Sanesi et al.: Avian Ecological Diversity 2009 International Society of Arboriculture80Avian Ecological Diversity as an Indicator of Urban Forest Functionality. Results from Two Case Studiesin Northern and Southern Italy.Abstract.Greenspacesandforesttreescontributetoanumberofenvironmentalfunctionsinurbanenvironments,suchasthesur-vivalofurban-dwellingspecies(e.g.,birdspecies).Thispaperanalyzestherelationshipbetweengreenspacecharacteristics(struc-turalandspatialattributes)andthediversityofavianecologyspecies.Thisprovidesresearchndingscomingfromtwostudies conductedinItaly.Usingpoint-countmethod,aquanticationwasdoneoftheabundanceanddiversityofbirdspeciesinanum-berofgreenspaceshavingdifferentstructuralattributes(e.g.,vegetationtype,treeheight)andspatialcharacteristics(e.g.,loca-tion,connectivity).Resultsshowedpositivecorrelationsbetweengreenspaceswithamorediverseandmatureforestvegetation andthenumberofspecimensandspeciesobservedinthetwostudies.Apositivecorrelationappearedalsobetweendistanceto thecitycentreandrichnessandabundanceofbirdspecies.Finally,wediscusssomeofthemainimplicationsforenhancingthe functionalattributesofgreenspacesbyusingavianecologicalindicatorstoinformecologicallysoundurbanplanninganddesign. Key Words. Urban Environments; Point-Counts; Urban Biodiversity; Forest Birds; Italy; Ecological Indicators; Urban Greenspaces. Greenspaces and forest areas are essential components of the ur-ban environment because they provide a wide range of environ-mental and social functions to cities and urban dwellers (Costanza et al. 1997; Orians 1986; Padoa-Schioppa et al. 2007; Sanesi and Chiarello 2006). Increasing levels of urban densication are call-ing attention to those measures that can mitigate urban island ef-fects (Mazza and Rydin 1997) or compensate for the overload of pollutants in (urban) air and soil (McPherson et al. 1994; Nowak etal.2006).Citizensarealsogrowingconcernedoverthethe consequence of intense urbanization and its effects on their phys-icaland/orpsychologicalwell-being(VanHerzeleandWiede-mann 2003; Chiesura 2004; Sanesi et al. 2006). A healthy urban environment is often associated with the availability of large for-est areas within cities and the accessibility of such areas by urban residents(e.g.,Hartig2004;HartigandCooper-Marcus2006). Foresttreesarealsoessentialforthesurvivalofmanyani-mal and plant species in urban environments. In particular, stud-ieshavedemonstratedpositiveeffectsofforesttreesonboth invertebrateandvertebratespecies,suchasspiders(Alaruikka etal.2002),ants(Yamaguchi2004),butteries(Hermyand Cornelis2000),carabides(Niemeletal.2002;Ishitanietal. 2003;Maguraetal.2005),andpasserines(Wiens1989;Keast 1990;PettyandAvery1990;MrtbergandWallentinus2000; Padoa-Schioppaetal.2006;Ferraraetal.2008).Forexample, WattsandLarivire(2004)showedhowthepresenceofcara-bidesintheurbanenvironmentcouldbeexplainedbythesize ofgreenareasandthepresenceofindigenousforestspecies. Highlydenseurbanareaswithalackofgreenspac-esandforesttreesareoftenassociatedwiththepres-enceofgeneralistspeciesnestinginhollowtrees(Em-len1974;LancasterandRees1979;Beissinger1982).Althoughtheinuenceofurbanforestsonspecieshasbeen thefocusofrecentstudies(Blair1996),fewcontributionshave exploredthesubjectbyconsideringthebiologicalresponseof species to different types and structures of forest vegetation in ur-ban environments. In this direction, this paper aims to explore the relationship between the urban forest structure and the abundance of certain bird species. We provide research ndings coming from two studies conducted in Italy at northern (Milan) and southern (Bari) locations. At both locations, bird species were used as in-dicators of ecological diversity in urban environments (i.e., avian ecologicaldiversity).Usingpoint-countmethod,wequantied the abundance and diversity of bird species in a number of green-spaces of different structural attributes (e.g., vegetation type, tree height) and spatial characteristics (e.g., location, connectivity). We nally discussed some of the main implications for enhancing the functional attributes by selecting avian ecological indicators and use them to inform ecologically sound urban planning and design.MATERIALS AND METHODSStudy AreasThisstudywasconductedonsixteengreenspaceslo-catedintwomainurbanenvironments:Milan,north-ernItaly(N.13)andBari,southernItaly(N.3). Greenspaceswereopportunisticallyselectedbyconsidering the availability of supplementary data and information on forest speciescompositionandstructureattheyearoftheirestablish-ment as well as data on past and current forest management prac-tices. Selection was also based on considerations on the extension ofeachcityandtheamountof(public)greenspacesavailable. Asageneralgure,Milan(455371N;92097E)ex-tendstoapproximately182km2(72.20mi2)withapopulation of1,303,602inhabitants(ISTAT,2005).Thisgurerisesupto 3,900,000 inhabitants when including surrounding towns and vil-Arboriculture & Urban Forestry 2009.35(2): 8086Giovanni Sanesi, Emilio Padoa-Schioppa, Leonardo LorussoLuciana Bottoni, and Raffaele LafortezzaArboriculture & Urban Forestry 35(2): March 20092009 International Society of Arboriculture81lages. Overall, greenspaces in Milan covers a surface of 15.20 km2 (5.86 mi2); the average amount of greenspaces per capita is approx-imately 11.60 m2 (124.86 ft2; Agenzia Mobilit e Ambiente, 2002). Bari(4173N;83255E)extendstoapproximately 116.20km2(44.87mi2)withapopulation316,000inhabitants. Publicgreenspacescoverasurfaceof1.13km2(0.44mi2)with 3.4m2(36.60ft2)ofgreenspacespercapita(ISTAT,2005).Bird Species SurveyIn each greenspace, we collected a number of data related to the richnessandabundanceofbirdspecies.FromMarch2005to July2006,birdswereobservedandrecordedduringthebreed-ingseasonbymeansofpoint-countswithunlimiteddistance (Bibbyetal.2000).Point-countsareacommonmethodfor samplingbirdspecies(Banietal.2006)becauseitallowsan extensivesurveyingofsampleareasandthesurroundingland-scape(Blondeletal.1970;Reynolds1990).Inaddition,this methodenablescollectingawiderangeofecologicaldataon species with a cost-effective balance (Selmi and Boulinier 2003). In the study, birds were surveyed placing each sample within a grid of 250 m x 250 m while avoiding the overlapping of two continuous observations. Overall, 80 point-counts were covered during eld campaigns. Among bird species surveyed in the two locations,twospecieswereassumedaspotentialindicatorsof urban forest functionality: great tit (Parus major Linnaeus 1758) andtheserin(SerinusserinusLinnaeus1766).Bothspecies werefoundinthetwolocationsinmorethan50point-counts. Furthermore,greattitandserinarewithinthe15targetspe-ciesdescribedbytheatlasofbirdsofMilan(Avium,2006). Species abundance for the two indicator species was expressed in terms of number of individuals per point-count (Bibby et al. 2000).DATA ANALYSISAsrststep,weperformedaclusteranalysisusingUPGMA method (Unweighted Pair Group Method using arithmetic Aver-ages)whichallowedcomparingbirdsintermsofspeciescom-positionoverthesixteengreenspaces(Spellerbergetal.1999).Inaddition,weanalyzedthestructuralandspatialchar-acteristicsofthesixteenurbangreenspaces,suchas:dimen-sioninhectares,percentageofvegetationcover,anddistance fromthecorecenterofthecity(identiedbythecenterof thepolygonalarearepresentingthecityseeTable1).These datawereanalyzedusinganonparametrictest:R-Spearman Coefcient(duetothenon-normaldistributionofobserva-tions).Linearregressionmodelswereusedtopredictspe-ciesrichnessonthebasisofgreenspacescharacteristics.We measured the DBH [Diameter Breast Height, taken at 1.3 m(4.27ft)aboveground]oftheclosest100treessurrounding each point-count within a radius of 100 m (328 ft). DBH values were then analyzed in relation to species abundance values con-sidering the following intervals of DBH: minimum, rst quartile, median, third quartile, and maximum. Such intervals were used to derive input data for an additional regression model. For each DBH interval, we compared the observed species abundance with the average abundance across the 80 point-counts and used those observations with higher values to construct an optimal model of the DBH distribution. All the other observations were instru-mentalforcreatingaminimalmodelofthisdistribution. The U-Mann-Whitney Test was used for the scope. This approach has been used in previous studies (Massa et al. 2003a) and it fol-lows the assumptions that: an high level of abundance is gener-ally preferable for birds in urban settings (Bock and Jones 2004); thatbirdsselectforestwithhighvaluesofDBH,matureurban forest; and that species in urban environments are likely to occur withinheterogeneousanduneven-agedforestvegetation(Blair 1996;DonnellyandMarzluff2006;Sandstrmetal.2006). RESULTSTable2illustratesbirdspeciesdiversityforeachoftheana-lyzedurbangreenspaces.Intotal,56specieswererecord-ed:53speciesinMilanand11inBari;and4,393speci-menswereindentied:3,587inMilanand649inBari. The large part of these species are typical of forest-type habitat (Keast 1990; Hinsley et al. 1995; Massa et al. 2003b; Bani et al. 2006), such as: wren (Troglodytes troglodytes L.); wryneck (JynxtorquillaL.);short-toedtreecreeper(Certhiabrachy-dactyla C.L.Brehm 1820); golden oriole (Oriolus oriolus L.); jay (Garrulus glandarius L.); and great spotted woodpecker (DendrocoposmajorL.).Otherspeciesarecommoninfarm-Table1.Syntheticparksfeatures.Forestcover(thearea coveredbytrees)correlationwasnotevaluatedinLama Balice park, because the natural vegetation was populated with shrubs and not trees.ForestUrban forestAreaDistance fromcoverarea(ha)Codethe city (ha)Milano Parco NordMI1596,5716880,117Milano TrennoMI261689546,71Milano Bosco in cittMI349,8880038,628Milano SempioneMI451,2150326,912Milano Monte stellaMI538,6525615,858Milano MontanelliMI619,4142410,54Parco RavizzaMI77,818123,284Milano CaveMI8119,1703237,042Parco SolariMI95,619512,122Milano ForlaniniMI1059,7557231,834Giardini Via PallavicinoMI116,223962,352Milano LambroMI1271,7577438,539Parco Trotter di TurroMI1313,143066,967Bari Umberto 1BA11,80,10,27Bari 2 giugnoBA2420001Bari Lama BaliceBA31197500N.A.Table2.Numberofbirdspeciesidentiedandnumberof specimens detected in each greenspace.Green spacesCodeN of species N of specimensMilano Parco NordMI1381378Milano TrennoMI218193Milano Bosco in cittMI332244Milano SempioneMI419397Milano Monte stellaMI519206Milano MontanelliMI61275Parco RavizzaMI7640Milano CaveMI834379Parco SolariMI91278Milano ForlaniniMI1022276Giardini Via PallavicinoMI111039Milano LambroMI1226227Parco Trotter di TurroMI13855Bari Umberto 1BA18402Bari 2 giugnoBA211125Bari Lama BaliceBA316122Sanesi et al.: Avian Ecological Diversity 2009 International Society of Arboriculture82lands and hedgerows (Chamberlain and Fuller 2001; Gregory et al. 2001; Padoa-Schioppa 2006), such as: stonechat (Saxicola torquataLinnaeus1766);red-backedstrike(Laniuscollirio L.);melodiuswarbler(HippolaispoliglottaL.).Mostofthe remaining species are without specic requirements in terms of habitatandcouldbedenedasgeneralistspecies(Hagemeijer andBlair1997;Tomialoj,1998;Jedicke2000;Massaetal. 2004),suchas:feralpigeon.(Columbalivia,Gmelin,1789); hoodedcrow(Corvuscoronecornix,L.);starling(Sturnus vulgaris, L.); italian sparrow (Passer domesticus X italiane, L.).Waterbirdspecieswerealsoidentiedbecauseofthe presenceofpondsandarticiallakesinsomeoftheana-lyzedgreenspaces(e.g.,ParcodelleCaveinMilan):little grebe(Tachybaptusrucollis);greatcrestedgrebe(Podic-escristatus);andlittlebittern(Ixobrychusminutus).All thesespecieshaveaninterestintermsofhabitatconserva-tioninurbanandperiurbanenvironments(Massaetal.2004).ThroughtheUPGMACluster Analysis,weclassiedthe16 greenspaces into 3 main clusters or groups (Figure 1), such as: (1) the three largest greenspaces of Milan (Parco Nord, Parco delle Cave,BoscoinCitt);(2)thethreegreenspacesinBari(Lama Balice,Parco2Giugno,GiardinidiPiazzaUmberto);and(3) the remaining 10 greenspaces in Milan (Milano Trenno, Milano Sempione,MilanoMonteStella,MilanoMontanelli,ParcoRa-vizza,ParcoSolari,MilanoForlanini,Giardini ViaPallavicino, MilanoLambro).Theseclustersofgreenspaces(inter-group) showedsimilarcharacteristicsinsidethegroup(intra-group).Figure2illustratestheresultsoftheregressionanaly-siswhichconsideredthemaincharacteristicsofurbangreen-spacesasindependentvariables,andspeciesrichnessasde-pendentvariable(expressedasnumberofbirdspecies).A highcorrelationemergedbetweenspeciesrichnessand distancefromthecityandbetweenspeciesrichnessand amountofforesttreecover.Thesendingsareconsis-tentwithotherstudies,e.g.,Gilbert(1989),Jokimki(1999), Hostetler and Holling (2000), Melles et al. (2003), Blair (2004).Figure 3 (Mann-Whitney U-test) illustrates the levels of abun-dance for the two indicator species (great tit and serin), based on DBHvalues(minimum,rstquarter,median,thirdquarterand maximum). In the case of serin, when DBHmin > 8 cm; DBH1st quarter > 20 cm; DBHmedian > 30 cm; DBH3rd quarter > 40 cm, species abundancegetssignicantlyhigherthantheonemeasuredat lower level of DBH (see: Mann-Whitnay U-test, in Figure 3). In the case of the great tit, DBHmax was the only interval providing signicantresults. Theresultingregressioncurveforthegreat titrevealedapositivecorrelationbetweenDBHandspecies abundance: the higher the tree diameter the higher the abundance of the species. This could be explained by the habitat preference of the great tit for large trees (Cowie and Hinsley 1988). The re-gression curves predicting the mimimal and optimal distribution of DBH for great tit and serin are reported in Figure 4. Such equa-tions could be used to design an ideal structural model of forest stands in urban environments supporting avian species diversity. Figure 1. Cluster analysis. See Table 1 for greenspaces names. Figure2.Spearmancorrelationcoefcientandregressionanal-ysisfornumberofspeciesandareaofthegreenspace.Forest cover is the area covered by trees.Arboriculture & Urban Forestry 35(2): March 20092009 International Society of Arboriculture83DISCUSSION AND CONCLUSIONSInurbansettings,birdspeciesareimportantindicatorsof environmentalqualityandecologicalfunctionality.Atur-banscale,thestudyofbirdspeciesinrelationtogreenspac-escharacteristicsisessentialtobetterunderstandthecur-rentstatusofurbanforestresourcesandrelatedfunctionsas wellastomonitorprogressestowardsurbansustainability.Inthisstudy,weprovidedevidenceontheresponseofbird speciestocertainstructuralattributesofgreenspaces,such asthepresenceofmatureandheterogeneousforeststands (highlevelofDBH).Amongtheanalyzedgreenspaces,Par-coNord(Milan)providedthemostencouragingresultsin termsofspeciesrichness.Suchresultscouldbeexplained by:thelargeextensioncoveredbythisgreenspace(approxi-mately600ha),thehighpercentageofmatureforesttrees, andtherelevantdistancetocitycenter(Sanesietal.2007). Besidesthesecharacteristics,itisimportanttoconsiderthe spatialconnectivityofgreenspaceswiththesurroundingland-scapecomponents,especiallyforestpatches,openspaces, grasslandsandmixed-croplandswithpresenceofhedgerows (Sodhietal.1999;Farina2006).Forexample,Giardinodivia Pallavicino,ParcoSolariandGiardinodiviaRavizzainMilan althoughhavingapproximatelythesameextension(16ha)re-vealedacontrastingpatternsintermsofspeciesrichness(see Table3).ThiscouldbeexplainedbythefactthatGiardinodi via Pallavicino and Parco Solari belong to a system of parks and othergreenspaces(publicandprivatelands)whichconstitutes akindofecologicalnetworksupportingbirdspeciesdispersal.Insynthesis,thisstudyprovidedthefollowingcaveats:1) The dimension of greenspaces and the amount of tree cover are critical factors supporting avian ecological diversity in urban environments. As a consequence, urban forest plan-nersandmanagersshouldpromotetheplanningandde-sign of large greenspaces within cities and the connection ofgreenspaceswiththesurroundinglandscapeelements. 2)Thestructuralheterogeneityofforesttreeswithingreen-spaces (explained by the DBH analysis) is a fundamental aspect supporting high level of species abundance of birds.3) The conservation of species diversity in urban areas should be based on the knowledge on one or more indicators species having different habitat requirements in terms of vegetation and trees structure (as explained by Ficetola et al. 2007). The results of our work suggests that following the approach of ecosystem services and the Biophilia hypothesis (Costanza etal.1997;Wilson1984)agreenspaceinurbanareasshould bemanagedforbothsocialneedsandconservationpurposes.Acknowledgments.TheresearchwasnancedbyMinistryoftheIn-struction of the University and the Research inside Program of Research of Interest National (PRIN-2004). 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Ecological Research 19:209216.Giovanni SanesiUniversit degli Studi di BariDipartimento di Scienze delle Produzioni Vegetalivia amendola 165/a-70126Bari, ItalyEmilio Padoa-Schioppa (Corresponding Author)Universit degli Studi di Milano-BicoccaDipartimento di Scienze dellAmbiente e del TerritorioResearch Unit of Landscape Ecologypiazza della Scienza 1-20126Milano, [email protected] LafortezzaUniversit degli Studi di BariDipartimento di Scienze delle Produzioni Vegetalivia amendola 165/a-70126Bari, ItalyLeonardo LorussoUniversit degli Studi di BariDipartimento di Scienze delle Produzioni Vegetalivia amendola 165/a-70126Bari, ItalyLuciana BottoniUniversit degli Studi di Milano-BicoccaDipartimento di Scienze dellAmbiente e del TerritorioResearch Unit of Landscape Ecologypiazza della Scienza 1-20126Milano, ItalySanesi et al.: Avian Ecological Diversity 2009 International Society of Arboriculture86Quantizierung des Vorkommens und der Diversitt vorgenommen. Die ErgebnissezeigeneinepositiveKorrelationzwischenGrnzonenmit mehr vielfltigem und lterem Baumbestand und der Anzahl an Vgeln und Vogelarten, die in diesen Studien beobachtet wurden. Eine positive KorrelationbestehtauchzwischenderEntfernungzumStadtzentrum und der Vielfalt der Vogelarten. Zum Schluss diskutieren wir einige der wichtigsten Implikationen fr die Frderung funktioneller Attribute von Grnzonen durch Einbeziehung von Informationen ber Vogelkologie, umzueinerkologischsinnvollePlanungundGestaltunginurbanen Rumen zu kommen.Resumen.Losbosquesylosrbolesdelosespaciosverdescon-tribuyen a un sinnmero de funciones ecolgicas en ambientes urbanos, talescomolasobrevivenciadeespeciesendmicas(porej.especiesde aves). Este trabajo analiza las relaciones entre caractersticas de los espa-cios verdes (atributos estructurales y espaciales) y la diversidad ecolgica deespeciesaviarias.Estainvestigacinprovienededosestudiosreal-izadosenItalia.Conelusodelmtododeconteopuntualsehizouna cuanticacindelaabundanciaydiversidaddeespeciesdeavesenun nmero de espacios verdes con diferentes atributos estructurales (tipo de vegetacin, altura de los rboles) y caractersticas espaciales (localidad, conectividad). Los resultados mostraron correlaciones positivas entre los espaciosverdesconlavegetacindelbosquemaduroyelnmerode especmenesyespeciesobservadasenlosdosestudios.Aparecetam-bin una correlacin positiva entre la distancia al centro de la ciudad y la riqueza y abundancia de especies de aves. Finalmente, discutimos algu-nas de las principales implicaciones para realzar los atributos funcionales delosespaciosverdes,conelusodeindicadoresecolgicosaviarios para informar ecolgicamente a la planeacin y el diseo urbano. Rsum. Les espaces verts ainsi que les arbres forestiers, de par leurs fonctions environnementales, contribuent lenvironnement urbain telles qulasurviedespcesdanslhabitaturbain(ex.:espcesdoiseaux). Cetarticleanalyselarelationentrecaractristiquesdesespacesverts (attributs structuraux et spatiaux) avec la diversit cologique en espc-esaviaires.Cesdcouvertesderechercheproviennentdedeuxtudes menes en Italie. Au moyen de la mthode des points cots, une quanti-cation a t faite de labondance et de la diversit en espces doiseaux au sein dun certain nombre despaces verts qui ont des attributs structuraux (ex.: type de vgtation, hauteur des arbres) et spatiaux (ex.: localisation, connectivit) diffrents. Les rsultats montrent des corrlations positives entre les espaces verts avec une vgtation forestire plus diversie et mature par rapport au nombre de spcimens et despces observes dans les deux tudes.Une corrlation positive est apparu galement entre la distance avec le centre de la ville et la richesse ainsi que labondance en espces doiseaux. Finalement, on y discute des applications principales pour amliorer les attributs fonctionnels des espaces verts en utilisant des indicateurs cologiques aviaires pour crer un design et une planication cologique urbaine plus pratique.Zusammenfassung.GrnzonenundBumeleistenihrenBeitrag zumFunktioniereneinerstdtischenUmwelt,zumBeispielzumber-lebenstadtbewohnender Vogelarten.DieseStudieanalysiertdieBezie-hungen zwischen Grnzonen-Charakteristika (strukturelle und rumliche Attribute)undder Vielzahlan Vogelarten.DievorgestelltenForschun-gsergebnissekommenauszweiStudien,dieinItaliendurchgefhrt wurden.Ineiner AnzahlvonGrnzonenmitverschiedenenstrukturel-len(z.B. Vegetationstyp,Baumhhe)undrumlichen Attributen(z.B. Standort,Verbindungen)wurdendurchdiePunkt-Zhl-Methodeeine
