Multiple components of environmental change drive populations of breeding waders in seminatural grasslands

Ecology and Evolution. 2018;8:10489–10496.   | 10489 www.ecolevol.org Received:14April2017 | Revised:24February2018 | Accepted:24March2018 DOI: 10.1002/ece3.4514 ORIGINAL RESEARCH Multiple components of environmental change drive populations of breeding waders in seminatural grasslands Karsten Laursen1 | Javier Balbontín2 | Ole Thorup3 | Henrik Haaning Nielsen4 | Tommy Asferg1 | Anders Pape Møller5 ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium, providedtheoriginalworkisproperlycited. ©2018TheAuthors.Ecology and EvolutionpublishedbyJohnWiley&SonsLtd. 1DepartmentofBioscience,Aarhus University,Rønde,Denmark 2DepartamentodeZoología,Facultadde Biología,Sevilla,Spain 3AmphiConsult,Ribe,Denmark 4AvifaunaConsult,Vesløs,Denmark 5EcologieSystématiqueEvolution, CNRS,UniversitéParis-Sud,AgroParisTech, UniversitéParis-Saclay,Orsay,France Correspondence KarstenLaursen,InstituteofBioscience, AarhusUniversity,Rønde,Denmark. Email:[email protected] Funding information AageV.JensenNaturfond Abstract Environmentsarerapidlychangingduetoclimatechange,landuse,intensiveagriculture,andtheimpactofhuntingonpredatorpopulations.Here,weanalyzedlong- termdatarecordedduring1928–2014onthesizeofbreedingpopulationsofwaders attwolargenaturereservesinDenmark,VejlerneandTipperne,todeterminethe effectsofcomponentsofenvironmentalchangeonbreedingpopulationsofwaders. Environmentalvariablesandcountsofwadersweretemporallyautocorrelated,and weusedgeneralizedleastsquare(GLS)byincorporatingthefirst-orderautoregressivecorrelationstructureintheanalyses.Weattemptedtopredicttheabundanceof wadersforshort-termtrendsfortwonaturereserves(35years)andforlong-term trendsforonenaturereserve(86years),usingprecipitation,temperature,nutrients, abundanceoffoxesVulpes vulpes,areagrazed,andnumberofcattle.Therewasevidenceofimpactsofnutrients,climate(long-termchangesintemperatureandprecipitation),grazing,mowing,andpredationonbirdpopulations.Weusedstandard randomeffectsmeta-analysesweightedby(N–3)toquantifythesemeaneffects. Therewasnosignificantdifferenceineffectsizeamongspecies,whilemeaneffect sizedifferedconsistentlyamongenvironmentalfactors,andtheinteractionbetween effectsizeforspeciesandenvironmentalfactorswasalsosignificant.Thus,environmentalfactorsaffectedthedifferentspeciesdifferently.Meaneffectsizewasthe largestat+0.20forrain,+0.11fortemperature,−0.09forfoxabundance,and−0.03 fornumberofcattle,whiletherewasnosignificantmeaneffectforfertilizer,area grazed, and year. Effect sizes for two short-term time series from Tipperne and Vejlernewerepositivelycorrelatedaswereeffectsizesforshort-termandlong-term timeseriesatTipperne.Thisimpliesthatenvironmentalfactorshadconsistenteffectsacrosslargetemporalandspatialscales. KEYWORDS climatechange,environmentalchange,fertilizer,landuse,long-termstudies,nutrients, precipitation,studymethods,temperature 10490 | LAURSEN Et AL. 1 | INTRODUCTION Breeding populations of waders are declining across western Europe(Thorup,2006;Roodbergen,vanderWert,&Hötker,2012; Robinson,Morrison,&Baillie,2014).Thereasonsforthesedeclines includeintensifiedagriculturalpractice,reclamationofcoastalhabitats,increasingpredationpressure,humandisturbance,andclimate change (Beintema & Müskens, 1987; Wilson, Ausden, & Milsom, 2004;Smart,Gill,Sutherland,&Watkinson,2006;Holm&Laursen, 2009;Roodbergenetal.,2012;Stephensetal.,2016).Demographic studiesshowthatthedeclinesaremainlycausedbypoorchicksurvivalratherthanadultsurvival(Roodbergen,Klok,&Schekkerman, 2008; Roodbergen etal., 2012). Low breeding success is caused bylossesofneststopredationandflooding(Hötker&Segebade, 2000;VandePoletal.,2010;Bellebaum&Bock,2009;Thorup& Koffijberg,2016).Studiesofwaderpopulationsduringrecentyears havefocusedonfarmlandrevealingcomplexinteractionsbetween agricultural practice and climate, affecting the survival of young (Kleijn etal., 2010; Schroeder etal., 2012). Young waders have tofindtheirownfood,andduetohighenergyrequirementsand poorabilitiestosaveenergy,theyoperatewithinnarrowenergetic margins, for example, a balance between quantity and quality of food (Schekkerman &Visser,2001;Maier,2013).Tothisarrayof parametersinfluencing waderpopulations,weincludedchange in nutrient load in the environment as a proxy for primary productivityandamountofbenthosandthusindirectlycarryingcapacity forbreedingbirds(Philippartetal.,2007;Møller,Flensted-Jensen, Laursen,&Mardal,2015).Thus,nutrientloadcanbeanimportant parameter,althoughastraightforwardrelationshipbetweennutrientsandamountofinvertebratefoodforyoungcannotbeexpected (Schekkerman & Beintema, 2007). Outside the breeding season duringmigrationandatwinteringsites,severalwaderspeciesstage and forage in marine estuaries and along coasts that are influencedbynutrients(Vitousek,Mooney,Lubchenko,&Melillo,1997; Windolf,Blicher-Mathiesen,Carstensen,&Krovang,2012). Different components of environmental change such as climatechange,landuse,andfisheriesarecurrentlybeingdescribed asdeterminantsofpoorreproductiveperformance,reducedsurvivorship,anddecliningpopulationtrendsforwadersandotherbird populations (Frederiksen, Wanless, Harries, Rothery, & Wilson, 2004; Schroeder etal.,2012;Maier,2013).However, fewstudies havedemonstratedforclimatechangethatdemographicvariables determine population size (Dunn & Møller, 2014; Robinson etal., 2014;Stephensetal.,2016).Attemptstomakeintegratedanalyses oftherelativecontributionsofmultiplefactorsaccountingforsuch trendsarescarce.Anumberofstudieshaverecentlyinvestigated theeffectsofclimatechangeandlanduseonpopulationsize(Møller, Flensted-Jensen,&Mardal,2007;Pimm,2009;Eglington&Pearce- Higgins,2012;Mantyka-Pringle,Martin,&Rhodes,2012;Jørgensen etal.,2015;Martin,vanDyck,Dendoncker,&Titeux,2013;Møller& Laursen,2015).Thisleavesanumberofadditionalfactorsinneedof study,includingpopulationchangesandeffectsofindustrializedagriculturewithhighlevelsoffertilizeruse.Sincesuchanalysesquickly includemanypredictors,theyareresourcedemandingandonlyfeasiblewhenbasedonlong-termstudies.Unfortunately,mosttimeseriesinecologicalresearchareshortandonlyrarelyexceed50years, therebyoftenpreventinginclusionofallorevenmostcrucialpredictorsandcertainlynotinclusionofinteractionsamongvariables. Theaimsofthisstudywere(a)toquantifytheeffectsizeforthe impactofenvironmentalconditionsonthepopulationsizeofseven waderspecies;(b)toanalyzetheeffectsofclimate,nutrients,land use,andpredatorabundanceonsizeoflocalbreedingpopulations ina86-yeartimeseriesofwaderbirdcommunitiesatTipperneand twoshort-termtimeseriesof35yearsatTipperneandVejlerne;(c) totestforconsistencyineffectsizebetweenoneshort-termand onelong-termtimeseriesatTipperneandforoneshort-termtime seriesofeffectsizesatTipperneandoneshort-termtimeseriesat Vejlerne.Wedidsobyanalyzingthebreedingabundanceofseven wader species during1928–2014 atthenaturereserveTipperne, Denmark, and during 1978–2014 at the nature reserve Vejlerne, Denmark. 2 | METHODS 2.1 | Sites, wader species, and study periods We studied breeding waders at two seminatural grassland sites (TipperneandVejlerne)inwesternDenmarkextensivelyfarmed,for example,grazedbycattleatlowdensity,latemowing,andwithout directuseoffertilizer(seesitedescriptioninSupportinginformation AppendixS1).Wefocusedonthewaderbirdcommunitycomposed of seven species: Oystercatcher Haematopus ostralegus, lapwing Vanellus vanellus,black-tailedgodwitLimosa limosa,redshankTringa totanus, dunlin Calidris alpina, ruff Philomachus pugnax, and avocet Recurvirostra avocetta. Data on bird numbers are available at Tipperneduring1928–2014andatVejlerne1978–2014,exceptfor 2004andforoystercatcherduring2004–2014(seeFig.1).Theyare allmigratorybirdswiththeearlybreedingspeciesarrivinginMarch (oystercatcher,lapwing),whiletheotherspeciesarriveinApril.The twostudyareasareNATURA-2000sitesthatarestrongholdsfor breedingwadersinDenmark(Thorup,2004). 2.2 | Census methods CensusmethodsaredescribedbyMøller(1983),Thorup(1998),and Kjeldsen(2008).Theyhavebeenadjustedduringthestudyperiod duetochangeinvegetationheight.AtTipperneduring1928–1957, nestsweresearchedintensively.During1958–1964,nestsearches weresupplementedbymappingbirdsgivingalarmcallstoidentify territories. In 1965–1985, breeding birds giving alarm calls were mapped together with nests. From 1986, breeding waders were mappedfromadistancewithatelescope(60×magnification)supplementedwithmappingeventsofwarningbirds.Thesemethods weregroupedinthreecategoriesandenteredinthestatisticalanalysesasafactorwiththefollowinglevels:nestsearch,nestsearch | 10491 LAURSEN Et AL. andterritorymapping,andterritorymappingandtelescopeuse.A detaileddescriptionofthecensusmethodsisgiveninSupporting informationAppendixS1. 2.3 | Climate Climate estimated as long-term change in precipitation and temperaturetogetherwithgroundwaterlevelisknowntoaffectbreeding wader populations (Thorup, 1998; Bellebaum & Bock, 2009; Schroederetal.,2012;Maier,2013).Weusedmeanofdailymaximumairtemperature(°C)inAprilandsumofmonthlyprecipitation forMarch, April, and May (mm, datafrom DanishMeteorological Institute). We used data on climate measured at a local coastal weatherstationatVestervig.GroundwateratTipperneandwater level at the outlet sluice at Vejlerne were measured, but not includedintheenvironmentalanalysisduetosignificantcorrelations (p<0.05)withprecipitationinmostspringmonths. 2.4 | Nutrients Data on fertilizer from farmland in Denmark were estimated for 1928–2014 as the annual amount of outlet of total-N (tons) to coastalwaters(Conleyetal.,2007)andupdatesbyHansen(2011) andThodsenetal.(2016).Eachupdatewascalibrated totheformerlevel.Thisdatasetwasusedforthelong-termstatisticalanalysesforTipperne.From1989,dataonnitrogen(μg/L)concentration werecollectedinRingkøbingFjord(surroundingTipperne)andfor nitrogen in Limfjorden (adjacent to Vejlerne) as a part of the nationalmonitoringprogramNOVANA(datafromEnvironmentCentre Ringkøbing;bothsites;Hansen,2015).Thesedatasetswereused fortheshort-termstatisticalanalysesatTipperneandVejlerne. 2.5 | Management and predation Habitatmanagementasgrazingandmowingisimportantformaintaining populations of breeding waders while predators reduce breedingsuccess(Thorup,1998;Bellebaum &Bock,2009;Maier, 2013). At Tipperne, we have data on the number of cattle, area grazed(ha),andtherelativeareamowedsince1931.Duetoqualitativeinformationonareamowed,itwasclassifiedas0(0%–5%ofthe meadowsmowed),1(6%–25%mowed),2(26%–50%mowed),or3 (51%–75%mowed).AtVejlerne,dataonthenumberofcattle,the areagrazed,andtheareamowedwereavailable. We analyzed the effects of foxes on nest predation (Thorup, 1998;Kjeldsen,2008).Informationaboutfoxabundancewastaken from the official Danish bag statistics, which goes back to 1941. Fromthisyearupto1972,weusedthenationalbagsizeoffoxesasa proxyforfoxabundance(annualnumberoffoxesshotinDenmark). From1973to2014,informationexistsaboutfoxbagatthecountry level(annualnumberoffoxesshotpercountysurroundingTipperne andVejlerne),andweusedthislocalinformationtoaccountfordifferences between regions. Environmental data for Tipperne and VejlerneareshowninSupportinginformationTablesS1andS2. 2.6 | Statistical methods Weusedgeneralizedleastsquare(GLS)thatallowserrorstobe correlatedandtohaveunequalvariances.WetestedfortemporalautocorrelationforeachwaderspeciesbuildingtwoGLS, FIGURE1 Numberofbreedingpairsofsevenwaderspeciesat (a)Tipperneduring1928–2014and(b)Vejlerneduring1978–2014 (a) (b) FIGURE2 Boxplotsofeffectsizeforimpactsofdifferent environmentalconditionsonpopulationsizeandpopulation trendsofwaders.Theboxplotsshowmedians,quartiles,5and95 percentiles,andextremevalues –0.8 –0.4 0.0 0.4 0.8 Effect size Area grazed No. of cattle Amount No. of foxes AmountTemperature Year fertilizer rain 10492 | LAURSEN Et AL. oneof themincorporatingthe first-orderautoregressivecorrelation structure for year and the other one without it. We comparedbothmodelsusingANOVAandlikelihood-ratiotest (LRT) to evaluate which model performed better (Pinheiro & Bates,2000).Allanalysesshowedevidenceoftemporalautocorrelation(allp <0.01).Hence,weusedGLSthatincorporate the first-order autoregressive correlation structure for year toevaluate foreachwaderspecies seven predictors explaining variation in population size across years. The predictors weretemperatureinApril,totalprecipitationfromFebruaryto May,amountofnutrients,numberofcattle,totalareagrazed, numberoffoxes,andyear.Countnumbersforeachwaderspecieswerelog-transformedpriortoanalyses(exceptforlapwing countsthatshowedadistributionclosetoaGaussiancurve).All predictorswerestandardizedtoameanofzeroandSD =1to ensurethatallvariablesbeingatthesamescaleandtheinterceptbeinginterpretable.Residualsofeachmodelwerevisually inspectedfordeviationfornormalityusingnormalQQplots, andheteroskedasticity wasalsovisuallyinspected withplots ofresidualsagainstthefittedvalues.Webuiltmodelsforlong- termandshort-termdataatTipperneandshort-termdataat Vejlerne. We employed the libraries “nlme” (Pinheiro, Bates, DebRoy,&Sarkar,2018)andusedRversion3.3.3(RCoreTeam 2017). WeestimatedeffectsizesasPearson’sproduct–momentcorrelationcoefficientsbyusingstandardconversions(Rosenthal,1994). Theseeffectsizeanalysesonlyincludedfewobservations,implying thatthestatisticalpowerofanyspecificanalysisislow.Weadopted Cohen’s(1988)recommendationsforthemagnitudeofeffectsbeing small(Pearsonr=0.10,explaining1%ofthevariance),intermediate (r=0.30,explaining9%ofthevariance),orlarge(r=0.50,explaining 25%ofthevariance). 3 | RESULTS 3.1 | Effect size, environmental change, and species at Tipperne during 1928–2014 Overall effect size weighted by (N–3) was on average +0.033 (SE =0.016), N =147, marginally differing from zero (t =2.02, df =146, p =0.045). There was no significant difference in effectsizebetweenthetwosites(F =0.254,df =1,145,r2 =0.00, p =0.615(Figure2)). Effectsizedidnotdiffersignificantlyamongspecies(F =1.08, df =6, 140, r2 =0.0003, p =0.377). The four largest effect sizes were for foxes reducing the short-term abundance of avocet at Vejlerne(r =−0.552,t =2.90,df =26,p =0.0074),rainincreasingthe long-term abundance of lapwing at Tipperne (r =+0.427, t =3.58, df =66, p =0.0077), temperature increasing the long-term abundanceofgodwitatTipperne(r =+0.412,t =3.44,df =66,p =0.001), andfoxesreducingtheshort-termabundanceoflapwingatVejlerne (r =−0.339,t =3.42,df =26,p =0.0021).Short-termeffectsizefor godwitatVejlerneincreasedwithnutrientswithalargeeffectof +0.468, t =2.476, df =26, p =0.020, and avocet in the long term at Tipperne likewise had a strong positive effect size of +0.313, t =2.655,df =66,p = 0.0099. Effect size differed significantly among environmental variables (Figure3; F =5.797, df =6, 140, r2 =0.16, p<0.0001). The interactionbetweenspeciesandenvironmentalvariableswasalso statistically significant (Figure3; F =3.415, df =36, 140, r2 =0.44, p<0.0001). Thus, not all six environmental variables had similar effectsonthedifferentspecies.Precipitationhadanintermediate significantpositiveeffectonabundance,whiletemperaturehada significantpositiveeffect,foxesasignificantnegativeeffect,numberofcattleasignificantnegativeeffect,andareagrazedasignificantpositiveeffect(Figure3;Table1). FIGURE3 (a)Relationshipbetweeneffectsizesfordifferent charactersbetweenshort-termstudiesatTipperneandlong-term studiesatTipperne.Thelinesshowthepositivelinearregressions. (b)Relationshipbetweeneffectsizesfordifferentcharacters betweenshort-termstudiesatTipperneandshort-termstudiesat Vejlerne –0.8 –0.4 0.0 0.4 0.8 –0.8 –0.4 0.0 0.4 0.8 Short-term effect sizes Vejlerne Short-term effect sizes Tipperne (b) – 0.8 – 0.4 0.00.4 0. 8 – 0.8 – 0.4 0.0 0.4 0.8 Long-term effect sizes Tipperne Short-term effect sizes Tipperne (a) | 10493 LAURSEN Et AL. 3.2 | Correlations between effect sizes at different sites and in periods of different duration For the data from Tipperne, there was a positive correlation between short- and long-term effect sizes (Figure 3a; F =10.187, df =1,47,r2 =0.16,p =0.0025,estimate(SE) =0.334(0.105),effect size+0.42).Thus,populationchangeshavebeenparallelatshortand at long terms.Similarly, there was a positivecorrelation between short-termeffectsizeatTipperneandshort-termeffectsatVejlerne (Figure3b; F =12.260, df =1, 47, r2 =0.19, p =0.0010, estimate (SE) =0.391(0.112),effectsize+0.45).Therefore,specificenvironmentalfactorshadsimilareffectsacrossspatialscales. 4 | DISCUSSION Themainfindingsofthislong-termstudyofpopulationtrendsof breedingwadersattwonaturereservesinDenmarksince1928and 1978weresignificantimpactsofmultiplecomponentsofenvironmentalchange.Inthepresentstudy,wetestedforconsistencyin effectsizesforenvironmentalvariableshypothesizedtoaffectpopulationtrendsofwaders.Wefocusedonasuiteofenvironmental changeparametershypothesizedtoactonbreedingwaderpopulations,althoughthesespeciesaremigrantsthatspendthenonbreedingseasonalongtheEastAtlanticFlywayfromtheWaddenSeain thenorthtoWestAfricainthesouth(Bønløkkeetal.,2006).The long-termtimeseriesdatingbackto1928allowedustotestforheterogeneity in strength of the relationship between abundance of breedingwadersandmultiplecomponentsofenvironmentalchange. Inparticular,wewereabletorankenvironmentalcomponentsin terms of importance. We found no significant difference among speciesineffectsize,butwedocumentedsignificantheterogeneityamongenvironmentalfactors,andtheseeffectsvariedamong species.Importantly, effectsizesfor thetwo shorttime seriesat TipperneandVejlernewerepositivelycorrelated,andthatwasalso thecasewhenrelatingeffectsizesfortheshorttermandthelong termatTipperne.Thus,effectsizesforenvironmentalfactorswere consistentacrosstemporalandspatialscales. Climatechangeiscurrentlyconsideredamajordeterminantof phenology, demography, distribution, and population trends (reviewsinMøller,Fiedler,&Berthold,2010;Pearce-Higgins&Green, 2014;Stephensetal.,2016).However,thereisonlylittleempirical evidencesuggestingthatpopulationsizeofbirdsisimpactedbyclimatechange(Dunn&Møller,2014;Stephensetal.,2016).Arrival dateandearlybreedinginwadersareclearlyaffectedbywarmer temperature in spring, although altered by agricultural practice (Petersen, Meltofte,&Tøttrup, 2012;Schroederetal.,2012).We showedconsiderablefluctuationsinbreedingpopulationsofwaders at Tipperne since 1928, explained by spring temperature and in particular precipitation. We documented a mean effect size of +0.197(SE =0.040)forspringprecipitationandaweakereffectsize of+0.110(0.044)forspringtemperature.Sincebothtemperature andprecipitationhaveincreased,thisimpliesthatthechangesinclimatearethosethatimprovedtheabundanceofbreedingwadersthe most.Temperatureandprecipitationareknowntoaffectreproductioninwaders(Schroederetal.,2012),andpopulationsresponding positivelytoclimatechangearelikelytoincrease(Møller,Rubolini,& Lehikoinen,2008;Stephensetal.,2016). Landusehaschangedconsistentlyinthetwostudysitesdueto management.Interestingly,wehaddetailedinformationonthearea grazedandthereforeonitsrelativeimportanceforbreedingwaders. Grazingreducedtheheightofthevegetation,sloweddownoreven reversedsuccessionalprocesses,andincreasedarthropodbiomass, which in turn had beneficial effects on growth of young (Norris etal.,1998;Eglingtonetal.,2008;Maier,2013).Inaddition,vegetationheightaffectstheabilityofwaderstoobservepredatorsata distance,butalsopreventsuseofsuitablenestingsitesandaccess topreferredforaginghabitatsforyoungduetotallswards(Cramp, 1985;Kleijnetal.,2010).Wefoundevidenceofaweakmeaneffectofthenumberofcattleonpopulationsizeofdifferentspecies ofwadersatthetwostudysites.However,theweakmeaneffect ofnumberofcattleof−0.032(0.026)impliesthatthismanagement toolinfacthadadetrimentaleffectratherthanabeneficialeffect onthenumberofbreedingwaders.Incontrast,theareagrazedhad ameaneffectof +0.031(0.030).This impliesthat thenumberof breedingwadersimprovedmarginallywiththeareagrazedbycattle. Weanalyzedtheeffectsoffoxesonpopulationsizeofbreeding waders that mainly act through effects on nest predation andtoasmallerextentonpredationonadultbirds(Beintema& Müskens, 1987; Meisner etal., 2014). We expected that foxes wouldnegativelyimpactpopulationtrendsofwaders.Indeed,we foundanexpectedmeaneffectof−0.106(0.050).Atotalof16 Variable Mean SE Wilcoxon W N p Year −0.014 0.053 −9,330 21 0.13 Amountof fertilizer +0.024 0.033 4,075 21 0.51 Areagrazed +0.031 0.030 33,871 21 <0.0001 No.ofcattle −0.032 0.026 −47,365 21 <0.0001 No.offoxes −0.086 0.041 −76,427 21 <0.0001 Temperature +0.110 0.044 82,291 21 <0.0001 Precipitation +0.197 0.040 19,652 21 <0.0001 TABLE1 Mean(SE)effectsizesfor environmentalfactorsatTipperneand Vejlerneandtestsfordifferencefromthe nullhypothesisofzeroinWilcoxon matched-pairssigned-ranktests 10494 | LAURSEN Et AL. outof21effectsizeswerenegative.Differencesineffectsoffox predationovertimeandbetweensitescouldbetheconsequence ofoutbreaksofthesarcopticmangediseasecausedbytheskin- dwellingmiteSarcoptes scabiei.Scabiescanreducefoxpopulations locallyandnationallywitheffectsonthebreedingwaterbirdcommunity(Forchhammer&Asferg,2000;Clausen&Kahlert,2010). There was a negative impact of foxes on waders, as shown by Roodbergenetal.(2012). Fertilizer increases nutrient availability, primary productivity, andsubsequenteffectsontheabundanceofanimalsathighertrophiclevelsinthemarineenvironment(Phillippartetal.,2007;Møller etal.,2015).Meaneffectsizeoffertilizeronwaderswasonly+0.024 (0.033),whichwasnotsignificantlydifferentfromzero.Here,we documentedtworelativelylargeeffects.Wefoundthateffectsize forgodwitatVejlerneincreasedwithfertilizerusewithalargeeffectsizeof+0.468,t =2.476,df =26,p =0.020,andavocetinthe long-termatTippernelikewisehadastrongpositiveeffectsizeof +0.313,t =2.655,df =66,p =0.0099.TipperneandthesurroundingRingkøbingFjordarestronglyimpactedbydrainagefromSkjern River,whichtransportshugeamountsofnutrientsfromlargesurroundingagriculturalareas(Petersenetal.,2008). Thisstudyhassignificantfutureprospects.First,weonlyanalyzed the main factors that most likely affect populations and populationtrendsofbreedingwaders.Clearly,itwouldbeinterestingtoassesstowhichextentinteractionsbetweenfactorsmay impactpopulationsandpopulationtrends.Second,thisstudyhas importantimplicationsforconservationintermsofmanagement ofnaturereserves,managementofpopulationsofpredatorssuch asfoxes,andmanagementofvegetationasaffectedbygrazing. Clearly,mostnaturereserves,oftensmallinsize,willbeimpacted byanumberoffactorsrelatedtoenvironmentalchange,butalso influenced by surrounding areasthat aremuch larger.Wehave shownherethateffectsizesforshort-andlong-termeffectsare positivelycorrelatedandthatdifferentfactorsaffectthesizeof breedingwaderpopulations. In conclusion, we have analyzed unique long-term data on breeding populations of waders with the longest time series starting in 1928. When analyzing the relationship between the abundanceofbreedingwadersandmultiplecomponentsofenvironmental change, we found significant evidence of effects. Whiletherewerepositivecorrelationsbetweeneffectsizesfor short-termstudiesatdifferentsites,orlong-andshort-termeffect sizesatthesamesite,thesecorrelationswererelativelystrongaccountingfor10%–15%ofthevariance.Thesefindingsemphasize theimportanceofconsideringheterogeneityinfuturemonitoring schemes. ACKNOWLEDGMENTS WethankJettePoulsenEngholm,EnvironmentCenterRingkøbing, for providing data for nutrients. O. Gordo provided constructive criticism.ThestudyreceivedfinancialsupportfromAageV.Jensen Naturfond.Wedeclarenoconflictofinterests. AUTHORS CONTRIBUTION APMconceivedtheproject;OTandHHNcollectedthedata;APM andKLanalyzedthedata;KL,APM,OT,HHN,andTAwrotethe manuscript. DATA ACCESSIBILITY WesuggesttostorethedataatTreeBASE,ifthepaperisaccepted. 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