J Appl Ecol. 2019;56:1839–1849. wileyonlinelibrary.com/journal/jpe  | 1839© 2019 The Authors. Journal of Applied Ecology © 2019 British Ecological Society

Received:31January2019  |  Accepted:10April2019DOI: 10.1111/1365-2664.13419

R E S E A R C H A R T I C L E

Remnant forest in Costa Rican working landscapes fosters bird communities that are indistinguishable from protected areas

Daniel S. Karp1  | Alejandra Echeverri2 | Jim Zook3 | Pedro Juárez4 | Alison Ke1 | Jaya Krishnan2 | Kai M.A. Chan2 | Luke O. Frishkoff5

1DepartmentofWildlife,Fish,andConservationBiology,UniversityofCalifornia,Davis,California2InstituteforResources,Environment,andSustainability,UniversityofBritishColombia,Vancouver,BC,Canada3UnióndeOrnitólogosdeCostaRica,NaranjodeAlajuela,CostaRica4HerbarioNacionaldeCostaRica,MuseoNacionaldeCostaRica,SanJosé,CostaRica5DepartmentofBiology,UniversityofTexasatArlington,Arlington,Texas

CorrespondenceDaniel S. KarpEmail:dkarp@ucdavis.edu

Funding informationNationalGeographicSociety,Grant/AwardNumber:9977-16;BelmontForum,Grant/AwardNumber:G8PJ-437336-2012;CanadianNetworkforResearchandInnovationinMachiningTechnology,NaturalSciencesandEngineeringResearchCouncilofCanada,Grant/AwardNumber:06-5566;GraduateLeadershipFellowship;KillamDoctoralFellowship;UniversityofToronto;NSFGRF;CanadaResearchChairs,Grant/AwardNumber:A15-0109;AnimalCareCommittee;CostaRicangovernment,Grant/AwardNumber:SINAC-SE-CUS-PI-R-036-2016andSINAC-SE-CUS-PI-R-030-2017

HandlingEditor:RicardoSolar

Abstract1. Theoutcomeof theongoingbiodiversitycrisisdependson thecapacityof theEarth’s wildlife to persist in working landscapes. Yet, the species that occupyworkinglandscapesareoftendistinctfromthoseinprotectedareas,withalargegroupof“sensitivespecies”thoughttorarelyventureintohuman-dominatedland-scapes.Asgovernmentshavecommittedtorestoringdegradedlandsworld-wide,determiningwhetherandhowworkinglandscapescanberestoredtobenefitsen-sitivespeciesremainsamajorchallenge.

2. We surveyed Neotropical birds across Northwestern Costa Rica in protectedareas,farmsandforestsembeddedwithinworkinglandscapes.Weanalysedcom-munitycompositiontounderstandhowgradientsofforestcover,fragmentationandregionalprecipitationdeterminehowconserving(orrestoring)tropicalforestsinworking landscapes could safeguard entire communities, especially sensitivespecieswithlimitedranges.

3. We foundagricultural sitesmaintained relativelyhighbirddiversitybuthostedvery distinct communities from those found in protected areas. The averagerange size of species found in agricultural communitieswas double the size ofspeciesinprotectedareas.However,highforestcoversitesinworkinglandscapeshousedbirdcommunitieswithsmallrangesizesthatwereequivalenttothoseinnearbyprotectedareas,despitebeingtwiceasfragmentedandsignificantlymoredisturbed.

4. Theeffectoflocalforestcoveronbirdcompositionwascontingentonbothland-scapecontextandregionalclimate.Whenlocalforestcoverincreasedinwetterregionsandmoreforested landscapes,birdcommunities inworking landscapesexhibited a stronger shift towards the assemblages found in protected areas.Specifically,wefoundthatreforestingthewettestsiteswouldincreasesimilaritytoprotectedareasfourfoldcomparedtoonlyatwofoldincreaseinthedriestsites.

5. Synthesis and applications. Despite experiencingmuchmore fragmentation anddegradation than protected areas, forests in Costa Rican working landscapescanmaintainbirdcommunitiesthatstronglyresemblethosefoundinprotectedareas.Thissuggeststhatconservingorrestoringforests inworkinglandscapes,

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1  | INTRODUC TION

Conservationbiologistsandpractitionersareincreasinglyrecogniz-ing the value ofworking landscapes for safeguarding biodiversity(Chazdonetal.,2009;Kremen&Merenlender,2018).Indeed,“work-inglandscapes,”orhuman-dominatedlandscomposedofpastures,multiplecropspeciesandpatchesof forests,grasslandsandothernatural habitats, have been repeatedly shown to sustain diversecommunities (Melo, Arroyo-Rodriguez, Fahrig,Martinez-Ramos, &Tabarelli,2013).Yet,thespeciesthatoccupyworkinglandscapesareoftendistinctfromthoseinprotectedareas,withthemostvulnera-blespeciesfailingtopersist(Karpetal.,2015;Newboldetal.,2016;Pfeiferetal.,2017).Evenminordisturbancesinotherwiseintactfor-estssometimesexactdeclinesinvulnerableforestspecies,necessi-tatingthecreationofprotectedareas(Barlowetal.,2016;Bettsetal.,2017).Thus,despiteencouraging findings related to themain-tenanceoflocaldiversity,humanmodificationofintactlandscapesisstillrestructuringbiologicalcommunities(Newboldetal.,2016).

Nonetheless,ongoingandprojectedtrends in land-useare im-pedingeffortstosufficientlyexpandtheglobalreservenetworktoslowtheongoingbiodiversitycrisis(Pouzolsetal.,2014).Therefore,while reservecreationmust remainacornerstoneofconservationpolicy, the fateof Earth'swildlifewill at least partially dependonthe hospitability of working landscapes (Chazdon et al., 2009).Ecologistsandpractitionersareincreasinglycallingforconservationinitiativesthattargetworkinglandscapes(Kremen&Merenlender,2018),includinglandscape-scalerestorationprojects.Forexample,theworld'sgovernmentshavebeenchallengedtorestore150Mhaofdegradedlandworld-wide—anareathesizeofMongolia (Menz,Dixon,&Hobbs,2013).

Akeyquestionfacingsuchinitiativesiswheretotargeteffortstomaximizethebenefitsforbothpeopleandnature(Menzetal.,2013).Atregionalscales,therelativerelianceofdifferentspeciesonintactforestmayshiftacrossclimategradients,whichcouldinfluenceres-torationplacementstrategies(Karpetal.,2018).Atlandscapescales,avarietyof factorsareknown tomediate thespeedandcapacityforrestorationprojectstorecruitviablepopulationsofnativespe-cies (Reid,Mendenhall, Rosales, Zahawi,&Holl, 2014). For exam-ple,the“intermediatelandscape-complexityhypothesis”positsthatconservation interventions should be targeted in human-modifiedlandscapeswithintermediateamountsofremainingnaturalhabitat(Tscharntkeetal.,2012).Thethinkingisthatincompletelyclearedlandscapes, sourcepopulationsmaynotexist to sendcolonists torestoredsites,and,inveryintactlandscapes,somuchhabitatexists

thatcolonistsmay“spillover”intoclearedareas,withorwithoutanyconservationinterventions.

The intermediate landscape-complexity hypothesis, however,wasprimarilyconceivedwiththegoalofbolsteringgeneralist,eco-system-serviceprovidersthatrelyonforestsbutreadilymoveintoagriculture.Consequently, restoringorconservinghabitat in inter-mediate landscapes may fail to conserve vulnerable species thatrarelyutilizeagriculture (Tscharntkeet al., 2012).Moreover,manyforest-restrictedbirdsrefusecrossinganydeforestedgapstocolo-nizenewfragments(Ibarra-Macias,Robinson,&Gaines,2011).Thus,restorationmaybemostsuccessfulatbolsteringforest-associatedspecieswhen sites are located in landscapeswith large blocks ofcontiguousforest(Reidetal.,2014).

We surveyed bird communities in Costa Rica to evaluate thepotential forworking-landscape conservation to bolster forest-re-stricted birds. Specifically, we censused birds at 150 sites over2 years in 5 reserves and 20working landscapes, arrayed acrossan independent precipitation gradient encompassingwet and dryforests(~1.5–2.8m,annualrainfall).Reservesvariedinsize(range:9.1–183 km2,mean: 59 km2) and time since establishment (range:1974–1994,mean:1984).Agriculturalsitesencompassedpastures,rice, sugarcane,andTaiwangrass (a foragecrop).Forests inwork-inglandscapesvariedintheamountofforestcoverwithin50m(i.e.local scale; range: 44%–100%,mean: 85%) andwithin 610m (i.e.landscapescale;range:16%–96%,mean:63%;seemethodsforscaledefinitions).Ourworkwasorganizedaroundthreequestions.First,towhatextentcanforestsandfarmsinworkinglandscapesmaintainlocal bird richness relative to protected areas? Second, given thatforestsinworkinglandscapesareoftenfragmentedanddegraded,how distinct are bird communities in working landscapes versusprotectedareas?Inparticular,canspeciesofconservationconcernpersist?Third,whereshouldforestconservationandrestorationbetargetedtofacilitatereserve-likebirdcommunities?

2  | MATERIAL S AND METHODS

2.1 | Bird surveys

Weselected25focallandscapesinNorthwestCostaRica:20inwork-ing landscapesand5 inprotectedareas (ReservaBiológicaLomasBarbudal,ReservaNaturalMonteAlto,andParquesNacionalesPaloVerde,BarraHonda,andDiriá).Protectedareasencompassedmostoftheprecipitationgradient(1.6–2.4mvs.1.5–2.8matothersites).Otherprotectedareas intheregionwouldnothaveservedasfair

particularlywithinwetterregionsandalreadyforestedlandscapes,maysafeguardbirdcommunitieswhencreatingprotectedareasisinfeasible.

K E Y W O R D S

avian,deforestation,fragmentation,habitatloss,landscapecontext,reserve,restoration,workinglandscapes

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comparisonstoourworking-landscapesites,astheywereeithertoofarawayorencompassedhabitattypesthatwedidnotsurvey.

Ineach landscape,we identified sixbird survey sites (N = 150 total).Inworkinglandscapes,threesiteswerelocatedinagricultureandthreeinadjacent,privatelyownedforests.Siteswithinthesamelandscapewere separatedby500monaverageandwerechosensothatlocalforestcovervariedindependentlyfromlandscape-levelforestcoverandconfiguration.That is,wesystemicallyvariedsitelocationswithineachlandscape,placingsitesinforestinteriorsandforestedges,inareassurroundedbysubstantialforestcoverandinsmallfragmentssurroundedbyagriculture(FigureS1andTableS1inMethodsS1).Inprotectedareas,foursiteswerelocatedinforestinteriorsandtwoatthereserves’edges.

Oneexpertobserver(J.Zook)conducted20min,50mfixedra-diuspointcountsateachsite.Becauseourfocuswasontheresidentavifauna, survey effort was concentrated on the Boreal summer(May–August).Dryseasonsurveyswouldhaveresultedinfewres-identdetections,asmanyspecies leavedryforestsduringthedryseason and vocalize less frequently. Sites in working landscapeswere surveyed in 2016 and2017; protected areaswere surveyedonly in 2017. Approximately half of the siteswere sampled threetimeseachyear(forbinomialmixturemodelling,seebelow)andtheotherswereonly surveyedonce.Zook surveyedone farmorpro-tectedareaperday(sixsites).Surveysbeganatsunriseandcontin-uedfor~5hr.Allbirdsseenorheardduringcountswererecorded,inadditiontothetimeofday,thepresenceofloudnoise(e.g.cicadas,streamsandfarmmachinery),numberofpeoplenearby,windspeed(usingananemometer)anddistancetonearestriver.

2.2 | Environmental gradients

We quantified the local vegetation structure, surrounding forestcoverand regionalprecipitationassociatedwitheachsite. In four,5-m-radiussubplotsateachsurveysite,wequantifiedthefollowingvegetationstructurevariables:canopy cover,proportion of trees with epiphytes or vines,proportion of trees with lianas,understorey density,herbaceous ground cover,shrub cover,tree species richness,number of tree stems,mean tree DBH and mean vegetation height(seeMethodsS1). To quantify surrounding forest cover, we hand-classified alltrees,includingplantations,within1.5kmofeachsurveysiteusingGoogle Earth imagery from2013 to 2017 (Karp et al., 2018).Wegroundtruthedourfinalmapusingthe600vegetationplotsdetailedabove.Wethendefinedlocal forest coverasthefractionoftreecoverwithin50mofeachsurveysite.Landscape forest coverwascalcu-lated atmultiple spatial scales andwas defined as the proportionoftreecoverwithin“doughnuts,”whichalwayshadaninnerradiusof50mbuttheouterradiusvariedfrom60mto1.5kmby10-mincrements.Tocalculatelandscapeconfigurationatmultiplescales,we first deleted all isolated tree clusters 75%forestcoveratlocalandlandscapescales),low‐cover forest (N = 45; forested sites inworking landscapeswith95%oftheposteriors.

To compare vegetation structure and landscape attributes be-tweenlanduses,weimplementedLinearMixedModels(LMMs;Bates,Maechler,Bolker,&Walker,2015)thatincludedcategoricallanduseasthesolefixedeffectandarandomeffectoflandscapetoaccountforspatialautocorrelation.Wetransformedresponsevariableswhennecessary to satisfymodel assumptions (FigureS8 inMethodsS1).Variablesignificancewasassessedusing likelihoodratiotests,com-paringnestedmodelswithandwithoutthecategoricalland-usefixedeffect(Zuur,Ieno,Walker,Saveliev,&Smith,2009).

2.4 | Modelling species richness, range size, and similarity to reserves

We used the binomial mixture model to estimate species abun-dancesacrosssites.Specifically,weextracted themodelledabun-dance of each species at each site in 2017 (Ni,j,2017)—the year in

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whichallsitesweresampled—alongeachiteration(N=2,000)oftheposterior (Karpetal.,2018).Usingeachof these2,000 “posteriorcommunities,”wecalculated thespecies richnessofeachsite.Wealsocalculatedtheaveragerangesizeacrossallspeciespresentateachsite,usingestimatesfromBirdLifeInternational(2019).

Next, we quantified the bird community similarity betweeneachpairofsitesusingpresence-absence(Sørensonsimilarity)andabundance (Bray–Curtissimilarity)metrics.Wedecomposedthesemetrics to analyse their turnover components, using “betapart” inr (Baselga,Orme,Villegar,Bortoli,&Leprieur,2018;RCoreTeam,2018). We visualized differences between sites in their speciescompositionsusingnon-metricmultidimensionalscaling,andtestedwhetherdifferentlanduseshostedsignificantlydifferentcommuni-tiesviapermutationalmultivariateanalysisofvariance.Wealsousedthecommunitysimilaritymetricstocalculatetheoverlapbetweenthebirdcommunityfoundateachsiteandcommunityfoundinthenearestprotectedarea. Specifically, for eachmetric andposteriorcommunity,wecalculatedthemultivariatebirdcommunitydistancefromeachsitetothecentroidoftheclosestprotectedarea(Karpetal.,2018).Aswewereinterestedinthemost“intact”reservecom-munity,weexcludedthetwoedgesitesineachprotectedareawhencalculatingsimilaritytoreservecommunities.

Wemodelledspeciesrichness,averagerangesize,andreservesimilarityusingLMMswithlandscapeasarandomeffectandthefol-lowing fixedeffects: local forest cover (linearandquadratic terms),landscape forest cover and edge, precipitation, vegetation structure, and interactions between local forest cover and precipitation,landscape forest cover,andforest edge.Forthespeciesrichnessandrangesizeanalyses, we included reserve sites and added reserve status (i.e.,whetherthesitewasinareserveornot)asanotherpredictor.Forthereservesimilarityanalysis,weomittedreservesitesbutincludeddistance to nearest reserve as another fixed effect to account forcommunitysimilaritydecayingwithdistance(Karpetal.,2018).Weomitteddistance to reservesinmodelsthatdidnotfocusoncommu-nitysimilarity.Inallmodels,vegetation structure wasmeasuredasthesecondandthirdprincipalcomponentsofaPCAonallvegetationstructure variables. The first principal componentwas highly cor-relatedwithlocal forest cover(Pearson'sr=0.88,df=148).

All fixed effects were standardized prior to analysis. Modelswere weighted by the posterior variance of the species richness,reserve size, and reserve similarity estimates (Karp et al., 2018).AllmodelsconformedtoLMMassumptions(i.e.normality,hetero-scedasticity)andnoneoftheincludedparametersdisplayedsevereevidenceofcollinearity(varianceinflationfactors

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While habitat fragmentation per se (measured as landscape-scale forestedge length)didnotaffectspeciesrichnessalone,wedidobserveaninteractionbetweenforest edge and local forest cover amount,suchthatthestrongestrichnessincreaseswithlocal forest coverwereobservedintheleastfragmentedlandscapes(Figure1b).Noneofourresultschangedwhenimplementingforwardorback-wardsmodel selection. Resultswere also largely consistentwhenexaminingrawdetections(ratherthanmodelledabundances).Rawdetectionmodelsdid,however,suggestaninteractionbetweenpre-cipitationand local forestcover, such that richnessdisproportion-atelyincreasedinwetter,moreforestedsites.Restrictingourfocusto forested sites and excluding agriculture, all models supportedtrends of increasing richness at sites with more landscape forestcoverandinwetterregions(TableS3andFigureS4inMethodsS1).Wefoundlessconsistentsupport,however,forrichnessincreasinginstandswithfewer,largertreesandatsiteswithmoreunderstoreydensityandherbaceousgroundcover.

3.2 | Are bird communities in working landscapes distinct from those in reserves?

We found strong evidence that community composition shiftedacross the environmental gradients (Table S4 in Methods S1;Figure2andFigureS5inMethodsS1).However,communitieswere

muchmoreresponsivetolocalforestcoverand,toalesserextent,regionalprecipitationthanothervariables.Wealsofoundthatcom-munitycompositionsignificantlydifferedbetweenprotectedareas,high-coverforest(i.e.sitesinworkinglandscapeswith>75%forestcoveratlocalandlandscapescales), low-coverforestsandagricul-ture.Onekeyexceptionwasprotectedareasandhigh-coverforests,whichcouldnotbedifferentiated (p>0.05). Indeed,birdcommu-nitiesrapidlyshiftedatsiteswith>75%localand landscapeforestcover, with “reserve-affiliated species” increasing in proportionalabundance(FigureS6inMethodsS1).

Average range sizes reflected these community shifts. Wide-rangingbirds replacednarrow-rangedbirds at siteswith less localforest cover, especially in less forested landscapes and in wetterregions (Figure 1). As a result, average range sizes in agriculturalcommunitiesweremorethantwiceaslargeascommunitiesinpro-tectedareas(FigureS3inMethodsS1).Rangesizetendedtodeclineinfragmentedlandscapes(Figure1),andinforestedsiteswithfewerlianasandmoreherbaceousvegetation (FigureS7 inMethodsS1).Critically,averagerangesizedidnotdifferbetweenprotectedareasandhigh-coverforests(FigureS3inMethodsS1).

Indeed,wefoundthatveryfewbirdspeciesuniformlydeclinedin abundance outside protected areas, after controlling for differ-encesinforestcover.Specifically,only3ofthe150surveyedspeciesweresignificantlymoreabundant inprotectedareas thanworking

F I G U R E 1  Speciesrichnessandaveragerangesizechangesalonggradients.Richnessexhibitedaslight,nonlinearincreasewithlocalforestcover,peakingat~80%(dottedline;a).Increasesinrichnesswithlocalforestcoverweremostpronouncedatsiteswithlessforestedgeinthelandscape(b).Richnessalsoincreasedwithprecipitation(c)andwiththesecondprincipalcomponentofavegetationstructurePCAthatdifferentiatedsiteswithmanythintreesfromsiteswithfewer,widertrees(d).Unlikerichness,averagerangesizeacrossbirdcommunitiesdeclinedsharplywithlocalforestcover(e).Declinesweremorerapidinsiteswithmorelandscapeforestcover(f)andinwetterregions(g).Rangesizealsodeclinedinmorefragmentedlandscapes(h).Linesindicatepredictedtrends;greyregionsdelineate95%confidenceintervals.Plussignsaresitesinprotectedareas(PA);greycirclesaresitesinworkinglandscapes

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landscapes(FigureS8inMethodsS1).Similarly,whenourbinomialmixture model was modified to compare land-use categories, wefoundthat7,32and50speciesweresignificantlymoreabundantinprotectedareasthanhigh-coverforests,low-coverforestsandagri-culturerespectively(AppendixS2andFigure3).

This near equivalency in bird community composition betweenprotectedareasandhigh-coverforestsexisteddespitestructuraldif-ferences(FigureS9inMethodsS1).High-coverforestswereembeddedinlandscapesthatweremorethantwiceasfragmentedasprotectedareas. Logging and other disturbances also contributed to distinct

vegetationstructures.Specifically,comparedtoprotectedareas,high-cover forests exhibited 13% lower canopy cover, 30% shorter treeheights,20%lowertreerichnessand35%lessdenseunderstories.

3.3 | How could working landscapes be managed to promote reserve‐like bird communities?

Communitiesinworkinglandscapeswithmoreforestcoveratlocalandlandscapescalesexhibitedahighdegreeofoverlapwithcom-munitiesinnearbyreserves(Figure4;TableS7inMethodsS1).The

F I G U R E 2  Non-metricmultidimensionalscalingplotsdepictingshiftsinbirdcommunitycompositionalongenvironmentalgradients.Thedistancebetweensites(points)correspondstodifferencesincommunitycomposition(Bray–Curtissimilarity).Sitesthatsharedsimilarlevelsoflocalforestcover(a;greentoorangegradient)orprecipitation(b;purpletoredgradient)alsohostedsimilarbirdcommunities.(c)Birdcommunitiesinreserves(darkgreen;plussigns),high-coverforests(sitesinworkinglandscapeswith>75%forestcoveratlocalandlandscapescales;olive),low-coverforests(lightgreen)andagriculture(orange)weredistinct,exceptthatreserveandhigh-coverforestcommunitiesoverlapped.OvalsareordinationellipsesbasedontheSDofpointscores

F I G U R E 3  Differencesinbirdabundancebetweenreservesandotherlanduses.(a)Barplotsdepictcomparisonsofspeciesabundancesbetweenreservesandhigh-coverforest(sitesinworkinglandscapeswith>75%forestcoveratlocalandlandscapescales;leftbar),low-coverforests(

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effect of local forest cover was nonlinear, with sites acceleratinginreservesimilarityasforestcoverincreased.Thiswasmostlytheresult of accelerating abundance increases of “reserve-affiliatedspecies” at high levels of forest cover; “agriculture-affiliated spe-cies”exhibitedamore lineardeclinewith forestcover (FigureS10inMethodsS1).Thus,themostforestedsitesinworkinglandscapesexhibited roughly the same degree of reserve similarity as actualreserve sites didwith sites in different reserves (Figure 4c,f).Wealsofoundthatincreasinglocalforestcoverinwetterregionsand/or in more forested landscapes increased reserve similarity moreso than anequivalent amountof forest increase indry regionsordeforestedlandscapes.Fragmentationhadnodetectableeffectoncommunitysimilaritywithreserves.Theseresultswerequalitativelysimilarwhenanalysingrawdetectionsandtheturnovercomponentofdissimilarity(TablesS7andS8inMethodsS1).Ourfindingswerealsogenerallyconsistentwhenreservesimilaritywascalculatedwithmetrics thatonlyconsideredspeciespresencesand ignoredabun-dances(FigureS11andTableS7inMethodsS1).

Withinforestsites,findingswerelessconsistentacrosssimilaritymetrics,modelselectionproceduresandanalysistargets(i.e.mod-elledcommunitiesvs.rawdetections;TablesS9andS10andFigureS12 inMethodsS1). In every case,we found that reserve similar-ity increasedatsiteswithmore landscape forestcover.Wefoundless consistent support for increased similarity with greater treeheights, canopy cover, understorey density, proportion of lianas,

tree richness and shrub cover. Finally,we foundvery inconsistentsupport that reserve similarity declined with precipitation, forestedge,numberoftreestemsandDBH.

Ourmodelofabundance-basedreservesimilarityadequatelyfittheobserveddata(conditionalR2=0.90)andcouldthusbeusedtopredictspatialvariationintheprojectedoverlapbetweenbirdcom-munities found inworking landscapes andnearby reserves acrossNorthwest Costa Rica. Both across Northwest Costa Rica andwithin theCorredorBiológicoHojancha-Nandayure (Figure5), re-sultingmapshighlightedthevalueofmaintainingorrestoringforestsinwetterregionsandinregionswithmorelandscapeforestcover.Specifically,modelspredictedthatrestoringagriculturalpixelsinthewettestareasresultedintwicethegainsinreservesimilarityasre-storing in thedriest areas. Similarly, restoring agriculture in100%forested landscapeswas2.65timesmoreeffective in termsof in-creasingreservesimilaritythanindeforestedlandscapes.

4  | DISCUSSION

Our study suggests that there is great scope for conservingNeotropicalbirdsinCostaRicanworkinglandscapes.Speciesrich-ness was no higher in reserves than in working landscapes withsubstantialforestcoveratlocalandlandscapescales,andfewspe-cies(

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forests.Consequently,high-coverforestsandreserveswerelargelyindistinguishableinspeciescompositionandbothhostedcommuni-tiesofbirdswithsmallrangesizes.Thiswassurprisingashigh-coverfragmentswereembedded inworking landscapes thatweretwiceasfragmentedasprotectedareas.Moreover,regular logging,fires,huntingandotherdisturbances likelyalteredthevegetationstruc-tureofforestsinworkinglandscapescomparedtoprotectedareas.Indeed,high-coverforestsinworkinglandscapeshadlowercanopycover,shorter treeheights, fewertreespecies,and lessdenseun-derstoriesthanprotectedareas.Landownerslikelymaintainforestformultiplereasonsincludinglawsthatmandatereforestationnearrivers(Ley7575,276),CostaRica'sflagshipPaymentforEcosystemServicesprogramthatincentivizesforestconservation,andbecausesomeareasmaybemarginalareasforcultivation(e.g.steeperslopes;FigureS13inMethodsS1).Regardless,thesefindingssuggestthatmaintainingforestinCostaRicanworkinglandscapescanpromoteavian communities that resemble those in protected areas, evenwhensubjecttodisturbances.

Critically,we found thatmany species alsopersisted in totallydeforested sites. Specifically, we detected a nonlinear, saturatingrelationship between species richness and local tree cover, suchthatrichnessonlydeclinedby20%(sevenspecies)atthemostde-forestedsites.This finding isnotunique toour region:agriculture

hasbeenshowntomaintainspeciosecommunitiesinotherareasofCostaRica(Karpetal.,2015)andabroad(e.g.Ranganathan,Daniels,Chandran, Ehrlich,&Daily, 2008;Waltert et al., 2005). Especiallybecausestudiesoftropicalwildlifeoftenfocusonforest-restrictedspecies(e.g.Barlowetal.,2016),thisdiversecommunityofagricul-turalspeciesbearsfurtherstudy.

Still, it is importanttoconsiderthe identityofthespeciesthatpersisted in farmland. Only two surveyed species are not listedas “least concern” by the IUCN—Great Curassow (Crax rubra) andYellow-napedParrot(Amazona auropalliata)—bothwhichweremostregularlydetected in forests inworking landscapes (butnot inag-riculture).More importantly,wefoundthat theaveragerangesizeofspeciesinagriculturalsiteswasmorethandoublethatofspeciesinprotectedareas,indicatingthateitheragriculturefacilitatesnatu-rallywide-rangingoverendemicspeciesorthatagriculturefavoursspecies thatwere initially range-restrictedbut laterbecamewide-rangingasagricultureexpanded.

Adivergenceinaveragerangesizereflectsourbroaderobserva-tion that aviancommunity composition stronglydifferedbetweenagriculture and protected areas. Other studies across the tropicshave documented strong shifts in community composition withhabitat conversion (Gibson et al., 2011; Newbold et al., 2016). InCameroon, similarbird richnessbetween forests and farmsbelied

F I G U R E 5  Mapsofstudysitesandsimilarityofbirdcommunitiesinworkinglandscapestoreservecommunities.(a)NorthwestCostaRicaencompassesastrongprecipitationgradient.(b)Mapdepictsprotectedareas(darkgreen),forestsinworkinglandscapes(blue)andagriculture(orange)acrosstheregion.In(a)and(b),whitedotsindicatereservesitesandreddotsaresitesinworkinglandscapes.(c)Wettersitesandsiteswithmoreforestcoveratlocalandlandscapescaleswerepredictedtohostmorereserve-likebirdcommunities.Greenpolygonsdenoteterrestrialreserves(UNEP-WCMC&IUCN,2018).YellowpolygondenotestheCorredorBiológicoHojancha-Nandayure,aregionbeingprioritizedforreforestation.(d)Simulatedreforestationofthecorridor'sagriculturalsitesfrom0%to100%localforestcoversuggestsgreaterincreasesinbirdcommunitysimilaritytoreservesforsiteslocatedinwetterregions(i.e.theSouthwest)andsurroundedbymoreforest(forestinworkinglandscapes=lightgreen;reserves=darkgreen;asopposedtootherland=grey)

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markeddifferencesincommunitycomposition(Waltertetal.,2005).Similarly, inBrazil'sAtlanticforest,vertebratecommunitiesexperi-encedanabruptshiftfromforestspecialiststodisturbance-adaptedspecies when landscape-level forest cover declined below 30%(Banks-Leite et al., 2014). Here, community similarity to reservesalsorespondedstronglytoforestcover,withreserve-affiliatedspe-ciesrapidlyincreasinginabundanceatsiteswithmorethan75%for-estcoveratlocalandlandscapesites.

Insomesenses,ourfindingthattheeffectoflocalforestcoveramplified in forested landscapes contradicts the intermediatelandscape-complexity hypothesis, which predicts stronger effectsof local management in landscapes of intermediate forest cover(Tscharntke et al., 22012). However, this hypothesis originally fo-cusedongeneralist,ecosystem-serviceproviders,ratherthanmoresensitiveforestspecies.Ourresultssuggestthatmaintainingorre-storinglargerswathsoftropicalforestmaybeessentialifthegoalistopreservemorereserve-likebiologicalcommunities,completewithrange-restrictedspeciesorothersofconservationconcern(Bettsetal.,2017;Pfeiferetal.,2017;Reidetal.,2014).

Thatsaid,forestedlandscapesmaymaintainseeddispersersthatcould facilitate restoration without active management (Hooper,Legendre,&Condit, 2005),meaning intermediately forested land-scapes should still be targeted for active restoration (Tambosi,Martensen,Ribeiro,&Metzger,2014).Moreover,recentapproachesareabletoprioritizesitesforrestorationbasedoncostsandmulti-plebenefits(i.e.notjustreservesimilarity;Strassburgetal.,2019).Forexample,ifanothergoalistoenhanceecosystemservices,thenrestoringforestindeforestedlandscapeswouldincreasefarmland–forestinterfacesandallowhabitatgeneraliststomovefromforeststofarms(Karpetal.,2015;Ricketts&Lonsdorf,2013).Similarly,agri-culturemaybecompatiblewithwaterbirdconservation:inourstudysystem,80%ofdetectedwaterbirdspecies(e.g.herons,ducksetc.)weremoreabundantinagriculturethanprotectedareas.

Itisalsoimportanttoacknowledgetheregionalcontextbeforeadvocatingthebenefitsofforestconservationinworkinglandscapeselsewhere.First,itispossiblethatoursurveysmissedespeciallyrareforest specialists that are restricted to protected areas.However,only21additional (non-migratory) speciesweredetected in a15-yearbirdcensuseffortat16sitesinourstudyregion(Frishkoffetal.,2014),allofwhicharelistedas“leastconcern.”Apossibilitythatwecannotexclude,however,isthatthemostsensitivespecieshaveal-readybeenextirpatedfromtheregion.Ourstudyregionexperiencedhigh rates of deforestation until the 1980s, atwhich point forestcoverbegan increasing,from23%in1986to47%in2005(Calvo-Alvarado,McLennan,Sanchez-Azofeifa,&Garvin,2009).Thismeansthatsensitivespeciescouldhaveregionallyextirpatedpriortothe1980s.Second,formalprotectedareasareoftensubjecttodegrada-tion,callingintoquestiontheirutilityasabaseline.Indeed,one-thirdofprotectedareasfaceseverehumanpressureandCostaRicaisnoexception(Jonesetal.,2018).Third,ourpriorworksuggeststhatdryforest-associated speciesmay be preadapted to thrive inworkinglandscapes(Frishkoffetal.,2016;Karpetal.,2018).Highsimilaritybetweencommunitiesinreservesandforestedworkinglandscapes

may thus partially reflect the fact that someof our reserves pro-tecteddryforests.Indeed,inwetterAmazoniansites,communitiesturnoverbetweenprimaryforestsandthesecondaryforeststhattypifyworkinglandscapes(Barlow,Mestre,Gardner,&Peres,2007).Finally,othertaxamayresponddifferentlythanbirds;forexample,arecentstudyfounditmaytakecenturiesforplantcommunitiesinsecondaryforeststoresemblethoseinprimaryhabitats(Rozendaaletal.,2019).Thus,prioritizingconservationoffragmented,disturbedforests inworking landscapesmay be still be inadvisable in areasthathostmoreendangeredspecies,are lessdegradedand/or thatarelocatedinwetterregions(Barlowetal.,2016).

5  | CONCLUSIONS

Ourworkyielded several conservation-relevant insights. First,wereportthatwhilebiodiversecommunitiespersistedinagriculture,as-semblageslackedtherange-restrictedspeciesofconservationcon-cernfoundinforests.Second,wefoundthatonly5%ofthespeciessurveyedweremore abundant in reserves than in high-cover for-ests,suggestingvulnerablespeciescouldgreatlybenefitfromcon-servingorrestoringforestinCostaRicanworkinglandscapes,eveniftheforestishighlyfragmentedanddisturbed.Third,ourmappingexerciseillustrateshowourmethodcanbeusedtoprovideconcreteguidanceforsitingconservationinitiatives(e.g.ongoingrestorationeffortsintheCorredorBiológicoHojancha-Nandayure;Figure5d).Indeed,NorthwestCostaRicaisexpectedtoexperiencefuturecli-matedrying (Rauscher,Giorgi,Diffenbaugh,&Seth,2008)andwehavepreviouslyshownthatbirdsassociatedwithwetterandmoreforestedsitesarethemostvulnerabletothesechanges(Karpetal.,2018).Thus,ourworksuggeststhattargetingfuturerestorationandconservationinwetterregionsandmoreforestedlandscapescouldhelp optimize biodiversity conservation, at least for forest-associ-atedbirdsinCostaRica.

ACKNOWLEDG EMENTS

We thank X. Campos, E. Rodríguez, D. Steyn, L. Bogantes, theFurturAgua team, SINAC staff and landowners for supporting ourfieldwork and analyses. Our work was supported by a GraduateLeadership Fellowship and a Killam Doctoral Fellowship to A.E., aUniversityofTorontopostdoctoralfellowshiptoL.O.F.,anNSFGRFtoA.K.andtheCanadaResearchChairsProgram(K.M.A.C.).Additionalfunding included grants from National Geographic (#9977-16), theBelmontForum(#G8PJ-437336-2012)andNSERC(UBC#06-5566).This research was conducted with approval from the Animal CareCommittee (A15-0109) and Costa Rican government (permits:SINAC-SE-CUS-PI-R-036-2016andSINAC-SE-CUS-PI-R-030-2017).

AUTHORS’ CONTRIBUTIONS

D.S.K.,A.E.,K.M.A.C.andL.O.F.designedresearch;D.S.K.,A.E.,J.Z.,P.J., andA.K. collecteddata;D.S.K., L.O.F.,A.E. and J.K. analysed

1848  |    Journal of Applied Ecology KARP et Al.

data;D.S.K.wrotethemanuscript.Allauthorscontributedtodraftsandgavefinalapprovalforpublication.

DATA ACCE SSIBILIT Y

Data available via the Dryad Digital Repository https://doi.org/10.5061/dryad.fg8kq66(Frishkoff&Karp,2019).

ORCID

Daniel S. Karp https://orcid.org/0000-0002-3832-4428

Luke O. Frishkoff https://orcid.org/0000-0001-5738-2140

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SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle.

How to cite this article:KarpDS,EcheverriA,ZookJ,etal.RemnantforestinCostaRicanworkinglandscapesfostersbirdcommunitiesthatareindistinguishablefromprotectedareas.J Appl Ecol. 2019;56:1839–1849. https://doi.org/10.1111/1365-2664.13419

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