF low floating plants type Mix mixed vegetation type
Mudflat mudflat type Pond pond type
FIGURE 4 Rarefaction curves based on species and individuals of waterbirds
between February 2013 and May 2017 at Lake Dianchi China
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Impacts of wetland parks on waterbirds
The construction of wetland parks resulted in a significantdecrease in species richness and H0 (Table 2) For the controlplot the whole lakeside wetland held a mean (6 SD) of 20186 587 species and 1965 6 377 species before and after the
wetland parks were constructed respectively There were nosignificant differences (F frac14 013 P frac14 072) between the 2periods For the impact plots S5 held 579 6 547 speciesand 208 6 200 species before and after the construction ofthe wetland park respectively There were significantdifferences (F frac14 1085 P 001) between the 2 periods S8supported 400 6 221 species and 030 6 129 species beforeand after wetland park construction respectively Therewere significant differences (Ffrac14 8228 P 001) between the2 periods (Figure 6A) H0 showed the same patterns as speciesrichness (Figure 6B)
Except for the Lariformes and Anseriformes the speciesrichness of other guilds decreased significantly afterconstruction of the wetland parks Except for Gruiformesand Anseriformes the H0 of other guilds decreasedsignificantly after construction of the wetland parks(Figure 7 Table 3)
Discussion
High waterbird diversity needs adequate protection andmanagement
In this study we found more than 60000 individuals from105 waterbird species accounting for 4038 of the totalnumber of waterbirds in China (Wang et al 2018) Inparticular we found that the species richness of the migrantswas high Most of the species were small shorebirds whichrely strongly on mudflats and marshlands This findingsuggests that continuous monitoring throughout consecutivemonths and years is important to collect complete data onwaterbird population composition and propose timelymanagement measures
However only 4 wetlands (Dashanbao Napahai Bitahaiand Lashihai) on the YGP have been listed as internationallyimportant sites (Ramsar Convention Secretariat 2020) Usingthe data from our field surveys over the past decadeliterature and the website of BirdReport of China (httpwwwbirdreportcn) we analyzed the species composition ofDianchi and the 4 Ramsar wetlands We found that the
FIGURE 5 Species diversity of waterbirds in Lake Dianchi from March 2013 to
May 2017 Indicates the species richness (A) and abundance (B) of each
residence type in different ecological guilds
TABLE 2 Asymmetrical analysis of variance comparing waterbird diversity (species richness and H0e) before and after wetland park construction at 2 affected sites and
1 control site using a lsquolsquobeyond before-after-control-impactrsquorsquo design Significant differences are marked in bold type
Source
Species richness H0e
SS df MS F Sig SS df MS F Sig
CI Hypothesis 248947 100 248947 13199 000 979 100 979 5306 000
Error 26855 1424 18861 957 5191 0184
BA Hypothesis 12769 100 12769 758 009 429 100 429 952 008
Error 3942 234 16847 097 215 0451
Year Hypothesis 10452 200 5226 146 034 038 200 019 039 072
Error 14237 397 35845 095 198 0480
BA3CI Hypothesis 9670 100 9670 7360 000 598 100 598 6674 000
Error 31742 24160 1314 027 298 0090
BA3CI3year Hypothesis 009 200 004 000 100 016 200 008 033 072
Error 480229 25700 18686 6099 25700 0237
Note SS sum of squares df degrees of freedom MS mean square Sig significance C control I impact B before A after
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waterbird species richness of Dianchi was higher than that ofany of the Ramsar sites (Table 4) Furthermore in recentyears Dianchi has supported 3 species consideredendangered according to the International Union forConservation of Nature (Appendix S1 Supplemental materialhttpsdoiorg101659MRD-JOURNAL-D-19-000551S1)According to the Ramsar Convention Manual lsquolsquoA wetlandshould be considered internationally important if itregularly supports 20000 or more waterbirdsrsquorsquo (RamsarConvention Secretariat 2013) Dianchi has recently met this
criterion every year (see Wang et al 2016 Wang and Yang2020) Therefore we suggest that monitoring and protectionfor Dianchi should be strengthened in the future
Wetland park construction needs to consider the habitat
requirements of waterbirds
The zones adjacent to mountainous lakes on the YGP arenarrow and disturbed by human activities (such as grazingand tourism) Our study found that the lakeside zone around
FIGURE 6 Differences in species richness (A) and H0e (B) before and after the
construction of 2 wetland parks at Lake Dianchi The control represented the
entire lakeside wetlands of Lake Dianchi impact 1 represented the Wangguan
wetland Park (S5) and impact 2 represented the Ancient Dian Kingdom wetland
park (S8)
FIGURE 7 Comparisons of species richness (A) and H0e (B) for different waterbird
guilds before and after the construction of 2 wetland parks at Lake Dianchi PODI
Podicipediformes CICO Ciconiiformes GRUI Gruiformes CHAR
Charadriiformes LARI Lariformes ANSE Anseriformes The H0e of
Podicipediformes and Lariformes were not compared because each had just 1
species P 005 P 001 P 0001
TABLE 3 Waterbird diversity differences before and after the wetland parks by paired t-test The H0e of Podicipediformes
and Lariformes were not tested because each had just 1 species Significant differences are marked in bold type
Order
Diversity
index Mean SD SE t df P
Podicipediformes SR 046 059 012 382 2300 0001
Ciconiiformes H0e 030 055 011 271 2300 0013
SR 158 228 047 340 2300 0002
Gruiformes H0e 002 027 005 030 2300 0767
SR 063 092 019 331 2300 0003
Charadriiformes H0e 062 107 022 286 2300 0009
SR 433 710 145 299 2300 0007
Lariformes SR 017 056 012 145 2300 0162
Anseriformes H0e 005 018 004 145 2300 0162
SR 017 064 013 128 2300 0213
Note df degrees of freedom SR species richness H0e ShannonndashWiener diversity index
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Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
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Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
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artificial wetlands are oxidation ponds appended to leisureand entertainment functions such as the pond-trail systemsin the lakeside areas of Lake Dianchi and Lake Erhai Theseponds are surrounded by dry grasslands trees and shrubs(Figure 1)
Waterbird population composition changes seasonallyand yearly as a result of climate change (Zhao et al 2019) TheYGP wetlands have always been regarded as a winteringplace for waterbirds Thus field surveys have mainly focusedon the winter months (eg Quan et al 2002 Yang et al 2010Cui et al 2014 Li and Yang 2015 Yang Liu He and Li 2020Yang Liu and Tian 2020) However few studies have focusedon the waterbird population composition across consecutivemonths and years To assess the waterbird biodiversity of theYGP lakes for the Aichi targets and then provide scientificguidance for lake management especially the constructionof lakeside wetlands it is essential to first ascertain theintegrated waterbird composition Related issues can then beconsidered In this study we used Lake Dianchi the largestin YGP as an example to (1) determine the speciescomposition and habitat requirements of waterbirds at LakeDianchi and (2) test the changes before and after theconstruction of lakeside wetland parks to propose targetedstrategies for subsequent wetland restoration and wetlandpark construction
Methods
Study area
Lake Dianchi (248400ndash258020N 1028370ndash1028480E hereafterDianchi) is a permanent freshwater lake located in KunmingCity Yunnan Province Southwest China The water area is281 km2 and the manually controlled water level has beenstable at 18875 masl over the past decade (Wu et al 2016Kunming Dianchi Administration Bureau 2018) The averagewater depth is ~43 m (Jin et al 2006) The lake is a crescent-shaped water body extending from north to south Dianchi isdivided into 2 parts Caohai in the north and Waihai in thesouth by a traffic dam The average length of the lake is~404 km the width is ~70 km and the shoreline is ~150km (Wang and Dou 1998) Dianchi is situated in thesubtropical climatic zone with an average annualtemperature of 1448C an average annual rainfall of 10361
mm and an annual frost-free period of 227 days (Wang andDou 1998)
Dianchi plays an important role in regulating themicroclimate of the surrounding area It contributes to theproductivity of the local industry agriculture husbandry andfisheries and it provides recreation for humans (Jin et al2006) However Dianchi is a relatively closed lake with a slowwater-exchange rate and low self-purification capacity A lakereclamation campaign carried out from 1966 to 1970 causedsevere damage to marsh wetlands in the Caohai area Inaddition large amounts of urban sewage and industrialwastewater have been discharged into the lake exceeding itsself-purification capacity and causing serious pollution It hasalso been badly affected by cyanobacteria outbreaks in recentdecades (Luo et al 2017) To control the pollution of Dianchithe Chinese government listed it as a national sewagetreatment project in the lsquolsquoThree Rivers and Three Lakesrsquorsquo(Liaohe Huaihe Haihe Taihu Chaohu and Dianchi) schemelaunched in 1995 (Liu and Qiu 2007) As a result somewetland parks have been constructed in the lakeside zone topurify the water and create leisure areas for citizens Wetlandparks are mainly in the form of oxidation ponds They aresmall water bodies with such aquatic plants as Phragmitesaustralis Typha orientalis Acorus calamus Eichhornia crassipesLemna minor and Pistia stratiotes (Wang et al 2016) outside theponds there are trails trees and lawns (Figure 1)
Selection of observation sites and sample plots
We surveyed all the lake surface and adjacent lakesidewetlands for Caohai For Waihai we used systematicsampling (every 5ndash7 km on the lakeshore) to set 22 fixedobstruction-free sites of approximately 1-km radius tosurvey the lake surface (Bibby et al 2000 Cao et al 2011)Adjacent sample plots were set on the outside of the lakeshoreline and the inner side of the lake road at eachobservation site Non-wetlands (village land farmland orgardens) with a width of at least 05 km were established asisolation belts to ensure that each plot was independent(Figure 2)
Selection of wetland parks
During our survey artificial lakeside wetlands were underconstruction Some wetland parks had already been built
FIGURE 1 A schematic model of lakeside wetland parks at Lake Dianchi The design includes 2 subsystems the central water purification system and the surrounding
leisure system The former consists of deep ponds and aquatic vegetation the latter consists of xerophytic vegetation (trees shrubs herbs) roads and trails
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before our survey and some started after This meant that wecould not obtain complete annual waterbird datasets forbefore and after construction for all of the wetland parksTherefore based on the completeness of our data collectionwe selected 2 representative sample plots S5 (Wangguanwetland park impact 1) and S8 (Ancient Dian Kingdomwetland park impact 2) for which there was annualwaterbird composition data for both before and afterconstruction (Figure 2) We integrated all the lakeside plotsof Dianchi into 1 large plot to act as a control plot (control)
Waterbird counts
We carried out a total of 104 surveys A preliminary surveyfor the selection of observation sites and plots wasconducted during 1 week in February 2013 Three surveyseach month (early middle and late) were conducted from
March 2013 to May 2015 One survey was conducted in themiddle of each month from June 2015 to May 2017 Therewere no surveys in April and November 2016 due tocontinued unfavorable weather (rainy foggy or windy) Eachsurvey lasted for 3 consecutive days from dawn to dusk Inthe case of unfavorable weather the survey was advanced orpostponed 1ndash2 days
For the lake surface we used a direct observation methodto count the rare birds (fewer than 1000 individuals perspecies) For the more common species (more than 1000individuals) such as Chroicocephalus ridibundus (black-headedgull) we used the component counts method to estimate theflock population (Bibby et al 2000 Cao et al 2011) Forconstructed wetlands and wetland parks we divided eachplot into several patches according to vegetation type andadopted a spot map census method to mark the species andtheir individuals on prepared maps (Bibby et al 2000) In
FIGURE 2 Study area and observation sites The upper inner graph shows the location of Lake Dianchi in the mountainous area of Asia shaded in gray (Keuroorner et al
2016)
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addition to obtain integrated information on thecomposition of the waterbird population of Dianchi inrecent years we obtained other waterbird distributioninformation from the literature and experiencedbirdwatchers
Statistical analysis
Species diversity estimation We used species accumulationcurves to assess our surveys and estimate species richness(Ugland et al 2003) We defined the cumulative number ofindividuals in a survey as the abundance of each species Inaddition we used the maximum abundance of each speciesto determine the population of waterbirds at Dianchi
Division of season and residence type According to thephenology and the seasonal classification method widelyused in China we set the seasons as spring (March to May)summer (June to August) autumn (September to November)and winter (December to February) We determined theresident types of waterbirds according to our continuousobservations and reference to The Avifauna of Yunnan ChinaVol I Non-Passeriformes (Yang et al 1995)
Ecological guilds classification Morphological form relates toecological function in birds (cf Ma et al 2010 Pigot et al2020) thus we divided the waterbirds into wading birds andswimming birds For the former we subdivided the birdsinto large shorebirds (herons storks godwits and others)which mainly rely on lakeside marshlands and smallshorebirds (sandpipers plovers and knots) which mainlyrely on mudflats We subdivided the latter into dabblingbirds (dabbling ducks and gulls) which mainly rely onshallow water and diving birds (diving ducks grebes andcormorants) which mainly rely on deep water
Changes in vegetation types We obtained satellite images ofthe 2 parks from Google Earth before and after wetlandconstruction and corrected habitat information (such asvegetation type) according to the field surveys We calculatedthe vegetation area of each patch before and afterconstruction in ArcGIS 93 (ESRI Inc) According to the typeof aquatic vegetation we classified each patch as high
emerging plant type (HE) high floating plant type (HF) lowemerging plant type (LE) low floating plant type (LF) mixedvegetation type (Mix) pond type (Pond) and mudflat type(Mudflat) (see Wang et al 2016) Changes in vegetation typemainly showed an increase in impervious surface and pondand a decrease in aquatic vegetation (Table 1 Figure 3)
Changes in waterbirds before and after the wetland parks Weused an asymmetric before-after-control-impact method toevaluate how wetland park construction affected waterbirds(Underwood 1994 Smith 2002) The species richness andShannonndashWiener diversity index (H0) of each plot (impact 1impact 2 and control) in a single survey were used asindicators of waterbird diversity In addition we used theaverage value of the aforementioned diversity to representlsquolsquobefore and after constructionrsquorsquo of impact 1 impact 2 andcontrol We used a general linear model to test differences inspecies diversity before and after wetland park constructionsusing IBM SPSS Statistics software (version 23) H0 andspecies richness were respectively used as dependentvariables survey sites (controlimpact CI) and the period(beforeafter BA) were used as fixed factors and survey yearswere used as random factors
We verified that the diversity and variance of eachguildmdashexcept for the H0 of Podicipediformes andLariformesmdashwere normally distributed and we used apaired t-test based on the monthly survey(s) to evaluatechanges in the diversity of each guild before and afterwetland park construction
Results
Species composition
We detected 67385 individuals belonging to 7 orders 15families and 99 species in all surveys from February 2013 toMay 2017 The species cumulation (rarefaction) curveshowed that our survey represented the waterbirdcomposition (Figure 4) The total number of species atDianchi was 105 including 6 species from recent referencesor birdwatchers Anser anser (greylag goose) (Xinhuanet 2017)Porzana cinerea (white-browed crake) (CBR 2020) Calidris
TABLE 1 Areas (ha) and their changing ratio () of different habitat types before and after the construction of 2 wetland parks at Lake Dianchi
Habitat type
S5 S8 Total
Be Af CR () Be Af CR () Be Af CA CR ()
HE 435 352 ndash196 959 000 ndash2393 1394 352 ndash1043 ndash1258
HF 935 000 ndash2184 230 1557 3313 1165 1557 392 473
LE 000 066 153 000 000 000 000 066 066 079
LF 1370 000 ndash3201 182 148 ndash087 1553 148 ndash1405 ndash1696
Mix 999 000 ndash2334 2059 000 ndash5141 3058 000 ndash3058 ndash3691
Mudflat 409 000 ndash955 000 000 000 409 000 ndash409 ndash494
Pond 132 2476 5476 576 1577 2499 708 4053 3345 4037
Total 4281 2893 ndash3242 4005 3281 ndash1809 8286 6174 ndash2112 ndash2549
Note S5 Wangguan wetland park S8 Ancient Dian Kingdom wetland park Be before wetland construction Af after wetland construction CR changing percentage
area () CA change area (ha) HE high emerging plant habitat HF high floating plant habitat LE low emerging plant habitat LF low floating plant habitat mix
mixed vegetation habitat mudflat mudflat habitat pond pond habitat
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melanotos (pectoral sandpiper) (Wang et al 2017) C alba(sanderling) (Wang et al 2017) Larus vegae (Vega gull) (Tu etal 2017) and L canus (mew gull) (Tu et al 2017) Three specieswere globally threatened (IUCN 2020) Aythya baeri (Baerrsquos
pochard) was listed as critically endangered Calidristenuirostris (great knot) was listed as endangered and Rissatridactyla (black-legged kittiwake) was listed as vulnerable(Appendix S1 Supplemental material httpsdoiorg101659MRD-JOURNAL-D-19-000551S1)
Ecological guilds and resident types
We found more wading species (69 species) than swimmingspecies (36 species) in all survey periods The formerincluded 33 large shorebirds and 36 small shorebirds andthe latter included 25 dabbling birds and 11 diving birdsShorebirds mainly comprised spring and autumn migrants(38 species) and resident birds (16 species) Swimming birdsmainly comprised winter visitors (29 species) (Figure 5A)The winter visitors which included more than 60000dabbling and large wading individuals were the dominantguilds at Dianchi These were followed by resident birdsmainly comprising large shorebirds (such as herons)Moreover more than 1000 migratory shorebirds usedDianchi as a stopover site (Figure 5B)
FIGURE 3 Changes in vegetation types before and after construction of 2 wetland parks Wangguan wetland park (A B) and Ancient Dian Kingdom wetland park (C D)
Habitat type HE high emerging plants type HF high floating plants type LE low emerging plants type LF low floating plants type Mix mixed vegetation type
Mudflat mudflat type Pond pond type
FIGURE 4 Rarefaction curves based on species and individuals of waterbirds
between February 2013 and May 2017 at Lake Dianchi China
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Impacts of wetland parks on waterbirds
The construction of wetland parks resulted in a significantdecrease in species richness and H0 (Table 2) For the controlplot the whole lakeside wetland held a mean (6 SD) of 20186 587 species and 1965 6 377 species before and after the
wetland parks were constructed respectively There were nosignificant differences (F frac14 013 P frac14 072) between the 2periods For the impact plots S5 held 579 6 547 speciesand 208 6 200 species before and after the construction ofthe wetland park respectively There were significantdifferences (F frac14 1085 P 001) between the 2 periods S8supported 400 6 221 species and 030 6 129 species beforeand after wetland park construction respectively Therewere significant differences (Ffrac14 8228 P 001) between the2 periods (Figure 6A) H0 showed the same patterns as speciesrichness (Figure 6B)
Except for the Lariformes and Anseriformes the speciesrichness of other guilds decreased significantly afterconstruction of the wetland parks Except for Gruiformesand Anseriformes the H0 of other guilds decreasedsignificantly after construction of the wetland parks(Figure 7 Table 3)
Discussion
High waterbird diversity needs adequate protection andmanagement
In this study we found more than 60000 individuals from105 waterbird species accounting for 4038 of the totalnumber of waterbirds in China (Wang et al 2018) Inparticular we found that the species richness of the migrantswas high Most of the species were small shorebirds whichrely strongly on mudflats and marshlands This findingsuggests that continuous monitoring throughout consecutivemonths and years is important to collect complete data onwaterbird population composition and propose timelymanagement measures
However only 4 wetlands (Dashanbao Napahai Bitahaiand Lashihai) on the YGP have been listed as internationallyimportant sites (Ramsar Convention Secretariat 2020) Usingthe data from our field surveys over the past decadeliterature and the website of BirdReport of China (httpwwwbirdreportcn) we analyzed the species composition ofDianchi and the 4 Ramsar wetlands We found that the
FIGURE 5 Species diversity of waterbirds in Lake Dianchi from March 2013 to
May 2017 Indicates the species richness (A) and abundance (B) of each
residence type in different ecological guilds
TABLE 2 Asymmetrical analysis of variance comparing waterbird diversity (species richness and H0e) before and after wetland park construction at 2 affected sites and
1 control site using a lsquolsquobeyond before-after-control-impactrsquorsquo design Significant differences are marked in bold type
Source
Species richness H0e
SS df MS F Sig SS df MS F Sig
CI Hypothesis 248947 100 248947 13199 000 979 100 979 5306 000
Error 26855 1424 18861 957 5191 0184
BA Hypothesis 12769 100 12769 758 009 429 100 429 952 008
Error 3942 234 16847 097 215 0451
Year Hypothesis 10452 200 5226 146 034 038 200 019 039 072
Error 14237 397 35845 095 198 0480
BA3CI Hypothesis 9670 100 9670 7360 000 598 100 598 6674 000
Error 31742 24160 1314 027 298 0090
BA3CI3year Hypothesis 009 200 004 000 100 016 200 008 033 072
Error 480229 25700 18686 6099 25700 0237
Note SS sum of squares df degrees of freedom MS mean square Sig significance C control I impact B before A after
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waterbird species richness of Dianchi was higher than that ofany of the Ramsar sites (Table 4) Furthermore in recentyears Dianchi has supported 3 species consideredendangered according to the International Union forConservation of Nature (Appendix S1 Supplemental materialhttpsdoiorg101659MRD-JOURNAL-D-19-000551S1)According to the Ramsar Convention Manual lsquolsquoA wetlandshould be considered internationally important if itregularly supports 20000 or more waterbirdsrsquorsquo (RamsarConvention Secretariat 2013) Dianchi has recently met this
criterion every year (see Wang et al 2016 Wang and Yang2020) Therefore we suggest that monitoring and protectionfor Dianchi should be strengthened in the future
Wetland park construction needs to consider the habitat
requirements of waterbirds
The zones adjacent to mountainous lakes on the YGP arenarrow and disturbed by human activities (such as grazingand tourism) Our study found that the lakeside zone around
FIGURE 6 Differences in species richness (A) and H0e (B) before and after the
construction of 2 wetland parks at Lake Dianchi The control represented the
entire lakeside wetlands of Lake Dianchi impact 1 represented the Wangguan
wetland Park (S5) and impact 2 represented the Ancient Dian Kingdom wetland
park (S8)
FIGURE 7 Comparisons of species richness (A) and H0e (B) for different waterbird
guilds before and after the construction of 2 wetland parks at Lake Dianchi PODI
Podicipediformes CICO Ciconiiformes GRUI Gruiformes CHAR
Charadriiformes LARI Lariformes ANSE Anseriformes The H0e of
Podicipediformes and Lariformes were not compared because each had just 1
species P 005 P 001 P 0001
TABLE 3 Waterbird diversity differences before and after the wetland parks by paired t-test The H0e of Podicipediformes
and Lariformes were not tested because each had just 1 species Significant differences are marked in bold type
Order
Diversity
index Mean SD SE t df P
Podicipediformes SR 046 059 012 382 2300 0001
Ciconiiformes H0e 030 055 011 271 2300 0013
SR 158 228 047 340 2300 0002
Gruiformes H0e 002 027 005 030 2300 0767
SR 063 092 019 331 2300 0003
Charadriiformes H0e 062 107 022 286 2300 0009
SR 433 710 145 299 2300 0007
Lariformes SR 017 056 012 145 2300 0162
Anseriformes H0e 005 018 004 145 2300 0162
SR 017 064 013 128 2300 0213
Note df degrees of freedom SR species richness H0e ShannonndashWiener diversity index
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Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
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Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
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before our survey and some started after This meant that wecould not obtain complete annual waterbird datasets forbefore and after construction for all of the wetland parksTherefore based on the completeness of our data collectionwe selected 2 representative sample plots S5 (Wangguanwetland park impact 1) and S8 (Ancient Dian Kingdomwetland park impact 2) for which there was annualwaterbird composition data for both before and afterconstruction (Figure 2) We integrated all the lakeside plotsof Dianchi into 1 large plot to act as a control plot (control)
Waterbird counts
We carried out a total of 104 surveys A preliminary surveyfor the selection of observation sites and plots wasconducted during 1 week in February 2013 Three surveyseach month (early middle and late) were conducted from
March 2013 to May 2015 One survey was conducted in themiddle of each month from June 2015 to May 2017 Therewere no surveys in April and November 2016 due tocontinued unfavorable weather (rainy foggy or windy) Eachsurvey lasted for 3 consecutive days from dawn to dusk Inthe case of unfavorable weather the survey was advanced orpostponed 1ndash2 days
For the lake surface we used a direct observation methodto count the rare birds (fewer than 1000 individuals perspecies) For the more common species (more than 1000individuals) such as Chroicocephalus ridibundus (black-headedgull) we used the component counts method to estimate theflock population (Bibby et al 2000 Cao et al 2011) Forconstructed wetlands and wetland parks we divided eachplot into several patches according to vegetation type andadopted a spot map census method to mark the species andtheir individuals on prepared maps (Bibby et al 2000) In
FIGURE 2 Study area and observation sites The upper inner graph shows the location of Lake Dianchi in the mountainous area of Asia shaded in gray (Keuroorner et al
2016)
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addition to obtain integrated information on thecomposition of the waterbird population of Dianchi inrecent years we obtained other waterbird distributioninformation from the literature and experiencedbirdwatchers
Statistical analysis
Species diversity estimation We used species accumulationcurves to assess our surveys and estimate species richness(Ugland et al 2003) We defined the cumulative number ofindividuals in a survey as the abundance of each species Inaddition we used the maximum abundance of each speciesto determine the population of waterbirds at Dianchi
Division of season and residence type According to thephenology and the seasonal classification method widelyused in China we set the seasons as spring (March to May)summer (June to August) autumn (September to November)and winter (December to February) We determined theresident types of waterbirds according to our continuousobservations and reference to The Avifauna of Yunnan ChinaVol I Non-Passeriformes (Yang et al 1995)
Ecological guilds classification Morphological form relates toecological function in birds (cf Ma et al 2010 Pigot et al2020) thus we divided the waterbirds into wading birds andswimming birds For the former we subdivided the birdsinto large shorebirds (herons storks godwits and others)which mainly rely on lakeside marshlands and smallshorebirds (sandpipers plovers and knots) which mainlyrely on mudflats We subdivided the latter into dabblingbirds (dabbling ducks and gulls) which mainly rely onshallow water and diving birds (diving ducks grebes andcormorants) which mainly rely on deep water
Changes in vegetation types We obtained satellite images ofthe 2 parks from Google Earth before and after wetlandconstruction and corrected habitat information (such asvegetation type) according to the field surveys We calculatedthe vegetation area of each patch before and afterconstruction in ArcGIS 93 (ESRI Inc) According to the typeof aquatic vegetation we classified each patch as high
emerging plant type (HE) high floating plant type (HF) lowemerging plant type (LE) low floating plant type (LF) mixedvegetation type (Mix) pond type (Pond) and mudflat type(Mudflat) (see Wang et al 2016) Changes in vegetation typemainly showed an increase in impervious surface and pondand a decrease in aquatic vegetation (Table 1 Figure 3)
Changes in waterbirds before and after the wetland parks Weused an asymmetric before-after-control-impact method toevaluate how wetland park construction affected waterbirds(Underwood 1994 Smith 2002) The species richness andShannonndashWiener diversity index (H0) of each plot (impact 1impact 2 and control) in a single survey were used asindicators of waterbird diversity In addition we used theaverage value of the aforementioned diversity to representlsquolsquobefore and after constructionrsquorsquo of impact 1 impact 2 andcontrol We used a general linear model to test differences inspecies diversity before and after wetland park constructionsusing IBM SPSS Statistics software (version 23) H0 andspecies richness were respectively used as dependentvariables survey sites (controlimpact CI) and the period(beforeafter BA) were used as fixed factors and survey yearswere used as random factors
We verified that the diversity and variance of eachguildmdashexcept for the H0 of Podicipediformes andLariformesmdashwere normally distributed and we used apaired t-test based on the monthly survey(s) to evaluatechanges in the diversity of each guild before and afterwetland park construction
Results
Species composition
We detected 67385 individuals belonging to 7 orders 15families and 99 species in all surveys from February 2013 toMay 2017 The species cumulation (rarefaction) curveshowed that our survey represented the waterbirdcomposition (Figure 4) The total number of species atDianchi was 105 including 6 species from recent referencesor birdwatchers Anser anser (greylag goose) (Xinhuanet 2017)Porzana cinerea (white-browed crake) (CBR 2020) Calidris
TABLE 1 Areas (ha) and their changing ratio () of different habitat types before and after the construction of 2 wetland parks at Lake Dianchi
Habitat type
S5 S8 Total
Be Af CR () Be Af CR () Be Af CA CR ()
HE 435 352 ndash196 959 000 ndash2393 1394 352 ndash1043 ndash1258
HF 935 000 ndash2184 230 1557 3313 1165 1557 392 473
LE 000 066 153 000 000 000 000 066 066 079
LF 1370 000 ndash3201 182 148 ndash087 1553 148 ndash1405 ndash1696
Mix 999 000 ndash2334 2059 000 ndash5141 3058 000 ndash3058 ndash3691
Mudflat 409 000 ndash955 000 000 000 409 000 ndash409 ndash494
Pond 132 2476 5476 576 1577 2499 708 4053 3345 4037
Total 4281 2893 ndash3242 4005 3281 ndash1809 8286 6174 ndash2112 ndash2549
Note S5 Wangguan wetland park S8 Ancient Dian Kingdom wetland park Be before wetland construction Af after wetland construction CR changing percentage
area () CA change area (ha) HE high emerging plant habitat HF high floating plant habitat LE low emerging plant habitat LF low floating plant habitat mix
mixed vegetation habitat mudflat mudflat habitat pond pond habitat
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melanotos (pectoral sandpiper) (Wang et al 2017) C alba(sanderling) (Wang et al 2017) Larus vegae (Vega gull) (Tu etal 2017) and L canus (mew gull) (Tu et al 2017) Three specieswere globally threatened (IUCN 2020) Aythya baeri (Baerrsquos
pochard) was listed as critically endangered Calidristenuirostris (great knot) was listed as endangered and Rissatridactyla (black-legged kittiwake) was listed as vulnerable(Appendix S1 Supplemental material httpsdoiorg101659MRD-JOURNAL-D-19-000551S1)
Ecological guilds and resident types
We found more wading species (69 species) than swimmingspecies (36 species) in all survey periods The formerincluded 33 large shorebirds and 36 small shorebirds andthe latter included 25 dabbling birds and 11 diving birdsShorebirds mainly comprised spring and autumn migrants(38 species) and resident birds (16 species) Swimming birdsmainly comprised winter visitors (29 species) (Figure 5A)The winter visitors which included more than 60000dabbling and large wading individuals were the dominantguilds at Dianchi These were followed by resident birdsmainly comprising large shorebirds (such as herons)Moreover more than 1000 migratory shorebirds usedDianchi as a stopover site (Figure 5B)
FIGURE 3 Changes in vegetation types before and after construction of 2 wetland parks Wangguan wetland park (A B) and Ancient Dian Kingdom wetland park (C D)
Habitat type HE high emerging plants type HF high floating plants type LE low emerging plants type LF low floating plants type Mix mixed vegetation type
Mudflat mudflat type Pond pond type
FIGURE 4 Rarefaction curves based on species and individuals of waterbirds
between February 2013 and May 2017 at Lake Dianchi China
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Impacts of wetland parks on waterbirds
The construction of wetland parks resulted in a significantdecrease in species richness and H0 (Table 2) For the controlplot the whole lakeside wetland held a mean (6 SD) of 20186 587 species and 1965 6 377 species before and after the
wetland parks were constructed respectively There were nosignificant differences (F frac14 013 P frac14 072) between the 2periods For the impact plots S5 held 579 6 547 speciesand 208 6 200 species before and after the construction ofthe wetland park respectively There were significantdifferences (F frac14 1085 P 001) between the 2 periods S8supported 400 6 221 species and 030 6 129 species beforeand after wetland park construction respectively Therewere significant differences (Ffrac14 8228 P 001) between the2 periods (Figure 6A) H0 showed the same patterns as speciesrichness (Figure 6B)
Except for the Lariformes and Anseriformes the speciesrichness of other guilds decreased significantly afterconstruction of the wetland parks Except for Gruiformesand Anseriformes the H0 of other guilds decreasedsignificantly after construction of the wetland parks(Figure 7 Table 3)
Discussion
High waterbird diversity needs adequate protection andmanagement
In this study we found more than 60000 individuals from105 waterbird species accounting for 4038 of the totalnumber of waterbirds in China (Wang et al 2018) Inparticular we found that the species richness of the migrantswas high Most of the species were small shorebirds whichrely strongly on mudflats and marshlands This findingsuggests that continuous monitoring throughout consecutivemonths and years is important to collect complete data onwaterbird population composition and propose timelymanagement measures
However only 4 wetlands (Dashanbao Napahai Bitahaiand Lashihai) on the YGP have been listed as internationallyimportant sites (Ramsar Convention Secretariat 2020) Usingthe data from our field surveys over the past decadeliterature and the website of BirdReport of China (httpwwwbirdreportcn) we analyzed the species composition ofDianchi and the 4 Ramsar wetlands We found that the
FIGURE 5 Species diversity of waterbirds in Lake Dianchi from March 2013 to
May 2017 Indicates the species richness (A) and abundance (B) of each
residence type in different ecological guilds
TABLE 2 Asymmetrical analysis of variance comparing waterbird diversity (species richness and H0e) before and after wetland park construction at 2 affected sites and
1 control site using a lsquolsquobeyond before-after-control-impactrsquorsquo design Significant differences are marked in bold type
Source
Species richness H0e
SS df MS F Sig SS df MS F Sig
CI Hypothesis 248947 100 248947 13199 000 979 100 979 5306 000
Error 26855 1424 18861 957 5191 0184
BA Hypothesis 12769 100 12769 758 009 429 100 429 952 008
Error 3942 234 16847 097 215 0451
Year Hypothesis 10452 200 5226 146 034 038 200 019 039 072
Error 14237 397 35845 095 198 0480
BA3CI Hypothesis 9670 100 9670 7360 000 598 100 598 6674 000
Error 31742 24160 1314 027 298 0090
BA3CI3year Hypothesis 009 200 004 000 100 016 200 008 033 072
Error 480229 25700 18686 6099 25700 0237
Note SS sum of squares df degrees of freedom MS mean square Sig significance C control I impact B before A after
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waterbird species richness of Dianchi was higher than that ofany of the Ramsar sites (Table 4) Furthermore in recentyears Dianchi has supported 3 species consideredendangered according to the International Union forConservation of Nature (Appendix S1 Supplemental materialhttpsdoiorg101659MRD-JOURNAL-D-19-000551S1)According to the Ramsar Convention Manual lsquolsquoA wetlandshould be considered internationally important if itregularly supports 20000 or more waterbirdsrsquorsquo (RamsarConvention Secretariat 2013) Dianchi has recently met this
criterion every year (see Wang et al 2016 Wang and Yang2020) Therefore we suggest that monitoring and protectionfor Dianchi should be strengthened in the future
Wetland park construction needs to consider the habitat
requirements of waterbirds
The zones adjacent to mountainous lakes on the YGP arenarrow and disturbed by human activities (such as grazingand tourism) Our study found that the lakeside zone around
FIGURE 6 Differences in species richness (A) and H0e (B) before and after the
construction of 2 wetland parks at Lake Dianchi The control represented the
entire lakeside wetlands of Lake Dianchi impact 1 represented the Wangguan
wetland Park (S5) and impact 2 represented the Ancient Dian Kingdom wetland
park (S8)
FIGURE 7 Comparisons of species richness (A) and H0e (B) for different waterbird
guilds before and after the construction of 2 wetland parks at Lake Dianchi PODI
Podicipediformes CICO Ciconiiformes GRUI Gruiformes CHAR
Charadriiformes LARI Lariformes ANSE Anseriformes The H0e of
Podicipediformes and Lariformes were not compared because each had just 1
species P 005 P 001 P 0001
TABLE 3 Waterbird diversity differences before and after the wetland parks by paired t-test The H0e of Podicipediformes
and Lariformes were not tested because each had just 1 species Significant differences are marked in bold type
Order
Diversity
index Mean SD SE t df P
Podicipediformes SR 046 059 012 382 2300 0001
Ciconiiformes H0e 030 055 011 271 2300 0013
SR 158 228 047 340 2300 0002
Gruiformes H0e 002 027 005 030 2300 0767
SR 063 092 019 331 2300 0003
Charadriiformes H0e 062 107 022 286 2300 0009
SR 433 710 145 299 2300 0007
Lariformes SR 017 056 012 145 2300 0162
Anseriformes H0e 005 018 004 145 2300 0162
SR 017 064 013 128 2300 0213
Note df degrees of freedom SR species richness H0e ShannonndashWiener diversity index
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Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
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Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
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addition to obtain integrated information on thecomposition of the waterbird population of Dianchi inrecent years we obtained other waterbird distributioninformation from the literature and experiencedbirdwatchers
Statistical analysis
Species diversity estimation We used species accumulationcurves to assess our surveys and estimate species richness(Ugland et al 2003) We defined the cumulative number ofindividuals in a survey as the abundance of each species Inaddition we used the maximum abundance of each speciesto determine the population of waterbirds at Dianchi
Division of season and residence type According to thephenology and the seasonal classification method widelyused in China we set the seasons as spring (March to May)summer (June to August) autumn (September to November)and winter (December to February) We determined theresident types of waterbirds according to our continuousobservations and reference to The Avifauna of Yunnan ChinaVol I Non-Passeriformes (Yang et al 1995)
Ecological guilds classification Morphological form relates toecological function in birds (cf Ma et al 2010 Pigot et al2020) thus we divided the waterbirds into wading birds andswimming birds For the former we subdivided the birdsinto large shorebirds (herons storks godwits and others)which mainly rely on lakeside marshlands and smallshorebirds (sandpipers plovers and knots) which mainlyrely on mudflats We subdivided the latter into dabblingbirds (dabbling ducks and gulls) which mainly rely onshallow water and diving birds (diving ducks grebes andcormorants) which mainly rely on deep water
Changes in vegetation types We obtained satellite images ofthe 2 parks from Google Earth before and after wetlandconstruction and corrected habitat information (such asvegetation type) according to the field surveys We calculatedthe vegetation area of each patch before and afterconstruction in ArcGIS 93 (ESRI Inc) According to the typeof aquatic vegetation we classified each patch as high
emerging plant type (HE) high floating plant type (HF) lowemerging plant type (LE) low floating plant type (LF) mixedvegetation type (Mix) pond type (Pond) and mudflat type(Mudflat) (see Wang et al 2016) Changes in vegetation typemainly showed an increase in impervious surface and pondand a decrease in aquatic vegetation (Table 1 Figure 3)
Changes in waterbirds before and after the wetland parks Weused an asymmetric before-after-control-impact method toevaluate how wetland park construction affected waterbirds(Underwood 1994 Smith 2002) The species richness andShannonndashWiener diversity index (H0) of each plot (impact 1impact 2 and control) in a single survey were used asindicators of waterbird diversity In addition we used theaverage value of the aforementioned diversity to representlsquolsquobefore and after constructionrsquorsquo of impact 1 impact 2 andcontrol We used a general linear model to test differences inspecies diversity before and after wetland park constructionsusing IBM SPSS Statistics software (version 23) H0 andspecies richness were respectively used as dependentvariables survey sites (controlimpact CI) and the period(beforeafter BA) were used as fixed factors and survey yearswere used as random factors
We verified that the diversity and variance of eachguildmdashexcept for the H0 of Podicipediformes andLariformesmdashwere normally distributed and we used apaired t-test based on the monthly survey(s) to evaluatechanges in the diversity of each guild before and afterwetland park construction
Results
Species composition
We detected 67385 individuals belonging to 7 orders 15families and 99 species in all surveys from February 2013 toMay 2017 The species cumulation (rarefaction) curveshowed that our survey represented the waterbirdcomposition (Figure 4) The total number of species atDianchi was 105 including 6 species from recent referencesor birdwatchers Anser anser (greylag goose) (Xinhuanet 2017)Porzana cinerea (white-browed crake) (CBR 2020) Calidris
TABLE 1 Areas (ha) and their changing ratio () of different habitat types before and after the construction of 2 wetland parks at Lake Dianchi
Habitat type
S5 S8 Total
Be Af CR () Be Af CR () Be Af CA CR ()
HE 435 352 ndash196 959 000 ndash2393 1394 352 ndash1043 ndash1258
HF 935 000 ndash2184 230 1557 3313 1165 1557 392 473
LE 000 066 153 000 000 000 000 066 066 079
LF 1370 000 ndash3201 182 148 ndash087 1553 148 ndash1405 ndash1696
Mix 999 000 ndash2334 2059 000 ndash5141 3058 000 ndash3058 ndash3691
Mudflat 409 000 ndash955 000 000 000 409 000 ndash409 ndash494
Pond 132 2476 5476 576 1577 2499 708 4053 3345 4037
Total 4281 2893 ndash3242 4005 3281 ndash1809 8286 6174 ndash2112 ndash2549
Note S5 Wangguan wetland park S8 Ancient Dian Kingdom wetland park Be before wetland construction Af after wetland construction CR changing percentage
area () CA change area (ha) HE high emerging plant habitat HF high floating plant habitat LE low emerging plant habitat LF low floating plant habitat mix
mixed vegetation habitat mudflat mudflat habitat pond pond habitat
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melanotos (pectoral sandpiper) (Wang et al 2017) C alba(sanderling) (Wang et al 2017) Larus vegae (Vega gull) (Tu etal 2017) and L canus (mew gull) (Tu et al 2017) Three specieswere globally threatened (IUCN 2020) Aythya baeri (Baerrsquos
pochard) was listed as critically endangered Calidristenuirostris (great knot) was listed as endangered and Rissatridactyla (black-legged kittiwake) was listed as vulnerable(Appendix S1 Supplemental material httpsdoiorg101659MRD-JOURNAL-D-19-000551S1)
Ecological guilds and resident types
We found more wading species (69 species) than swimmingspecies (36 species) in all survey periods The formerincluded 33 large shorebirds and 36 small shorebirds andthe latter included 25 dabbling birds and 11 diving birdsShorebirds mainly comprised spring and autumn migrants(38 species) and resident birds (16 species) Swimming birdsmainly comprised winter visitors (29 species) (Figure 5A)The winter visitors which included more than 60000dabbling and large wading individuals were the dominantguilds at Dianchi These were followed by resident birdsmainly comprising large shorebirds (such as herons)Moreover more than 1000 migratory shorebirds usedDianchi as a stopover site (Figure 5B)
FIGURE 3 Changes in vegetation types before and after construction of 2 wetland parks Wangguan wetland park (A B) and Ancient Dian Kingdom wetland park (C D)
Habitat type HE high emerging plants type HF high floating plants type LE low emerging plants type LF low floating plants type Mix mixed vegetation type
Mudflat mudflat type Pond pond type
FIGURE 4 Rarefaction curves based on species and individuals of waterbirds
between February 2013 and May 2017 at Lake Dianchi China
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Impacts of wetland parks on waterbirds
The construction of wetland parks resulted in a significantdecrease in species richness and H0 (Table 2) For the controlplot the whole lakeside wetland held a mean (6 SD) of 20186 587 species and 1965 6 377 species before and after the
wetland parks were constructed respectively There were nosignificant differences (F frac14 013 P frac14 072) between the 2periods For the impact plots S5 held 579 6 547 speciesand 208 6 200 species before and after the construction ofthe wetland park respectively There were significantdifferences (F frac14 1085 P 001) between the 2 periods S8supported 400 6 221 species and 030 6 129 species beforeand after wetland park construction respectively Therewere significant differences (Ffrac14 8228 P 001) between the2 periods (Figure 6A) H0 showed the same patterns as speciesrichness (Figure 6B)
Except for the Lariformes and Anseriformes the speciesrichness of other guilds decreased significantly afterconstruction of the wetland parks Except for Gruiformesand Anseriformes the H0 of other guilds decreasedsignificantly after construction of the wetland parks(Figure 7 Table 3)
Discussion
High waterbird diversity needs adequate protection andmanagement
In this study we found more than 60000 individuals from105 waterbird species accounting for 4038 of the totalnumber of waterbirds in China (Wang et al 2018) Inparticular we found that the species richness of the migrantswas high Most of the species were small shorebirds whichrely strongly on mudflats and marshlands This findingsuggests that continuous monitoring throughout consecutivemonths and years is important to collect complete data onwaterbird population composition and propose timelymanagement measures
However only 4 wetlands (Dashanbao Napahai Bitahaiand Lashihai) on the YGP have been listed as internationallyimportant sites (Ramsar Convention Secretariat 2020) Usingthe data from our field surveys over the past decadeliterature and the website of BirdReport of China (httpwwwbirdreportcn) we analyzed the species composition ofDianchi and the 4 Ramsar wetlands We found that the
FIGURE 5 Species diversity of waterbirds in Lake Dianchi from March 2013 to
May 2017 Indicates the species richness (A) and abundance (B) of each
residence type in different ecological guilds
TABLE 2 Asymmetrical analysis of variance comparing waterbird diversity (species richness and H0e) before and after wetland park construction at 2 affected sites and
1 control site using a lsquolsquobeyond before-after-control-impactrsquorsquo design Significant differences are marked in bold type
Source
Species richness H0e
SS df MS F Sig SS df MS F Sig
CI Hypothesis 248947 100 248947 13199 000 979 100 979 5306 000
Error 26855 1424 18861 957 5191 0184
BA Hypothesis 12769 100 12769 758 009 429 100 429 952 008
Error 3942 234 16847 097 215 0451
Year Hypothesis 10452 200 5226 146 034 038 200 019 039 072
Error 14237 397 35845 095 198 0480
BA3CI Hypothesis 9670 100 9670 7360 000 598 100 598 6674 000
Error 31742 24160 1314 027 298 0090
BA3CI3year Hypothesis 009 200 004 000 100 016 200 008 033 072
Error 480229 25700 18686 6099 25700 0237
Note SS sum of squares df degrees of freedom MS mean square Sig significance C control I impact B before A after
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waterbird species richness of Dianchi was higher than that ofany of the Ramsar sites (Table 4) Furthermore in recentyears Dianchi has supported 3 species consideredendangered according to the International Union forConservation of Nature (Appendix S1 Supplemental materialhttpsdoiorg101659MRD-JOURNAL-D-19-000551S1)According to the Ramsar Convention Manual lsquolsquoA wetlandshould be considered internationally important if itregularly supports 20000 or more waterbirdsrsquorsquo (RamsarConvention Secretariat 2013) Dianchi has recently met this
criterion every year (see Wang et al 2016 Wang and Yang2020) Therefore we suggest that monitoring and protectionfor Dianchi should be strengthened in the future
Wetland park construction needs to consider the habitat
requirements of waterbirds
The zones adjacent to mountainous lakes on the YGP arenarrow and disturbed by human activities (such as grazingand tourism) Our study found that the lakeside zone around
FIGURE 6 Differences in species richness (A) and H0e (B) before and after the
construction of 2 wetland parks at Lake Dianchi The control represented the
entire lakeside wetlands of Lake Dianchi impact 1 represented the Wangguan
wetland Park (S5) and impact 2 represented the Ancient Dian Kingdom wetland
park (S8)
FIGURE 7 Comparisons of species richness (A) and H0e (B) for different waterbird
guilds before and after the construction of 2 wetland parks at Lake Dianchi PODI
Podicipediformes CICO Ciconiiformes GRUI Gruiformes CHAR
Charadriiformes LARI Lariformes ANSE Anseriformes The H0e of
Podicipediformes and Lariformes were not compared because each had just 1
species P 005 P 001 P 0001
TABLE 3 Waterbird diversity differences before and after the wetland parks by paired t-test The H0e of Podicipediformes
and Lariformes were not tested because each had just 1 species Significant differences are marked in bold type
Order
Diversity
index Mean SD SE t df P
Podicipediformes SR 046 059 012 382 2300 0001
Ciconiiformes H0e 030 055 011 271 2300 0013
SR 158 228 047 340 2300 0002
Gruiformes H0e 002 027 005 030 2300 0767
SR 063 092 019 331 2300 0003
Charadriiformes H0e 062 107 022 286 2300 0009
SR 433 710 145 299 2300 0007
Lariformes SR 017 056 012 145 2300 0162
Anseriformes H0e 005 018 004 145 2300 0162
SR 017 064 013 128 2300 0213
Note df degrees of freedom SR species richness H0e ShannonndashWiener diversity index
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Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
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Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
R37Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
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melanotos (pectoral sandpiper) (Wang et al 2017) C alba(sanderling) (Wang et al 2017) Larus vegae (Vega gull) (Tu etal 2017) and L canus (mew gull) (Tu et al 2017) Three specieswere globally threatened (IUCN 2020) Aythya baeri (Baerrsquos
pochard) was listed as critically endangered Calidristenuirostris (great knot) was listed as endangered and Rissatridactyla (black-legged kittiwake) was listed as vulnerable(Appendix S1 Supplemental material httpsdoiorg101659MRD-JOURNAL-D-19-000551S1)
Ecological guilds and resident types
We found more wading species (69 species) than swimmingspecies (36 species) in all survey periods The formerincluded 33 large shorebirds and 36 small shorebirds andthe latter included 25 dabbling birds and 11 diving birdsShorebirds mainly comprised spring and autumn migrants(38 species) and resident birds (16 species) Swimming birdsmainly comprised winter visitors (29 species) (Figure 5A)The winter visitors which included more than 60000dabbling and large wading individuals were the dominantguilds at Dianchi These were followed by resident birdsmainly comprising large shorebirds (such as herons)Moreover more than 1000 migratory shorebirds usedDianchi as a stopover site (Figure 5B)
FIGURE 3 Changes in vegetation types before and after construction of 2 wetland parks Wangguan wetland park (A B) and Ancient Dian Kingdom wetland park (C D)
Habitat type HE high emerging plants type HF high floating plants type LE low emerging plants type LF low floating plants type Mix mixed vegetation type
Mudflat mudflat type Pond pond type
FIGURE 4 Rarefaction curves based on species and individuals of waterbirds
between February 2013 and May 2017 at Lake Dianchi China
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Impacts of wetland parks on waterbirds
The construction of wetland parks resulted in a significantdecrease in species richness and H0 (Table 2) For the controlplot the whole lakeside wetland held a mean (6 SD) of 20186 587 species and 1965 6 377 species before and after the
wetland parks were constructed respectively There were nosignificant differences (F frac14 013 P frac14 072) between the 2periods For the impact plots S5 held 579 6 547 speciesand 208 6 200 species before and after the construction ofthe wetland park respectively There were significantdifferences (F frac14 1085 P 001) between the 2 periods S8supported 400 6 221 species and 030 6 129 species beforeand after wetland park construction respectively Therewere significant differences (Ffrac14 8228 P 001) between the2 periods (Figure 6A) H0 showed the same patterns as speciesrichness (Figure 6B)
Except for the Lariformes and Anseriformes the speciesrichness of other guilds decreased significantly afterconstruction of the wetland parks Except for Gruiformesand Anseriformes the H0 of other guilds decreasedsignificantly after construction of the wetland parks(Figure 7 Table 3)
Discussion
High waterbird diversity needs adequate protection andmanagement
In this study we found more than 60000 individuals from105 waterbird species accounting for 4038 of the totalnumber of waterbirds in China (Wang et al 2018) Inparticular we found that the species richness of the migrantswas high Most of the species were small shorebirds whichrely strongly on mudflats and marshlands This findingsuggests that continuous monitoring throughout consecutivemonths and years is important to collect complete data onwaterbird population composition and propose timelymanagement measures
However only 4 wetlands (Dashanbao Napahai Bitahaiand Lashihai) on the YGP have been listed as internationallyimportant sites (Ramsar Convention Secretariat 2020) Usingthe data from our field surveys over the past decadeliterature and the website of BirdReport of China (httpwwwbirdreportcn) we analyzed the species composition ofDianchi and the 4 Ramsar wetlands We found that the
FIGURE 5 Species diversity of waterbirds in Lake Dianchi from March 2013 to
May 2017 Indicates the species richness (A) and abundance (B) of each
residence type in different ecological guilds
TABLE 2 Asymmetrical analysis of variance comparing waterbird diversity (species richness and H0e) before and after wetland park construction at 2 affected sites and
1 control site using a lsquolsquobeyond before-after-control-impactrsquorsquo design Significant differences are marked in bold type
Source
Species richness H0e
SS df MS F Sig SS df MS F Sig
CI Hypothesis 248947 100 248947 13199 000 979 100 979 5306 000
Error 26855 1424 18861 957 5191 0184
BA Hypothesis 12769 100 12769 758 009 429 100 429 952 008
Error 3942 234 16847 097 215 0451
Year Hypothesis 10452 200 5226 146 034 038 200 019 039 072
Error 14237 397 35845 095 198 0480
BA3CI Hypothesis 9670 100 9670 7360 000 598 100 598 6674 000
Error 31742 24160 1314 027 298 0090
BA3CI3year Hypothesis 009 200 004 000 100 016 200 008 033 072
Error 480229 25700 18686 6099 25700 0237
Note SS sum of squares df degrees of freedom MS mean square Sig significance C control I impact B before A after
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waterbird species richness of Dianchi was higher than that ofany of the Ramsar sites (Table 4) Furthermore in recentyears Dianchi has supported 3 species consideredendangered according to the International Union forConservation of Nature (Appendix S1 Supplemental materialhttpsdoiorg101659MRD-JOURNAL-D-19-000551S1)According to the Ramsar Convention Manual lsquolsquoA wetlandshould be considered internationally important if itregularly supports 20000 or more waterbirdsrsquorsquo (RamsarConvention Secretariat 2013) Dianchi has recently met this
criterion every year (see Wang et al 2016 Wang and Yang2020) Therefore we suggest that monitoring and protectionfor Dianchi should be strengthened in the future
Wetland park construction needs to consider the habitat
requirements of waterbirds
The zones adjacent to mountainous lakes on the YGP arenarrow and disturbed by human activities (such as grazingand tourism) Our study found that the lakeside zone around
FIGURE 6 Differences in species richness (A) and H0e (B) before and after the
construction of 2 wetland parks at Lake Dianchi The control represented the
entire lakeside wetlands of Lake Dianchi impact 1 represented the Wangguan
wetland Park (S5) and impact 2 represented the Ancient Dian Kingdom wetland
park (S8)
FIGURE 7 Comparisons of species richness (A) and H0e (B) for different waterbird
guilds before and after the construction of 2 wetland parks at Lake Dianchi PODI
Podicipediformes CICO Ciconiiformes GRUI Gruiformes CHAR
Charadriiformes LARI Lariformes ANSE Anseriformes The H0e of
Podicipediformes and Lariformes were not compared because each had just 1
species P 005 P 001 P 0001
TABLE 3 Waterbird diversity differences before and after the wetland parks by paired t-test The H0e of Podicipediformes
and Lariformes were not tested because each had just 1 species Significant differences are marked in bold type
Order
Diversity
index Mean SD SE t df P
Podicipediformes SR 046 059 012 382 2300 0001
Ciconiiformes H0e 030 055 011 271 2300 0013
SR 158 228 047 340 2300 0002
Gruiformes H0e 002 027 005 030 2300 0767
SR 063 092 019 331 2300 0003
Charadriiformes H0e 062 107 022 286 2300 0009
SR 433 710 145 299 2300 0007
Lariformes SR 017 056 012 145 2300 0162
Anseriformes H0e 005 018 004 145 2300 0162
SR 017 064 013 128 2300 0213
Note df degrees of freedom SR species richness H0e ShannonndashWiener diversity index
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Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
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Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
R37Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Impacts of wetland parks on waterbirds
The construction of wetland parks resulted in a significantdecrease in species richness and H0 (Table 2) For the controlplot the whole lakeside wetland held a mean (6 SD) of 20186 587 species and 1965 6 377 species before and after the
wetland parks were constructed respectively There were nosignificant differences (F frac14 013 P frac14 072) between the 2periods For the impact plots S5 held 579 6 547 speciesand 208 6 200 species before and after the construction ofthe wetland park respectively There were significantdifferences (F frac14 1085 P 001) between the 2 periods S8supported 400 6 221 species and 030 6 129 species beforeand after wetland park construction respectively Therewere significant differences (Ffrac14 8228 P 001) between the2 periods (Figure 6A) H0 showed the same patterns as speciesrichness (Figure 6B)
Except for the Lariformes and Anseriformes the speciesrichness of other guilds decreased significantly afterconstruction of the wetland parks Except for Gruiformesand Anseriformes the H0 of other guilds decreasedsignificantly after construction of the wetland parks(Figure 7 Table 3)
Discussion
High waterbird diversity needs adequate protection andmanagement
In this study we found more than 60000 individuals from105 waterbird species accounting for 4038 of the totalnumber of waterbirds in China (Wang et al 2018) Inparticular we found that the species richness of the migrantswas high Most of the species were small shorebirds whichrely strongly on mudflats and marshlands This findingsuggests that continuous monitoring throughout consecutivemonths and years is important to collect complete data onwaterbird population composition and propose timelymanagement measures
However only 4 wetlands (Dashanbao Napahai Bitahaiand Lashihai) on the YGP have been listed as internationallyimportant sites (Ramsar Convention Secretariat 2020) Usingthe data from our field surveys over the past decadeliterature and the website of BirdReport of China (httpwwwbirdreportcn) we analyzed the species composition ofDianchi and the 4 Ramsar wetlands We found that the
FIGURE 5 Species diversity of waterbirds in Lake Dianchi from March 2013 to
May 2017 Indicates the species richness (A) and abundance (B) of each
residence type in different ecological guilds
TABLE 2 Asymmetrical analysis of variance comparing waterbird diversity (species richness and H0e) before and after wetland park construction at 2 affected sites and
1 control site using a lsquolsquobeyond before-after-control-impactrsquorsquo design Significant differences are marked in bold type
Source
Species richness H0e
SS df MS F Sig SS df MS F Sig
CI Hypothesis 248947 100 248947 13199 000 979 100 979 5306 000
Error 26855 1424 18861 957 5191 0184
BA Hypothesis 12769 100 12769 758 009 429 100 429 952 008
Error 3942 234 16847 097 215 0451
Year Hypothesis 10452 200 5226 146 034 038 200 019 039 072
Error 14237 397 35845 095 198 0480
BA3CI Hypothesis 9670 100 9670 7360 000 598 100 598 6674 000
Error 31742 24160 1314 027 298 0090
BA3CI3year Hypothesis 009 200 004 000 100 016 200 008 033 072
Error 480229 25700 18686 6099 25700 0237
Note SS sum of squares df degrees of freedom MS mean square Sig significance C control I impact B before A after
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MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
waterbird species richness of Dianchi was higher than that ofany of the Ramsar sites (Table 4) Furthermore in recentyears Dianchi has supported 3 species consideredendangered according to the International Union forConservation of Nature (Appendix S1 Supplemental materialhttpsdoiorg101659MRD-JOURNAL-D-19-000551S1)According to the Ramsar Convention Manual lsquolsquoA wetlandshould be considered internationally important if itregularly supports 20000 or more waterbirdsrsquorsquo (RamsarConvention Secretariat 2013) Dianchi has recently met this
criterion every year (see Wang et al 2016 Wang and Yang2020) Therefore we suggest that monitoring and protectionfor Dianchi should be strengthened in the future
Wetland park construction needs to consider the habitat
requirements of waterbirds
The zones adjacent to mountainous lakes on the YGP arenarrow and disturbed by human activities (such as grazingand tourism) Our study found that the lakeside zone around
FIGURE 6 Differences in species richness (A) and H0e (B) before and after the
construction of 2 wetland parks at Lake Dianchi The control represented the
entire lakeside wetlands of Lake Dianchi impact 1 represented the Wangguan
wetland Park (S5) and impact 2 represented the Ancient Dian Kingdom wetland
park (S8)
FIGURE 7 Comparisons of species richness (A) and H0e (B) for different waterbird
guilds before and after the construction of 2 wetland parks at Lake Dianchi PODI
Podicipediformes CICO Ciconiiformes GRUI Gruiformes CHAR
Charadriiformes LARI Lariformes ANSE Anseriformes The H0e of
Podicipediformes and Lariformes were not compared because each had just 1
species P 005 P 001 P 0001
TABLE 3 Waterbird diversity differences before and after the wetland parks by paired t-test The H0e of Podicipediformes
and Lariformes were not tested because each had just 1 species Significant differences are marked in bold type
Order
Diversity
index Mean SD SE t df P
Podicipediformes SR 046 059 012 382 2300 0001
Ciconiiformes H0e 030 055 011 271 2300 0013
SR 158 228 047 340 2300 0002
Gruiformes H0e 002 027 005 030 2300 0767
SR 063 092 019 331 2300 0003
Charadriiformes H0e 062 107 022 286 2300 0009
SR 433 710 145 299 2300 0007
Lariformes SR 017 056 012 145 2300 0162
Anseriformes H0e 005 018 004 145 2300 0162
SR 017 064 013 128 2300 0213
Note df degrees of freedom SR species richness H0e ShannonndashWiener diversity index
R35Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
R36Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
R37Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
waterbird species richness of Dianchi was higher than that ofany of the Ramsar sites (Table 4) Furthermore in recentyears Dianchi has supported 3 species consideredendangered according to the International Union forConservation of Nature (Appendix S1 Supplemental materialhttpsdoiorg101659MRD-JOURNAL-D-19-000551S1)According to the Ramsar Convention Manual lsquolsquoA wetlandshould be considered internationally important if itregularly supports 20000 or more waterbirdsrsquorsquo (RamsarConvention Secretariat 2013) Dianchi has recently met this
criterion every year (see Wang et al 2016 Wang and Yang2020) Therefore we suggest that monitoring and protectionfor Dianchi should be strengthened in the future
Wetland park construction needs to consider the habitat
requirements of waterbirds
The zones adjacent to mountainous lakes on the YGP arenarrow and disturbed by human activities (such as grazingand tourism) Our study found that the lakeside zone around
FIGURE 6 Differences in species richness (A) and H0e (B) before and after the
construction of 2 wetland parks at Lake Dianchi The control represented the
entire lakeside wetlands of Lake Dianchi impact 1 represented the Wangguan
wetland Park (S5) and impact 2 represented the Ancient Dian Kingdom wetland
park (S8)
FIGURE 7 Comparisons of species richness (A) and H0e (B) for different waterbird
guilds before and after the construction of 2 wetland parks at Lake Dianchi PODI
Podicipediformes CICO Ciconiiformes GRUI Gruiformes CHAR
Charadriiformes LARI Lariformes ANSE Anseriformes The H0e of
Podicipediformes and Lariformes were not compared because each had just 1
species P 005 P 001 P 0001
TABLE 3 Waterbird diversity differences before and after the wetland parks by paired t-test The H0e of Podicipediformes
and Lariformes were not tested because each had just 1 species Significant differences are marked in bold type
Order
Diversity
index Mean SD SE t df P
Podicipediformes SR 046 059 012 382 2300 0001
Ciconiiformes H0e 030 055 011 271 2300 0013
SR 158 228 047 340 2300 0002
Gruiformes H0e 002 027 005 030 2300 0767
SR 063 092 019 331 2300 0003
Charadriiformes H0e 062 107 022 286 2300 0009
SR 433 710 145 299 2300 0007
Lariformes SR 017 056 012 145 2300 0162
Anseriformes H0e 005 018 004 145 2300 0162
SR 017 064 013 128 2300 0213
Note df degrees of freedom SR species richness H0e ShannonndashWiener diversity index
R35Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
R36Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
R37Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Dianchi provided important habitats for many shorebirdsTherefore monitoring (including multiyear and full-monthmonitoring) and management of the lakeside zone ofDianchi and other lakes in the YGP should be strengthened
Furthermore we found that the construction of wetlandparks at the lakeside in Dianchi significantly reduced thediversity of waterbirds This was mainly related to changes inaquatic vegetation because vegetation is one of the mostimportant factors affecting the distribution of waterbirds(Ma et al 2010) Our previous research found that the lowemerging plants mixed vegetation and mudflat habitatsheld high species diversity while low floating plants andpond habitats had low species diversity (Wang et al 2016)The construction of wetland parks resulted in the conversionof aquatic vegetation to pond habitats and the loss ofmudflat and mixed vegetation habitats Therefore mostshorebirds have dramatically decreased in number and theirdiversity has also decreased
Although ecotourism may increase employment andincome from tourism it can also create some negativeecological impacts For example ecotourism in wetlands inSri Lanka has increased human disturbance and decreasedbiodiversity (Fernando and Shariff 2013) Most waterbirdsavoid potential threats from humans (Dear et al 2015 Kumaret al 2016) Therefore the decrease in waterbird diversityafter the construction of wetland parks in Dianchi might alsobe related to human disturbance In addition park roads(visitor corridors) fragmented the habitats of somewaterbirds and reduced diversity (Sarkar et al 2014) Wetlandparks (including area size and vegetation configuration)should therefore be designed to cater adequately for humansand wildlife This will be an essential task for ecologists andmanagers
Conclusions
We conducted an intensive investigation of Dianchi thelargest wetland on the YGP It showed that Dianchi was animportant wintering place for waterbirds and a breeding andstopover place for other seasonal waterbirds The resultssuggest that the monitoring of waterbirds should beincreased in all seasons especially during migration inspring and autumn The current oxidation pond style ofwetland parks aimed at water purification and tourism is notsuited to most waterbirds We suggest that designs forartificial wetlands or wetland parks at Dianchi and otherwetlands on the YGP should consider the habitatrequirements of different waterbirds in different seasons
and focus on the protection of mudflats which small wadingbirds require
A C K N O W L E D G M E N T S
This work was funded by Kunming Dianchi and Plateau Lakes Institute theSecond Terrestrial Wild Animal Resources Investigation of Yunnan ProvinceChina and the Doctoral Science Foundation of Dali University (KYBS201701)
R E F E R E N C E S
Amano T Szekely T Sandel B Nagy S Mundkur T Langendoen T Blanco DSoykan CU Sutherland WJ 2018 Successful conservation of global waterbirdpopulations depends on effective governance Nature 553(7687)199ndash202httpsdoiorg101038nature25139Bibby CJ Burguess ND Hill DA Mustoe S 2000 Bird Census Techniques 2ndedition (1st edition 1992) London United Kingdom Academic PressCao L Barter M Zhao M Meng H Zhang Y 2011 A systematic scheme formonitoring waterbird populations at Shengjin Lake China Methodology andpreliminary results Chinese Birds 2(1)1ndash17 httpwwwchinesebirdsnetENabstractabstract61shtmlCBD [Convention on Biological Diversity] 2010 Biodiversity 2011ndash2020 and theAichi biodiversity targets COP 10 Decision X2 Montreal Canada CBD httpswwwcbdintdecisioncopidfrac1412268 accessed on 15 August 2019CBR [China Bird Report] 2020 Bird Report [in Chinese] Kunming China CBRhttpwwwbirdreportcn accessed on 6 July 2020Cui P Wu Y Ding H Wu J Cao M Chen L Chen B Lu X Xu H 2014 Status ofwintering waterbirds at selected locations in China Waterbirds 37(4)402ndash409httpsdoiorg1016750630370407Dear EJ Guay PJ Robinson RW Weston MA 2015 Distance from shorepositively influences alert distance in three wetland bird species WetlandsEcology and Management 23(2)315ndash318 httpsdoiorg101007s11273-014-9376-0Fernando SLJ Shariff NM 2013 Wetland ecotourism in Sri Lanka Issues andchallenges Malaysian Journal of Society and Space 9(4)99ndash105 httpsejournalukmmygmjssarticleview18263Han L Luo X Huang SL 2010 Birds In Zhou W Chen BK editors Yunnan BitahaiNature Reserve [in Chinese] Kunming China Yunnan Science and TechnologyPress pp 207ndash225Han LX Peng JS 2012 The Birds of Napahai Wetland Shangri-La Yunnan China [inChinese] Beijing China Encyclopedia of China Publishing HouseIUCN [International Union for Conservation of Nature] 2020 The IUCN Red List ofThreatened Species Version 2020-2 Gland Switzerland IUCN httpswwwiucnredlistorg accessed on 26 August 2020Jin XC 2003 Analysis of eutrophication state and trend for lakes in China Journalof Limnology 62(s1)60ndash66 httpsdoiorg104081jlimnol2003s160Jin XC Wang L He LP 2006 Lake Dianchi Experience and lessons learned briefIn ILEC [International Lake Environment Committee] editor LBMI Experience ampLessons Learned Briefs Kusatsu Japan ILEC pp 159ndash178 httpsiwlearnnetdocuments6005 accessed on 16 March 2021Keuroorner C Jetz W Paulsen J Payne D Rudmann-Maurer K Spehn EM 2016 Aglobal inventory of mountains for bio-geographical applications Alpine Botany127(1)1ndash15 httpsdoiorg101007s00035-016-0182-6Kumar P Rai D Gupta SK 2016 Wetland bird assemblage in rural ponds ofKurukshetra India Waterbirds 39(1)86ndash98 httpsdoiorg1016750630390111Kunming Dianchi Administration Bureau 2018 Regulations on the Protection ofDianchi Lake in Yunnan Province Kunming Japan Kunming Dianchi AdministrationBureau httpdgjkmgovcnc2018-12-072844346shtml accessed on 26August 2020Li LX Yang GJ 2015 Analysis and investigation on wintering waterfowl ofYunnan Lugu Lake [in Chinese with English abstract] Forest Inventory andPlanning 40(2)74ndash78 httpsdoiorg103969jissn1671-3168201502017
TABLE 4 Waterbird species richness at Lake Dianchi and 4 Ramsar wetlands on the YunnanndashGuizhou Plateau
Wetland
Species
richness
Number of
threatened
species Abundance Data source
Dianchi 105 3 67385 This study
Bitahai 40 1 186 Our field survey Han et al (2010) CBR (2020)
Dashanbao 54 2 5665 Our field survey CBR (2020)
Lashihai 68 3 14649 Our field survey Quan et al (2002) Liu (2004) Liao et al (2017) CBR (2020)
Napahai 77 4 4153 Our field survey Han and Peng (2012) CBR (2020)
R36Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
R37Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use
Liao JT Yue H Huang TF Peng GH 2017 Seasonal waterbird population changesin Lashihai Lake in northwest Yunnan China Journal of Mountain Science14(9)1852ndash1862 httpsdoiorg101007s11629-016-4164-3Liu N 2004 New records of birds in Yunnan province Anser erythropus [inChinese] Zoological Research 25(3)204 httpwwwzooresaccnenarticleid1469Liu W Li S Bu H Zhang Q Liu G 2012 Eutrophication in the Yunnan Plateaulakes the influence of lake morphology watershed land use and socioeconomicfactors Environmental Science and Pollution Research 19(3)858ndash870 httpsdoiorg101007s11356-011-0616-zLiu W Qiu R 2007 Water eutrophication in China and the combating strategiesJournal of Chemical Technology and Biotechnology 82(9)781ndash786 httpsdoiorg101002jctb1755Luo Y Yang K Yu Z Chen J Xu Y Zhou X Yang Y 2017 Dynamic monitoring andprediction of Dianchi Lake cyanobacteria outbreaks in the context of rapidurbanization Environmental Science and Pollution Research 24(6)5335ndash5348httpsdoiorg101007s11356-016-8155-2Ma RH Yang GS Duan HT Jiang JH Wang SM Feng XZ Li AN Kong FX Xue BWu JL et al 2011 Chinarsquos lakes at present Number area and spatialdistribution Science China Earth Sciences 54(2)283ndash289 httpsdoiorg101007s11430-010-4052-6Ma Z Cai Y Li B Chen J 2010 Managing wetland habitats for waterbirds Aninternational perspective Wetlands 30(1)15ndash27 httpsdoiorg101007s13157-009-0001-6Pigot A Sheard C Miller ET Bregman TP Freeman BG Roll U Seddon N TrisosCH Weeks BC Tobias A 2020 Macroevolutionary convergence connectsmorphological form to ecological function in birds Nature Ecology amp Evolution4230ndash239 httpsdoiorg101038s41559-019-1070-4Quan RC Wen X Yang X 2002 Numbers of migratory waterbirds at LakeLashihai China Waterbirds 25(2)239ndash243 httpsdoiorg1016751524-4695(2002)025[0239NOMWAL]20CO2Ramsar Convention Secretariat 2013 The Ramsar Convention Manual A guide tothe Convention on Wetlands 6th edition (1st edition 1971) Gland SwitzerlandRamsar Convention Secretariat pp 52ndash53 httpswwwramsarorgdocumentthe-ramsar-convention-manual-6th-edition accessed on 16 March 2021Ramsar Convention Secretariat 2020 The List of Wetlands of InternationalImportance Gland Switzerland Ramsar Convention Secretariat httpswwwramsarorgaboutwetlands-of-international-importance-ramsar-sites accessedon 27 July 2020Sarkar B Hazra P Kumar SP Ghosh P Banerjee A Khan TN 2014 Habitatattributes and waterbird-use of four wetlands in Manas National Park AssamIndia Proceedings of the Zoological Society 67(2)94ndash107 httpsdoiorg101007s12595-013-0074-3Smith EP 2002 BACI design In El-Shaaraw AH Piegorsch WW editorsEncyclopedia of Environmetrics Chichester United Kingdom Wiley pp 141ndash148httpsdoiorg1010029780470057339vab001pub2Tu W Yang Q Liu B Xiao J Jin Z Wen M 2017 Synchronous survey of thewintering waterfowl in Dianchi Lake [in Chinese with English abstract] ForestInventory and Planning 42(6)52ndash57 httpsdoiorg103969jissn1671-3168201706011Ugland KI Gray JS Ellingsen KE 2003 The speciesndashaccumulation curve andestimation of species richness Journal of Animal Ecology 72(5)888ndash897httpsdoiorg101046j1365-2656200300748x
Underwood AJ 1994 On beyond BACI Sampling designs that might reliablydetect environmental disturbances Ecological Applications 4(1)3ndash15 httpsdoiorg1023071942110Wang R Wu F Chang Y Yang X 2016 Waterbirds and their habitat utilization ofartificial wetlands at Dianchi lake Implication for waterbird conservation inYunnanndashGuizhou Plateau lakes Wetlands 36(6)1087ndash1095 httpsdoiorg101007s13157-016-0823-yWang RX Yang XJ 2020 Seasonal pattern of waterbird communities at LakeDianchi YunnanGuizhou Plateau south-west China Forktail 3697ndash105httpswwworientalbirdcluborgforktail-36Wang SM Dou HS editors 1998 Lakes of China [in Chinese] Beijing ChinaScience PressWang X Kuang F Tan K Ma Z 2018 Population trends threats andconservation recommendations for waterbirds in China Avian Research 914httpsdoiorg101186s40657-018-0106-9Wang ZB Bai HT Zhao XB 2017 New records of birds in Yunnan provinceCalidris melanotos and Calidris alba [in Chinese] Sichuan Journal of Zoology36(3)284 httpwwwscdwzzcomnewsviewaspxnewsidfrac142349amptypefrac143Wu P Shen H Cai N Zeng C Wu Y Wang B Wang Y 2016 Spatiotemporalanalysis of water area annual variations using a Landsat time series A case studyof nine plateau lakes in Yunnan province China International Journal of RemoteSensing 37(24)5826ndash5842 httpsdoiorg1010800143116120161251630Xinhuanet 2017 Kunming Greylag geese are seen on Lake Dianchi [in Chinese]Xinhuanet httpmxinhuanetcomyn2017-1126c_136779875htmaccessed on 26 May 2021Yang L Li H Yang XJ 2010 Wetlands of Yunnan [in Chinese] Beijing ChinaChina Forestry Publishing HouseYang L Wen XJ Han LX Yang XJ Shi WY Wang SZ 1995 The Avifauna of YunnanChina Vol I Non-Passeriformes [in Chinese] Kunming China Yunnan Science andTechnology PressYang W Liu Q Tian K 2020 Community characteristics and population dynamicsof winter waterbirds in Jianhu Lake Yunnan China [in Chinese with Englishabstract] Chinese Journal of Wildlife 41(1)92ndash99 httpsdoiorg1019711jcnkiissn2310-1490202001014Yang WJ Liu Q He X Li YQ 2020 Characteristics of winter waterbirdscommunity of lakes in central Yunnan China [in Chinese with English abstract]Chinese Journal of Ecology 39(6)1858ndash1864 httpsdoiorg1013292j1000-4890202006035Zhao Q Boomer GS Royle JA 2019 Integrated modeling predicts shifts inwaterbird population dynamics under climate change Ecography 42(9)1470ndash1481 httpsdoiorg101111ecog04548
Supplemental material
APPENDIX S1 Checklist of waterbirds
Found at httpsdoiorg101659MRD-JOURNAL-D-19-000551S1
R37Mountain Research and Development httpsdoiorg101659MRD-JOURNAL-D-19-000551
MountainResearch
Downloaded From httpsbiooneorgjournalsMountain-Research-and-Development on 21 Apr 2022Terms of Use httpsbiooneorgterms-of-use