Research Article Quantifying Effects of Spatial …downloads.hindawi.com/journals/ijbd/2013/914837.pdfQuantifying Effects of Spatial Heterogeneity of Farmlands on Bird Species Richness

Hindawi Publishing CorporationInternational Journal of BiodiversityVolume 2013 Article ID 914837 9 pageshttpdxdoiorg1011552013914837

Research ArticleQuantifying Effects of Spatial Heterogeneity of Farmlands onBird Species Richness by Means of Similarity Index Pairwise

Federico Morelli

DiSTeVA University of Urbino Scientific Campus 61029 Urbino Italy

Correspondence should be addressed to Federico Morelli morelliusliberoit

Received 6 March 2013 Revised 30 April 2013 Accepted 10 May 2013

Academic Editor Antonio Terlizzi

Copyright copy 2013 Federico Morelli This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Many studies have shown how intensification of farming is the main cause of loss biodiversity in these environments During thelast decades agroecosystems in Europe have changed drastically mainly due to mechanization of agriculture In this work speciesrichness in bird communities was examined on a gradient of spatial heterogeneity of farmlands in order to quantify its effectsFour categories of farmland spatial heterogeneity were defined based on landscape and landuse parametersThe impact of featuresincreasing the spatial heterogeneitywas quantified comparing the similarity indexes between bird communities in several farmlandsof Central Italy The effects of environmental variables on bird richness were analyzed using GLM The results highlighted thatlandscape features surrogates of high nature values (HNVs) of farmlands can increase more than 50 the bird species richnessThe features more related to bird richness were hedgerows scattered shrubs uncultivated patches and powerlines The resultsconfirm that the approach based on HNV for evaluating the farmlands is also suitable in order to study birdsrsquo diversity Howeversome species are more sensitive to heterogeneity while other species occupy mainly homogeneous farmlands As a consequencedifferent conservation methods must be considered for each farmland bird species

1 Introduction

Agricultural intensification is one of the main drivers ofbiodiversity decline During the last twenty-five years a rapidand large scale change of the agricultural landscape occurredin Europe caused by the intensification andmechanization ofagricultural activities [1 2] and for this reason understandingthe relations between biodiversity and land-use intensityis quite important to developed effective plans for habitatconservation [3] Many studies about biodiversity in agroe-cosystems usually faced the problem that both managementtype and landscapes features can affect it [4ndash6] but aquantification of the real impact of each of these factorson the composition of animal communities is complicatedBiodiversity in farmlands is affected by land-usemanagementat a small spatial scale (grazing intensity or crop rotation)and also at a large spatial scale [3] All of this is related tothe presence andor distribution of landscape features thatmay reflect a low fragmentation of the habitat which is oftencalled ldquofunctional heterogeneityrdquo and is very important insupporting biodiversity [7ndash11]

Many studies have shown that organic systems mayenhance bird species diversity over nonorganic counterpartsas a result of increased complexity in landscape features [1213] because in ecology the habitat diversity is associated withan increase of niche availability for the species [14] Mainlyfor this reason farmers are increasingly being encouraged toconserve biodiversity through the maintenance of extensivefarming systems the preservation of seminatural landscapefeatures or the extension of intensive farming systems [1516] However at the moment most of our knowledge ofagricultural practices and farmland bird ecology comes froma few countries only with 76 of papers in theWeb of Scienceoutsourcing from the UK France the Netherlands SpainGermany and Sweden and less than 10 from Central andEastern European countries [17]The results of many of theseworks show that the correlation between biodiversity andagricultural heterogeneity varies from positive to negative indifferent systems in Europe [9 18 19]

The spatial heterogeneity in an agroecosystems ismeasur-able through landscape features that can be used also to assessbird species richness as a surrogate of biodiversity [20]

2 International Journal of Biodiversity

The first aim of the present study is examining therelationships between bird species richness and spatial het-erogeneity of farmlands in Central Italy and quantifying theimpact of spatial heterogeneity on biodiversity through theuse of an index easy to apply and useful for conservationstrategies

The second aim is identifying the main environmentalcharacteristics associatedwith the heterogeneity of farmlandsand investigating whether the species living in heterogeneousagricultural areas are also present also in more homogeneousfarmlands to help in this way to identify the bird speciesmostrelated to landscape heterogeneity as possible indicators ofHNV farmlands

2 Material and Methods

21 Study Area The study area was an agricultural area of theNorth Eastern Marches region (Central Italy 43∘451015840473010158401015840N12∘45101584052010158401015840E) that was 2500 ha wide ranged from 0 to800masl This area was selected because it includes farm-lands representative of the different farming practices in theregion Within the area 80 sites were selected randomly andsurveyed There sites were located uniformly and each far atleast 500m from one other

22 Species and Environmental Data To survey the birdcommunity composition during the breeding period of theyear 2010 the sites were visited in the morning within 0600AM and 1000 AM with sunny weather conditions betweenmid-April and the end of July Each visit lasted 10min andall birds detected visually and acoustically within a radius of100m from the observer were recorded [21] using single pointcounts Species not breeding and diurnal or nocturnal raptorswere excluded from subsequent analyses because sometimesthey require different survey methods Also occasional or notbreeding species were excluded from the statistical analysisbecause their presence was very rare and therefore did notaffect the total richness The only exception was Circuspygargus that was considered strongly related to the studiedhabitats [22 23] and then counted into bird richness butexcluded from the further environmental analysis becauseif compared with passeriform birds the species could beconsidered a wide-ranged species

Description in situ of the 3 ha (100m radius area) aroundthe point-count was made in order to quantify the land-usecomposition and the structural characteristics in the sam-pling sites and to obtain an updated information concerningcrop types The percentages of land-use composition esti-mated in situ were adjusted by checking aerial photographsand using a 100m radius buffer overlapped with ArcGIS 10in order to avoid the difficulties determinated by the exclusiveuse of digital maps to study limited environments [24] Alsoaltitude of the point count was recorded using a GPS

23 Spatial Heterogeneity of Farmlands In order to classifythe farmland heterogeneity an approach in line with thatrecently used for evaluating high nature value (HNV) farm-land in Europe [25ndash28] was used The presence and size

Table 1 Environmental parameters used to describe the farmlandsin Central Italy The spatial scale of measurement was 100m radiusaround a single point count

Parameters Abbreviation Level Details

Altitude alt Landscape Altitude of the pointcount (masl)

Terrain slope slo Landscape

No slope (less than 3degrees) 0 slight slope

(between 3 and 8degrees) 1 mean slope(greater than 8 degrees)

2

Roads roa LandscapePresence and type ofroads (paved and

unpaved)

Power lines pow Landscape Number of electricitywires

Urban urb Land-use Forest for Land-use Shrubs shr Land-use Uncultivated unc Land-use Badland bad Land-use Grassland gra Land-use Hedgerows hed Land-use Isolated trees tre Land-use Vineyards vin Land-use Olive oli Land-use Cultivated total cul Land-use Sum of all crop types Forage ofo Crop type Wheat whe Crop type Alfalfa alf Crop type Hay hay Crop type Sunflower sun Crop type Coriander cri Crop type Sugarbeet sug Crop type Corn cor Crop type Garlic gar Crop type Oats oat Crop type Brassica sp bra Crop type Lettuce let Crop type

of natural and seminatural farmland features (ie shrubsuncultivated patches) or linear features (ie field marginshedgerows) were analyzed since they could increase thenumber of ecological niches in which wildlife can coexistwith farming activities and create a heterogeneity gradientThe spatial features were analyzed at three different scalelevel landscape diversity land-use diversity and crop type(Table 1)

231 Landscape Diversity To define the landscape diversitythe following parameters were used

(1) road presence and type paved unpaved or mixed

(2) power lines presence and number

International Journal of Biodiversity 3

Table 2 Ranking of farmland spatial heterogeneity according to landscape and land-uses characteristics where FSH is farmland spatialheterogeneity

FSH description FSH rank Terrain slope Marginal vegetation Land-use diversityVery heterogeneous 4 None slight mean Linear + point gt10Heterogeneous 3 None slight mean Linear 08 lt 10Homogeneous 2 None slight mean Point 06 lt 08Very homogeneous 1 None slight None lt06

(3) terrain slope classified as no slope (less than 3degrees) 0 slight slope (between 3 and 8 degrees) 1and mean slope (greater than 8 degrees) 2

(4) marginal vegetation level on cultivated taking intoaccount the presence (isolated or simultaneous) ofnatural and semi-natural features max level (lin-ear features (hedgerows) + point features (scatteredshrubs)) mid-level (linear features (hedgerows)) lowlevel (point features (scattered shrubs)) and minlevel (without hedgerows and scattered shrubs) (seeFigure 1) The hedgerows were considered as a factorof greater level than scattered shrubs because in thestudy area they always resulted as larger features inrelative terms thus offering a greater edge effects onhabitat fragmentation The minimum radius size ofthe scattered shrubs considered in this study was 05meter The marginal vegetation is also used to definethe HNV of farmlands [27 28]

232 Land-Use Diversity The land-use diversity in each sitewas calculated using Shannon diversity index on land-uses1198671015840

= minussum119901119894times log119901

119894 where 119901

119894is the relative proportion of

each land-use type 119894 [30]This index can express the fragmen-tation of land-uses as more fragmented land-use types havelarger number of patches each of a smaller average sizewithinthe sampled area

233 Crop Type Crop diversity was estimated for each siteapplying the Shannon diversity index on crop types into thecultivated category (Table 1) However this feature was alsoanalyzed as another level of farmland heterogeneity becauseit appears in contrast compared to the land-use (the cropdiversity was greater when the land-use diversity was lowerbecause of being dominated by cultivated typology)

Four categories of spatial heterogeneity of farmlandwere defined considering both landscape and land-use datacollected in situ The sampled sites were ranked in relationto a decreasing spatial heterogeneity value as follows veryheterogeneous mosaic 4 heterogeneous mosaic 3 homoge-neousmosaic 2 and very homogeneousmosaic 1 (see detailsin Table 2) When a site could not be clearly categorized(considering all parameters in Table 2) it was classified in theclosest category

24 Data Analysis Biodiversity was estimated as bird speciesrichness at each sampled site and was estimated for eachfarmland heterogeneity level too Total biodiversity was thesum of all bird species recorded in the entire study area To

I II III IV

Figure 1 Scheme of the criteria used to classify the level of marginalvegetation of farmlands in Central ItalyThe point features representscattered shrubs while linear features represent hedgerows

test the effects of environmental parameters (associated withfarmland spatial heterogeneity) on biodiversity bird richnessin different spatial heterogeneity categories was comparedusing ANOVA (after doing the normality and homoscedas-ticity tests) Similarity between bird communities in differentheterogeneity categories was explored using the SorensenSimilarity IndexThe Sorensen similarity index (SI) [31] is a 120573diversity index that vary from 0 where the assemblages differtotally to 1 where they are identical (SI = 2119888(119886 + 119887) where119888 is the number of species shared by the two sites and 119886 and119887 are the total number of species at each site) The Sorensensimilarity index was calculated for pairwise comparisonsbetween different heterogeneity categories and also betweeneach of them and the total biodiversity This method wasused to quantify the differences on bird communities betweenspatial heterogeneity gradient

The nature and strength of the relationship between birdrichness and environmental parameters on farmlands wereexamined using GLM [32] with the dependent variable (birdrichness) modeled specifying Poisson errors Independentpredictive variables were expressed as arcsin square root inthe case of proportions In order to avoid multicolinearity ofland-use and crop types the parameters (regressors) showingthe strongest correlation (gt08) were manually eliminatedA stepwise backward procedure was carried out using alldata pooled in order to select the best predictors usingAIC criterion to select the lowest AIC values [33 34] Inmodels sites were treated as independent units becausethe values of spatial autocorrelation between geographicdistance and dissimilarity matrix of sites (obtained fromlandscapes variables) were low (Mantel test 119903 = 013119899 = 80 sites not significant) [35] Dissimilarity indicesamong sites were calculated by means of ldquovegdistrdquo functionof the vegan package [36] using five different landscapevariables (altitude urban roads hedgerows and cultivatedtotal) Internal validation of models was performed using abootstrap resampling procedure (119899 bootstrap = 999) All testswere performed with R program (RDevelopment Core Team2011)


3 Results

Sixty-six bird species were recorded during the breedingperiod For the analysis a total of 1133 records were collectedThe maximum potential bird richness for the studied farm-land was fifty-five species (Tables 3 and 5) considering thatwere excluded not-breeding species diurnal and nocturnalraptors

The most common farmland types had high or mediumspatial heterogeneity (over 73) whereas farmlands withlower heterogeneity were only 27 (Table 3) mainly dis-tributed near the coast in lowland zones Roads were presentin all farmlands The most common road type was paved(64) while unpaved roads were 20 andmixed (paved andunpaved) roads represented 16 of cases Power lines werewidespread in farmlands (90) and no differences in this ele-ment were found between different farmland heterogeneitylevels The differences in crop diversity across the gradient ofspatial heterogeneity were not significant (Table 4)

31 Effects of Spatial Heterogeneity on Bird Richness The birdspecies richness on different farmland spatial heterogeneitycategories was different being higher in farmlands withgreater heterogeneity (119865 378 df 3 119875 value 0000 Figure 2)Themost heterogeneous farmlands had a maximum richnessvalue of fifty-one species whereas in the most homogeneousfarmlands the maximum richness value was twenty-fivespecies

The impact of FSH on biodiversity was quantified bymeans of similarity index pairwise between the FSH cate-gories The homogenization of farmlands was able to reducethe similarity index on bird richness up to a half compared tovery heterogeneous farmlandsThe total effect was quantifiedas a fall of circa 53 of diversity in comparison with the totalamount of species and 40 between very heterogeneous andvery homogeneous farmlands (Table 5) On the other handthe difference between bird species in very heterogeneousareas and potential bird richness of farmlands was small only4

32 Parameters of Farmlands Useful to Explain Bird Distribu-tion Following the results of this work the linear featuresas hedgerows were more important than point features asshrubs for the total bird richness (more dissimilarities fromindex were found between 1 and 3 than between 1 and 2 FSHcategories) (Table 5)

The model that best described the relationships betweenbird species richness and environmental parameters in farm-lands included three land-use variables (shrubs uncultivatedand hedges) and one landscape variable (presence of power-lines) The ratio between explained and total deviance for thebest model was 083 These four parameters were statisticallysignificant for all the farmland typologies and if compared tothe initial model including all the variables the model withonly these four variables appeared to be the most suitableAltitude had not effect on bird diversity in the study areaThe results of backwise procedure have not selected altitudeas variable related to the bird species richness (Tables 6 and 7)

Num

ber o

f bird

spec

ies

Farmland spatial heterogeneity (FSH)

5

10

15

20

25

1 2 43

Figure 2 Relationship between bird species richness and gradientof spatial heterogeneity of farmlands in Central Italy

33 Bird Species Frequencies on Farmland Type The birdspeciesmost frequently observed in heterogeneous farmlandswere Sylvia atricapilla Turdus merula and Emberiza cirlusHowever the species present only in this category wereEmberiza cirlus and Emberiza calandra followed by the forestbirds Oriolus oriolus Troglodytes troglodytes and the raptorCircus pygargus all considered vulnerable species in theItalian Red List The only one endangered species recordedwas Jynx torquilla

The bird species most frequently observed in homo-geneous farmlands were Passer domesticus italiae Alaudaarvensis and Motacilla flava all considered vulnerablespecies in the Italian Red List (Table 3)

Some species such as Serinus serinus Carduelis chlorisand Emberiza hortulana were indistinctly present in farm-lands with different level of spatial heterogeneity

4 Discussion

The use of environmental variables collected in situ andadjusted by interpretation of aerial photographs could bemore accurate than only GIS analysis When computingseveral indexes of fragmentation and spatial heterogeneity onlandscapes (eg Fragstat and V-Late) the GIS tools workingover land cover maps are limited by the spatial resolutionof their maps For this reason they may not be accurateenough in order to quantify small objects as shrubs and shorthedges [11 24 37] Although the link between biodiversityand farming practices or landscape structural characteristicshas been underlined since the early nineties by Bennett et al[38] and Beaufoy et al [39] efforts in characterizing the highnatural value of farmland have been carried out morerecently [28 40ndash42] The HNV farmland concept has alsobeen embedded in the Common Agricultural Policy (CAP)ldquoto protect and enhance the EUrsquos natural resources andlandscapes in rural areas the resources devoted to axis 2


Table 3 Total frequency () relative frequency and concern status of bird species [29] in farmlands of Central Italy classified into differentspatial heterogeneity categories

Species FSH category Total Red List Italy4 (119899 = 30) 3 (119899 = 28) 2 (119899 = 14) 1 (119899 = 8)

Sylvia atricapilla 90 963 846 625 863 LCSerinus serinus 667 852 923 75 763 LCPasser domesticus italiae 633 741 923 100 738 VUTurdus merula 867 889 462 25 725 LCApus apus 70 778 846 50 713 LCLuscinia megarhynchos 767 667 538 125 613 LCCorvus cornix 767 778 231 25 613 LCHirundo rustica 567 63 538 100 613 NTEmberiza cirlus 80 667 154 0 55 LCFringilla coelebs 767 556 308 125 538 LCSturnus vulgaris 533 519 769 25 525 LCStreptopelia turtur 667 556 385 125 513 LCCarduelis carduelis 467 519 615 125 463 NTStreptopelia decaocto 40 519 462 25 425 LCCarduelis chloris 333 407 385 50 375 NTOriolus oriolus 633 37 0 0 363 LCAlauda arvensis 30 259 462 625 338 VUEmberiza hortulana 367 296 538 125 338 DDEmberiza calandra 50 296 231 0 325 LCCyanistes caeruleus 40 259 308 0 288 LCErithacus rubecula 30 37 77 0 25 LCParus major 267 333 154 125 25 LCGarrulus glandarius 433 222 0 0 238 LCTroglodytes troglodytes 30 333 0 0 225 LCSylvia communis 333 185 154 0 213 LCPhoenicurus phoenicurus 20 222 77 125 175 LCPica pica 20 222 77 125 175 LCLanius collurio 30 111 0 125 163 VUPhasianus colchicus 67 148 308 25 15 NASaxicola torquatus 233 111 77 0 138 VUCoturnix coturnix 133 148 77 125 125 DDSylvia cantillans 233 74 0 0 113 LCCisticola juncidis 10 37 154 25 10 LCLullula arborea 10 74 154 0 88 LCPasser montanus 0 111 154 125 75 VUCorvus monedula 10 37 77 0 63 LCDendrocopos minor 133 0 77 0 63 LCPicus viridis 10 74 0 0 63 LCColumba palumbus 67 74 0 0 5 LCDendrocopos major 10 37 0 0 5 LCMerops apiaster 67 37 77 0 5 LCRegulus ignicapillus 67 37 0 0 38 LCAegithalos caudatus 67 0 0 0 25 LCAlectoris rufa 67 0 0 0 25 DDCircus pygargus 33 37 0 0 25 VUColumba livia 33 37 0 0 25 DDMotacilla alba 33 37 0 0 25 LC


Table 3 Continued


Motacilla flava 0 0 0 25 25 VUPeriparus ater 67 0 0 0 25 LCPhoenicurus ochruros 33 37 0 0 25 LCCarduelis cannabina 0 37 0 0 13 NTEmberiza citrinella 33 0 0 0 13 LCJynx torquilla 33 0 0 0 13 ENMuscicapa striata 0 37 0 0 13 LCUpupa epops 33 0 0 0 13 LC

Table 4 Descriptive elements of agricultural mosaic along the gradient of spatial heterogeneity of farmland in Central Italy

Environmental parameter FSH category F df P value1 2 3 4 Total

Altitude (m) 1227 plusmn 772 1833 plusmn 1562 2988 plusmn 1682 3825 plusmn 1298 2924 plusmn 1688 101 3 0000lowastlowastlowast

Terrain slope (mode) Low Low Low Low-medium Low mdash mdash mdashRoads (mode) Paved Paved Paved Paved Paved mdash mdash mdashPowerlines (mean) 31 plusmn 25 29 plusmn 20 25 plusmn 16 38 plusmn 28 31 plusmn 23 15 3 0221Crop diversity (mean) 0632 plusmn 03 0554 plusmn 03 0533 plusmn 04 0489 plusmn 04 0530 plusmn 03 03 3 0790Significance codes lowastlowastlowastP lt 0001 lowastlowastP lt 001 lowastP lt 005 lsquoP lt 01

Table 5 Similarity index pairwise of the bird species richnessamong the farmlands according to their spatial heterogeneitygradient

FSH category Similarity index1 2 3 4 Total

1 mdash 0780 0667 0605 04722 mdash mdash 0815 0776 07643 mdash mdash mdash 0959 09224 mdash mdash mdash mdash 0962Number of bird species (total) 25 34 47 51 55

should contribute to three EU-level priority areas biodiver-sity and the preservation and development of HNV farmingand forestry systems and traditional agricultural landscapeswater and climate changerdquo (Communityrsquos Strategic Guide-lines for rural development 2007ndash2013 OJL5520 2006)TheHNV is characterized by three main criteria low intensityfarming presence of semi-natural vegetation (hedgerowsuncultivated shrubs etc) and diversity of land covermosaic

The results showed how in Central Italy bird richnessis related to spatial heterogeneity of farmlands highlightinghow the lack of several features such hedgerows or scatteredshrubs causes the loss of more than 53 of the total potentialbird species richness These findings point out the importantrole of these few marginal components typical of mostheterogeneous mosaics corresponding to HNV farmlandsThe results also show that diversity of land-use rather thancrop types seems to be important for bird species richnessin farmlands However because these two variables arecorrelated is hard determinate the real contribution of each

one Shannon index of crop types decreases with farmlandheterogeneity because diversity of crop types corresponds tomore extended and less complex farmlands from a structuralpoint of view The characteristics of farmlands seemingto support high numbers of bird species are hedgerowsscattered shrubs uncultivated patches and the presence ofpower lines The first three elements could improve the land-use diversity offering habitat availability to several species[7 9 43] Other studies underlined how electricity wires mayoffer useful perches and singing posts representing attractivestructures to insectivorous and to those birds hunting fromobservation posts like the Lanidae [44 45] Moreover apositive effect on bird detection may also be consideredHowever the same structures could be dangerous and causemortality by collision or electrocutions for several raptorsspecies that were excluded in this study [46 47] In ourstudy the absence of all these features and structural itemsis associated with a deep decrease of biodiversity

The comparison between similarities index provided aquantitative measure of the total influence of the spatialheterogeneity on bird community The approach by meanof Sorensen index can constitute an easy and fast decisionaltool useful to compare and quantify how a gradient ofurbanization can modify the biodiversity of ecosystems [48]The quantification of the impact of landscape or land-usefeatures on the biodiversity can constitute a useful tool forconservation planning landscape restoring and for main-taining HNV farmlands

The results of this work can be useful to select themost important environmental parameters to maintain thebiodiversity and to characterize the bird communities orthe presence of threatened species on different farmlandtypes tooThe bird species frequencies on farmland types are


Table 6 Different candidate models ranked according to the AIC values used to select the best models to relate bird richness to landscapeland-use and crop types in farmlands of Central Italy

Variables included in the model Total number of variables Scale level AICAlt + slo + pow + shr + for + unc + bad + gra + hed + tre +urb + cul + ofo + whe + alf + hay + sun + cri + sug + cor +gar + oat + bra + let + land-use div

25 Landscape land-use crop type 42453

Alt + slo + pow + shr + for + unc + bad + gra + hed + tre +urb + cul 12 Landscape land-use 42973

Alt + pow + shr + unc + bad + gra + hed + urb 8 Landscape land-use 42251Pow + shr + unc + hed 4 Landscape land-use 41731

Table 7 Results of Poisson regression for the best model relatingthe bird species richness to environmental parameters of farmlandsin Central Italy The table shows the most significant variablesselected after a stepwise backward procedure using AIC criterionA comparison of models with all possible variables classified in thefour different categories of spatial heterogeneity showed that thesignificant parameters are the same for all the evaluated levels

Environmentalparameter Estimate SE Z value P-values

Farmlands(119899 = 80)Powerlines 002805 001242 2257 00240lowast

Shrubs 123966 050681 2446 00144lowast

Uncultivated 094663 053777 1760 00784Hedgerows 151644 033585 4515 633119890 minus 06

lowastlowastlowast

Intercept 221632 009018 24576 2119890 minus 16lowastlowastlowast

Significance codes lowastlowastlowastP lt 0001 lowastlowastP lt 001 lowastP lt 005 lsquoP lt 01

useful to develop any bioindicator approach (farmland birdindexmonitoring ofHNV farmlands farmland focal speciesetc) For example Italian Sparrow in decreasing throughoutthe whole Italian peninsula [49] was present mainly inhomogeneous farmlands almost twice times if comparedto the only 11 records from more heterogeneous fields TheOrtolan Bunting that is considered in decline in Europe[50ndash54] did not show preferences between homogeneous orheterogeneous farmlands The Western Yellow Wagtail waspresent only in farmlands with less spatial heterogeneityand completely absent in more heterogeneous fields On theother hand some species only occur in very heterogeneousfarmlands and could be targeted as good indicators ofbiodiversity in farmlands in the sense of the ldquofocal speciesrdquoapproach [55] Two typical farmland birds mainly present inmore heterogeneous farmlands were the Cirl Bunting and theCorn Bunting (Table 3)

Finally our results help filling the lack of data aboutfarmland bird ecology in southern Europe [17] and sug-gest the necessity of coordinating the management actionsestablished by conservations plans and the different farm-lands involved possibly through an agricultural policy ona regional scale according to the guidelines of detailed EUrural policiesThe importance found for several features suchas linear hedgerows can suggest conservation policies as thecreation and maintenance of hedges field margins retention

of uncropped areas or the use of intercropping cultures inthe fields this way we can increase the spatial heterogeneityand help to enhancing thus favoring the settlement of severalconcern bird species [9 29 56] Furthermore the impor-tance of using species-specific strategies for maintainingand preserving the structure and the functionality of agro-ecosystems is highlighted as the necessity of more localscale studies from the applied point of view consideringthat currently the farmland environment in Central-EasternEurope is generallymore extensive andmore complex than inWestern Europe and this fact generates different biodiversityconditions in agricultural areas [57]

Acknowledgments

The author is very grateful to the following people DanChamberlain Jon Mc Kean Marco Girardello RaffaeleSecchi Maria Balsamo Yanina Benedetti and anonymousreviewers for their suggestions or valuable comments onearlier versions of the manuscript or in the field He alsothanks ION Proofreading for the critical revision of Englishversion of the paper

References

[1] D E Chamberlain R J Fuller R G H Bunce J C DuckworthandM Shrubb ldquoChanges in the abundance of farmland birds inrelation to the timing of agricultural intensification in EnglandandWalesrdquo Journal of Applied Ecology vol 37 no 5 pp 771ndash7882000

[2] P F Donald R E Green and M F Heath ldquoAgriculturalintensification and the collapse of Europersquos farmland birdpopulationsrdquo Proceedings of the Royal Society B vol 268 no1462 pp 25ndash29 2001

[3] D Kleijn F Kohler A Baldi et al ldquoOn the relationship betweenfarmland biodiversity and land-use intensity in Europerdquo Pro-ceedings of the Royal Society B vol 276 no 1658 pp 903ndash9092009

[4] A C Weibull O Ostman and A Granqvist ldquoSpecies richnessin agroecosystems the effect of landscape habitat and farmmanagementrdquo Biodiversity and Conservation vol 12 no 7 pp1335ndash1355 2003

[5] G M Siriwardena H Q P Crick S R Baillie and J DWilson ldquoAgricultural land-use and the spatial distribution ofgranivorous lowland farmland birdsrdquo Ecography vol 23 no 6pp 702ndash719 2000


[6] J R Krebs J DWilson R B Bradbury and GM SiriwardenaldquoThe second silent springrdquo Nature vol 400 no 6745 pp 611ndash612 1999

[7] H J W Vermeulen ldquoCorridor function of a road verge fordispersal of stenotopic heathland ground beetles CarabidaerdquoBiological Conservation vol 69 no 3 pp 339ndash349 1994

[8] J Hoffmann and J M Greef ldquoMosaic indicatorsmdashtheoreticalapproach for the development of indicators for species diversityin agricultural landscapesrdquo Agriculture Ecosystems and Envi-ronment vol 98 no 1-3 pp 387ndash394 2003

[9] T G Benton J A Vickery and J D Wilson ldquoFarmlandbiodiversity is habitat heterogeneity the keyrdquoTrends in Ecologyand Evolution vol 18 no 4 pp 182ndash188 2003

[10] F Morelli ldquoImportance of road proximity for the nest site selec-tion of the Red-backed shrike Lanius collurio in an agriculturalenvironment inCentral Italyrdquo Journal ofMediterranean Ecologypp 21ndash29 2011

[11] F Morelli R Santolini and D Sisti ldquoBreeding habitat of Red-backed Shrike Lanius collurio on farmland hilly areas of CentralItaly is functional heterogeneity an important keyrdquo EthologyEcology amp Evolution vol 24 pp 127ndash139 2012

[12] L Norton P Johnson A Joys et al ldquoConsequences of organicand non-organic farming practices for field farm and landscapecomplexityrdquo Agriculture Ecosystems and Environment vol 129no 1-3 pp 221ndash227 2009

[13] N A Beecher R J Johnson J R Brandle R M Case andL J Young ldquoAgroecology of birds in organic and nonorganicfarmlandrdquo Conservation Biology vol 16 no 6 pp 1620ndash16312002

[14] Y Kisel L Mcinnes N H Toomey and C D L Orme ldquoHowdiversification rates and diversity limits combine to create large-scale species-area relationshipsrdquo Philosophical Transactions ofthe Royal Society B vol 366 no 1577 pp 2514ndash2525 2011

[15] D J Pain and M W Pienkowski Eds Birds and Farming inEuropeThe Common Agricultural Policy and Its Implications forBird Conservation Academic Press SanDiego Calif USA 1997

[16] D Kleijn and W J Sutherland ldquoHow effective are Europeanagri-environment schemes in conserving and promoting biodi-versityrdquo Journal of Applied Ecology vol 40 no 6 pp 947ndash9692003

[17] A Baldi and P Batary ldquoSpatial heterogeneity and farmlandbirds different perspectives in Western and Eastern EuroperdquoIbis vol 153 no 4 pp 875ndash876 2011

[18] P Batary A Baldi and S Erdos ldquoGrassland versus non-grassland bird abundance and diversity in managed grasslandslocal landscape and regional scale effectsrdquo Biodiversity andConservation vol 16 no 4 pp 871ndash881 2007

[19] P Batary J Fischer A Baldi T O Crist and T TscharntkeldquoDoes habitat heterogeneity increase farmland biodiversityrdquoFrontiers in Ecology and the Environment vol 9 no 3 pp 152ndash153 2011

[20] R Barbault La Biodiversite Introduction a la Biologie de laConservation Collection les Fondamentaux Hachette ParisFrance 1997

[21] C J BibbyND Burgess andDAHillBirdCensus TechniquesAcademic Press London UK 1997

[22] R ClarkeMontagursquos Harrier Arlequin Press Chelmsford UK1996

[23] B Arroyo J T Garcıa and V Bretagnolle ldquoConservation ofthe Montagursquos harrier (Circus pygargus) in agricultural areasrdquoAnimal Conservation vol 5 no 4 pp 283ndash290 2002

[24] M Brambilla F Casale V Bergero et al ldquoGIS-models workwell but are not enough habitat preferences of Lanius collurioat multiple levels and conservation implicationsrdquo BiologicalConservation vol 142 no 10 pp 2033ndash2042 2009

[25] D Baldock G Beaufoy G Bennett and J Clark NatureConservation and New Directions in the Common AgriculturalPolicy Institute for European Environmental Policy LondonUK 1993

[26] E M Bignal and D I McCracken ldquoLow-intensity farmingsystems in the conservation of the countrysiderdquo Journal ofApplied Ecology vol 33 no 3 pp 413ndash424 1996

[27] E Andersen D Baldock H Bennett et al ldquoDeveloping a HighNature Value Farming area indicatorrdquo Report for the EuropeanEnvironment Agency Copenhagen Denmark 2003 httpwwwieepeuassets646Developing HNV indicatorpdf

[28] P Pointereau M L Paracchini J-M Terres F Jiguet Y Basand K Biala ldquoIdentification of high nature value farmlandin France through statistical information and farm practicesurveysrdquo Report EUR 22786 EN Office for Official Publicationsof the European Communities Brussels Luxembourg 2007

[29] V Peronace J G Cecere M Gustin and C Rondinini ldquoListaRossa 2011 degli uccelli nidificanti in Italiardquo Avocetta vol 36pp 11ndash58 2012

[30] P F Donald and C Forrest ldquoThe effects of agricultural changeon population size of corn buntings Miliaria calandra onindividual farmsrdquo Bird Study vol 42 no 3 pp 205ndash215 1995

[31] R H G Jongman C J F ter Braak and O F R TongerenDataAnalysis in Community and Landscape Ecology CambridgeUniversity Press Cambridge UK 1995

[32] P McCullagh and J A Nelder Generalized Linear ModelsChapman and Hall London UK 1989

[33] H Akaike ldquoA new look at the statistical model identificationrdquoIEEE Transactions on Automatic Control vol 19 no 6 pp 716ndash723 1974

[34] Anon S-PLUS 2000 Guide to Statistics vol 1 MathSoft SeattleWash USA 1999

[35] M G Betts A W Diamond G J Forbes M A Villard andJ S Gunn ldquoThe importance of spatial autocorrelation extentand resolution in predicting forest bird occurrencerdquo EcologicalModelling vol 191 no 2 pp 197ndash224 2006

[36] J Oksanen F G Blanchet R Kindt et al ldquovegan Com-munity Ecology Package R package version 20-6rdquo 2013httpCRANR-projectorgpackage=vegan

[37] F Morelli ldquoPlasticity of habitat selection by red-backed shrikesLanius collurio breeding in different landscapesrdquo The WilsonJournal of Ornithology vol 124 pp 52ndash57 2012

[38] A F Bennett J Q Radford and A Haslem ldquoProperties of landmosaics implications for nature conservation in agriculturalenvironmentsrdquo Biological Conservation vol 133 no 2 pp 250ndash264 2006

[39] G BeaufoyD Baldock and J ClarkTheNature of Farming LowIntensity Farming Systems in Nine European Countries Institutefor European Environmental Policy London UK 1994

[40] EENRDEC ldquoGuidance document The application of theHigh Nature Value impact indicator European Commu-nitiesrdquo 2009 httpeceuropaeuagriculturerurdevevalhnvguidance enpdf

[41] M L Paracchini J-M Terres E Petersen et al ldquoHigh naturevalue farmland in Europe An estimate of the distributionpatterns on the basis of land cover and biodiversity dataEuropean Commission Joint Research Centre Institute for


Environment and Sustainabilityrdquo Report EUR 23480 EN Officefor Official Publications of the European Communities Brus-sels Luxembourg 2008

[42] European Environment Agency ldquoHigh nature value farmlandcharacteristics trends and policy challengesrdquo EEA Report No12004 Copenhagen Denmark 2004

[43] H J W Vermeulen and P F M Opdam ldquoEffectiveness of road-side verges as dispersal corridors for small ground-dwellinganimals a simulation studyrdquo Landscape and Urban Planningvol 31 no 1ndash3 pp 233ndash248 1995

[44] A Bechet P Isenmann and R Gaudin ldquoNest predationtemporal and spatial breeding strategy in the Woodchat ShrikeLanius senator in Mediterranean Francerdquo Acta Oecologica vol19 no 1 pp 81ndash87 1998

[45] N Lefranc Les Pies-grieches drsquoEuropa drsquoAfrique du nord etdu moyen-Orient Delachaux et Niestle SA Lausanne ParisFrance 1993

[46] R E Harness and K R Wilson ldquoElectric-utility structuresassociated with raptor electrocutions in rural areasrdquo WildlifeSociety Bulletin vol 29 no 2 pp 612ndash623 2001

[47] K Bevanger ldquoBiological and conservation aspects of birdmortality caused by electricity power lines a reviewrdquo BiologicalConservation vol 86 no 1 pp 67ndash76 1998

[48] P Clergeau S Croci J Jokimaki M L Kaisanlahti-Jokimakiand M Dinetti ldquoAvifauna homogenisation by urbanisationanalysis at different European latitudesrdquo Biological Conserva-tion vol 127 no 3 pp 336ndash344 2006

[49] L Fornasari E de Carli L Buvoli et al ldquoSecondo bollettino delprogetto MITO2000 valutazioni metodologiche per il calcolodelle variazioni interannualirdquoAvocetta vol 28 pp 59ndash76 2004

[50] S Dale ldquoCauses of population decline of the Ortolan Buntingin Norwayrdquo in Bunting Studies in Europe P TryjanowskiT S Osiejuk and M Kupczyk Eds pp 33ndash41 BoguckiWydawnictwo Naukowe Poznan Poland 2001

[51] P F Donald F J Sanderson I J Burfield and F P Jvan Bommel ldquoFurther evidence of continent-wide impacts ofagricultural intensification on European farmland birds 1990ndash2000rdquo Agriculture Ecosystems and Environment vol 116 no 3-4 pp 189ndash196 2006

[52] F Morelli ldquoCorrelations between landscape features and croptype and the occurrence of the Ortolan Bunting Emberizahortulana in farmlands of Central Italyrdquo Ornis Fennica vol 89pp 264ndash272 2012

[53] I Newton ldquoThe recent declines of farmland bird populations inBritain an appraisal of causal factors and conservation actionsrdquoIbis vol 146 no 4 pp 579ndash600 2004

[54] G M Tucker and M F Heath Birds in Europe Their Con-servation Status BirdLife Conservation Series no 3 BirdLifeInternational Cambridge UK 1994

[55] R J Lambeck ldquoFocal species a multi-species umbrella fornature conservationrdquo Conservation Biology vol 11 no 4 pp849ndash856 1997

[56] M J Whittingham and K L Evans ldquoThe effects of habitatstructure on predation risk of birds in agricultural landscapesrdquoIbis vol 146 no 2 pp 210ndash220 2004

[57] P Tryjanowski T Hartel A Baldi et al ldquoConservation of farm-land birds faces different challenges in Western and Central-Eastern EuroperdquoActa Ornithologica vol 46 no 1 pp 1ndash12 2011

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


The first aim of the present study is examining therelationships between bird species richness and spatial het-erogeneity of farmlands in Central Italy and quantifying theimpact of spatial heterogeneity on biodiversity through theuse of an index easy to apply and useful for conservationstrategies

The second aim is identifying the main environmentalcharacteristics associatedwith the heterogeneity of farmlandsand investigating whether the species living in heterogeneousagricultural areas are also present also in more homogeneousfarmlands to help in this way to identify the bird speciesmostrelated to landscape heterogeneity as possible indicators ofHNV farmlands

2 Material and Methods

21 Study Area The study area was an agricultural area of theNorth Eastern Marches region (Central Italy 43∘451015840473010158401015840N12∘45101584052010158401015840E) that was 2500 ha wide ranged from 0 to800masl This area was selected because it includes farm-lands representative of the different farming practices in theregion Within the area 80 sites were selected randomly andsurveyed There sites were located uniformly and each far atleast 500m from one other

22 Species and Environmental Data To survey the birdcommunity composition during the breeding period of theyear 2010 the sites were visited in the morning within 0600AM and 1000 AM with sunny weather conditions betweenmid-April and the end of July Each visit lasted 10min andall birds detected visually and acoustically within a radius of100m from the observer were recorded [21] using single pointcounts Species not breeding and diurnal or nocturnal raptorswere excluded from subsequent analyses because sometimesthey require different survey methods Also occasional or notbreeding species were excluded from the statistical analysisbecause their presence was very rare and therefore did notaffect the total richness The only exception was Circuspygargus that was considered strongly related to the studiedhabitats [22 23] and then counted into bird richness butexcluded from the further environmental analysis becauseif compared with passeriform birds the species could beconsidered a wide-ranged species

Description in situ of the 3 ha (100m radius area) aroundthe point-count was made in order to quantify the land-usecomposition and the structural characteristics in the sam-pling sites and to obtain an updated information concerningcrop types The percentages of land-use composition esti-mated in situ were adjusted by checking aerial photographsand using a 100m radius buffer overlapped with ArcGIS 10in order to avoid the difficulties determinated by the exclusiveuse of digital maps to study limited environments [24] Alsoaltitude of the point count was recorded using a GPS

23 Spatial Heterogeneity of Farmlands In order to classifythe farmland heterogeneity an approach in line with thatrecently used for evaluating high nature value (HNV) farm-land in Europe [25ndash28] was used The presence and size

Table 1 Environmental parameters used to describe the farmlandsin Central Italy The spatial scale of measurement was 100m radiusaround a single point count

Parameters Abbreviation Level Details

Altitude alt Landscape Altitude of the pointcount (masl)

Terrain slope slo Landscape

No slope (less than 3degrees) 0 slight slope

(between 3 and 8degrees) 1 mean slope(greater than 8 degrees)

2

Roads roa LandscapePresence and type ofroads (paved and

unpaved)

Power lines pow Landscape Number of electricitywires

Urban urb Land-use Forest for Land-use Shrubs shr Land-use Uncultivated unc Land-use Badland bad Land-use Grassland gra Land-use Hedgerows hed Land-use Isolated trees tre Land-use Vineyards vin Land-use Olive oli Land-use Cultivated total cul Land-use Sum of all crop types Forage ofo Crop type Wheat whe Crop type Alfalfa alf Crop type Hay hay Crop type Sunflower sun Crop type Coriander cri Crop type Sugarbeet sug Crop type Corn cor Crop type Garlic gar Crop type Oats oat Crop type Brassica sp bra Crop type Lettuce let Crop type

of natural and seminatural farmland features (ie shrubsuncultivated patches) or linear features (ie field marginshedgerows) were analyzed since they could increase thenumber of ecological niches in which wildlife can coexistwith farming activities and create a heterogeneity gradientThe spatial features were analyzed at three different scalelevel landscape diversity land-use diversity and crop type(Table 1)

231 Landscape Diversity To define the landscape diversitythe following parameters were used

(1) road presence and type paved unpaved or mixed

(2) power lines presence and number








119894 where 119901






I II III IV





3 Results







Num

ber o

f bird

spec

ies


5

10

15

20

25

1 2 43





4 Discussion







Table 3 Continued
























Shrubs 123966 050681 2446 00144lowast


lowastlowastlowast






Acknowledgments


References




































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








119894 where 119901






I II III IV





3 Results







Num

ber o

f bird

spec

ies


5

10

15

20

25

1 2 43





4 Discussion







Table 3 Continued
























Shrubs 123966 050681 2446 00144lowast


lowastlowastlowast






Acknowledgments


References




































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


3 Results







Num

ber o

f bird

spec

ies


5

10

15

20

25

1 2 43





4 Discussion







Table 3 Continued
























Shrubs 123966 050681 2446 00144lowast


lowastlowastlowast






Acknowledgments


References




































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology






Table 3 Continued
























Shrubs 123966 050681 2446 00144lowast


lowastlowastlowast






Acknowledgments


References




































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table 3 Continued
























Shrubs 123966 050681 2446 00144lowast


lowastlowastlowast






Acknowledgments


References




































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology










Shrubs 123966 050681 2446 00144lowast


lowastlowastlowast






Acknowledgments


References




































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


























Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Documents

Research Article Quantifying Effects of Spatial …downloads.hindawi.com/journals/ijbd/2013/914837.pdfQuantifying Effects of Spatial Heterogeneity of Farmlands on Bird Species Richness