The value of forest strips for understorey birds in an Amazonian plantation landscape

17 Pages·2008·1 MB·English

ARTICLE IN PRESS
BIOLOGICAL CONSERVATION xxx (2008) xxx–xxx
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
The value of forest strips for understorey birds
in an Amazonian plantation landscape
Joseph Hawesa,*, Jos Barlowb,c, Toby A. Gardnera, Carlos A. Peresa
aSchoolofEnvironmentalSciences,UniversityofEastAnglia,NorwichNR47TJ,UK
bMuseuParaenseEm´ılioGoeldi(MPEG),Av.Perimetral1901,BairroTerraFirme,Bele´m,PA66077-530,Brazil
cSchoolofBiologicalScience,LancasterEnvironmentCentre,LancasterUniversity,LancasterLA14YW,UK
A R T I C L E I N F O A B S T R A C T
Articlehistory: Remnant forest strips are frequently proposed as valuable conservation tools in frag-
Received25November2007 mentedtropicallandscapes,yetwecurrentlylackevidencetoevaluatetheirpotentialcon-
Receivedinrevisedform servationvaluefornativebiota.Weexaminedthepotentialvaluefor understoreyforest
19June2008 birdsof30-year-oldriparianandterrafirme(unflooded)primaryforeststripswithinalarge
Accepted24June2008 silviculturallandscapeinthenorth-eastBrazilianAmazon,wherethematrixisdominated
by Eucalyptus plantations. We conducted mist-netting in eight foreststrips connected to
continuous forest (four of each forest type), with a total of 24 replicate sampling sites
Keywords: located near to (<1km), far from (2.5–9km), and within undisturbed forest controls (i.e.
Amazon 16 samples within the strips, and 8 in controls). Bird communities in both strip types
Brazil changed with increasing distance along forest remnants into the plantation matrix.
Countryside Matrix-embeddedsampleswerecharacterisedbyahigherrepresentationofbirdstypical
Fragmentation ofsecondarygrowthforestbutnotthosetypicaloftheEucalyptus-dominatedmatrix.While
Plantations thelong-termviabilityofthebirdpopulationsintheseremnantsremainsunclear,ourdata
Productionlandscapes demonstratethatforeststripscanprovideimportanthabitatformanybirdspeciesthatare
otherwiserarelyfoundoutsideprimaryforest.Foreststripsthereforeprovideanimportant
tooltoenhancebiodiversityconservationinplantationlandscapes.Therelativepractical
easewith whichthese areascan be selected and maintained means that theprotection
offoreststripsaspartofawiderconservationstrategyislikelytohaveparticularappeal
topolicymakersandlandscapemanagersworkinginthehuman-dominatedtropics.
(cid:2)2008ElsevierLtd.Allrightsreserved.
1. Introduction threat currently facing the future of tropical forest species,
leading to calls to prioritise the protection of large tracts of
Deforestationratesremainhighthroughoutthetropics,with remainingpristinehabitat(e.g.Peres,2005).However,beyond
Brazilian Amazonia recently experiencing the highest abso- acertainlevelofhabitatlossmanyfaunalgroupsalsorespond
lute rates in the world (INPE, 2006). The two main conse- negatively to fragmentation (Didham et al., 1996; Malcolm,
quences of deforestation, which are often mistaken as 1997; Laurance et al., 2002; Lees and Peres, 2006; Peres and
synonymous, are habitat loss and habitat fragmentation Michalski,2006),and as thearea ofland alreadyaffected by
(SchmiegelowandMo¨nkko¨nen,2002;Fahrig,2003;Lindenma- deforestation increases, the ‘megareserve’ approach will re-
yerandFischer,2007).Habitatlossisundoubtedlythegreatest quirecomplementaryconservationeffortsintheintervening
* Correspondingauthor:Tel.:[phone];fax:[phone].
E-mailaddresses:[email protected](J.Hawes),[email protected](J.Barlow),[email protected](T.A.Gardner),c.peres@
uea.ac.uk(C.A.Peres).
0006-3207/$-seefrontmatter (cid:2)2008ElsevierLtd.Allrightsreserved.
doi:10.1016/j.biocon.2008.06.017
Please cite this article in press as: Hawes, J. et al., The value of forest strips for understorey birds ..., Biol. Conserv. (2008),
doi:10.1016/j.biocon.2008.06.017
ARTICLE IN PRESS
2 BIOLOGICAL CONSERVATION xxx (2008) xxx–xxx
human-dominated ‘countryside’ (Barlow et al., 2007a; Daily Thepurposeofthisstudywastoaddressthecriticallack
et al., 2001; Hughes et al., 2002; Lindenmayer and Franklin, of knowledge regarding the potential value of forest strips
2002;Sekerciogluetal.,2002;Sekerciogluetal.,2007). inthetropicsbyexamining30-year-oldterrafirmeandripar-
Deforested areas in the tropics are usually characterised ianforeststripsinthenorth-eastBrazilianAmazon.Inpartic-
by high levels of fragmentation (e.g. Lees and Peres, 2006), ular, we examine the effects of forest strip type and length
andconservationeffortshavefocusedonenhancingtherep- (with any corresponding variations in local and landscape
resentationofnativebiotabothwithinremnantareasoffor- habitatstructure)onthepotentialconservationvalueofthese
est and the intervening landscape matrix. One persistently remnants.Todothisweexaminedpatternsofabundanceand
popular conservation strategy in human-dominated land- occupancyofbirdspeciesalreadyidentifiedascharacteristic
scapes has been the use of ‘wildlife corridors’ (Diamond, of continuous primary forest (very rarely found in planted
1975; Wilson and Willis, 1975), which are generally defined orregeneratingforest).Birdswereselectedasthefocaltaxon
as strips or areas of habitat specifically connecting two or because of their well-documented ecology (e.g. Stotz et al.,
more larger habitat blocks (Fahrig and Merriam, 1985; Beier 1996), and because they have been shown to be particularly
andNoss,1998)anddifferingfromtheland-usetypeoneither cost-effective to survey in tropical forests (Gardner et al.,
side(LindenmayerandFranklin,2002).Anothercommonfea- 2008).Furthermore,ourknowledgeofthesurroundingmatrix
ture of many agricultural production and plantation land- habitatsintheJarilandscapeandtheirrelativevalueforna-
scapes is the existence of forest strips (also termed ‘linear tiveforestbirds(Barlowetal.,2007b)offersaveryrareoppor-
forestremnants’:LimaandGascon,1999;LauranceandLau- tunitytocomparetheavifaunasampledinforeststripswith
rance,1999),whicharethinremnantsofforestoftenextend- thatwhichisknowntooccurinneighbouringcontinuousfor-
ingfromcontinuousprimaryforestintothematrixbutwhich, est. Specifically, we test the a priori hypotheses that (1) bird
unlike‘corridors’,donotnecessarilydirectlyconnecthabitat speciesrichnessandcommunitystructureinremnantforest
patches(Bennett,2003;Tayloretal.,2006).Theseforeststrips stripswillbeclearlydistinctfrombirdassemblagesincontin-
are particularly common features of degraded Amazonian uousprimaryforest,(2)birdspeciesrichnessandcommunity
landscapes.Forexample,theBrazilianForestCodelegallyre- structure will become more similar to the matrix avifauna
quires landowners to set aside 30–200m wide forest strips withincreasingdistancefromadjoiningareasofcontinuous
alongsidestreamsandrivers,dependingonthewidthofthe forest(StratfordandStouffer,1999;Lauranceetal.,2006a,b).
watercourse (Co´digo Florestal, 2001). Terra firme (unflooded)
foreststripsarelesscommonthantheseriparianremnants, 2. Methods
butneverthelessareoftenusedtoseparatelargeagricultural
and silvicultural blocks to help prevent soil erosion and the 2.1. Studysites
spreadofpests,diseaseandfire(e.g.Zanuncioetal.,1998).
While forest strips are therefore usually maintained to Sampling was conducted in the 1.7Mha landholding of Jarı´
protect water sources or production interests, a number of Celulose S.A., located on the border between the states of
studies have suggested that they can also be a potentially Amapa´ and Para´ in north-eastern Brazilian Amazonia
valuable conservation asset (Sodhi et al., 1999; Haddad (0(cid:3)530S, 52(cid:3)360W). Average annual rainfall is 2115mm, and
et al., 2003), by providing areas of habitat in theirown right themeandailyairtemperatureis26(cid:3)C(CoutinhoandPires,
(LimaandGascon,1999;LeesandPeres,2008).Itisimportant 1996). About 10% of the primary forest in this landholding
to note that while remnant forest strips do not necessarily was converted to exotic tree plantations between 1969 and
providephysicallinkagestheycanstillconferalevelof‘‘func- 1990. At the time of study the landscape consisted of fast-
tional connectivity’’ (i.e. as perceived by organisms them- growing Eucalyptus plantations on 5–7 year rotations, large
selves, Taylor et al., 2006) by increasing the representation tracts of regenerating secondary forest (14–19 years old),
andfacilitatingthemovementofspecies(Castello´nandSiev- and vast expanses of relatively undisturbed primary forest
ing,2006)aswellasthepersistenceofkeyplant–animalinter- (Fig. 1). We examined remnant forest strips that extended
actions(Tewksburyetal.,2002)acrossthelandscape. from areas of primary forest into the matrix of plantations
Despite their potential benefits for biodiversity and rela- andfallowland(secondaryforest)bothonunfloodedland(ter-
tively common existence (together with the approval, or at ra firme forest strips) and along perennial streams (riparian
least widespread tolerance of them by large landowners), foreststrips).Alloftheremnantstripswerepartofanexten-
wehaveaverypoorunderstandingofthepotentialconserva- sive and continuous region of undisturbed primary forest
tion value of forest strips in production landscapes (Hobbs, when the area was initially cleared approximately 30 years
1992; Harrison and Bruna, 1999; Haddad and Tewksbury, ago. These remnant strips have since been exposed to little
2006).Specifically,thereisadistinctlackofknowledgeregard- furtherdisturbanceotherthanselectiveloggingofafewcom-
ing the relative importance of strip type (i.e. terra firme or merciallyvaluablespeciesfromsomesitesduringtheinitial
riparianforest),striplength,togetherwithcorrelatedchanges landclearance.
inforeststructureanddegradationstatus(MacDonald,2003; Weselectedeightforest stripsin total,withfouronterra
butseeLeesandPeres,2008),andwhethernarrowforestrem- firme and fouralong perennial streams. Twosamplingtreat-
nantssufferthesame‘‘ecologicalimplosion’’assmallforest mentswereconductedineachstrip:‘near’siteswerealways
fragments (Lindenmayer et al., 1997; Laurance et al., 1997; located where the remnant became substantially wider and
Gascon et al., 2000). Finally, there is a marked research bias connectedwiththeneighbouringcontinuousforest,and‘far’
towardstemperatezones(Wiens,2006)andaresultingdeficit siteswerelocatedaminimumof2.5kmalongremnantsthe
ofstudiesfromtropicalforestregions. stripintothematrix.Controlsiteswerelocatedwithinanarea
Please cite this article in press as: Hawes, J. et al., The value of forest strips for understorey birds ..., Biol. Conserv. (2008),
doi:10.1016/j.biocon.2008.06.017
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BIOLOGICAL CONSERVATION xxx (2008) xxx–xxx 3
Fig.1–Mapofstudyareashowingthe24samplingsitesandareasofplantation(darkgrey),secondaryforest(lightgrey)and
primaryforest(white).Symbolsshowcontinuousforest(circles),‘near’sites(squares)and‘far’sites(triangles)interrafirme
(black)andriparian(white)foreststrips.Insetshowsdetailofthethreesampletreatmentsinforeststrips.
ofcontinuousprimaryforestthatwasadjacenttoeachofthe seasons, thus providing a snap-shot of the distribution of
strips.Wethereforesampledatotalof24sitesinafullyrepli- thesebirdsacrossourstudyareas.Theorderofsamplingin
cated block-design, with four replicates for each sampling the different sites was stratified to minimise the potential
treatment(near,farandcontrol)forbothterrafirmeandripar- influence of seasonality, by alternating both between the
ian strips. Unfortunately, the landscape configuration limits two types of forest strip and the three distance treatments
ourabilitytocomparedirectlybetweenriparianandterrafirme (distance from continuous forest). We erected 24 mist nets
stripsbecauseofsomeimportantdifferences:remnantswere (12·2.5m;meshsize36mm)endtoendalongaclearedtran-
generallywider(terrafirmemeanwidth=115m[range95–150]; sect at each of the 24 sampling sites, creating a net-line of
riparianmeanwidth=213m[125–300])and‘far’siteswithin approximately 320m once large treefalls had been avoided.
riparianremnantsweretypicallyfurtherfromcontinuousfor- Netswereopenedfrom0630hto1230hforthreeconsecutive
est(terrafirmemeandistance=3.4km[2.5–4.0];riparianmean daysateachsite,withextranet-hoursaddedtoaccountfor
distance=7.0km[range6.0–9.0]).Furthermore,ripariansites the closure of nets during periods of persistent heavy rain,
wereconsiderablymoredispersedgeographicallythantheter- givingastandardeffortof432net-hourspersiteandatotal
ra firme sites (Fig. 1). Site characteristics are summarised in effortof10,368net-hours.Netswerecheckedhourly,andall
Table1. captures were identified to species, and weighed, measured
and sexed whenever possible. All birds were marked by a
2.2. Avifaunalsampling small notch cut in their 3rd outermost primary feather (or
3rdoutermosttailfeatherinhummingbirds)enablingrecap-
Weusedunderstoreymist-nettingtoexaminetheavifaunaat turestobeexcludedfromthisanalysis.
each of the 24 sites. Although this sampling technique can Althoughmistnetsaregenerallylessefficientthanpoint-
occasionallycapturesomecanopyspecies,toavoidmisinter- counts(Thiollay,1994;BlakeandLoiselle,2001;Barlowetal.,
pretationwerefertoallcapturesastheunderstoreybirdcom- 2007b) and resulted in relatively small sample sizes in this
munity.Allsamplingwasundertakenbetween19Januaryand study,theyarealsofreeofobserverbias,andprovideauseful
29April2006,duringthetransitionbetweenthedryandwet standardisedtechniqueforcomparingunderstoreyavifaunal
Please cite this article in press as: Hawes, J. et al., The value of forest strips for understorey birds ..., Biol. Conserv. (2008),
doi:10.1016/j.biocon.2008.06.017
4
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.0ss Table1–Landscapeandhabitatvariables(means±SE)foreachlocationinbothtypesofforeststrip(n=4ineachcase)
17as
: Variable Unit Terrafirme Riparian Pair-wiseMann–WhitneyU
H
a testsbetweenterrafirme B
w andriparianremnants IO
es, (p-valuesinparentheses) LO
J G
.e Mean SE Mean SE Mean SE v2 p Mean SE Mean SE Mean SE v2 p Controls Nears Fars IC
t A
a control near far control near far L A
l.,T Primaryforestwithin1km % 58.3 2.6 15.8 6.5 3.7 0.8 8.8 0.01* 88.6 1.4 43.1 8.9 14.7 3.3 9.8 0.01** 0.0*(0.03) 2.0(0.11) 0.0*(0.03) CON RT
he Distancefromprimaryforest km 0.0 0.0 0.6 0.3 3.4 0.3 9.5 0.01** 0.0 0.0 0.6 0.3 7.0 0.7 9.5 0.01** 8.0(1.00) 8.0(1.00) 0.0*(0.03) SE IC
va Distancefromremnantedge m – – 45.1 3.4 45.5 3.8 0.0 1.00 – – 66.6 45.0 72.3 43.0 0.5 0.47 – 5.0(0.44) 6.0(0.69) RV L
lueo CLianneoapryreompennannetswsidth %m 6–.7 0–.7 1138..88 131..09 1168..36 07..37 30..13 00..2516 5–.8 1–.1 2507..06 201..42 1757..04 420..16 12..83 00..1391 5–.0(0.49) 06..00*((00..6093)) 22..05((00..1111)) ATIO EI
f Understoreydensity n 8.2 0.7 6.3 1.6 5.3 1.6 1.9 0.39 5.4 0.5 6.7 1.0 7.3 1.3 1.0 0.61 0.0*(0.03) 7.0(0.89) 4.0(0.34) N N
forest DLievaedtrtereeebbaasasallaarereaa 06..67 00..26 05..45 00..24 03..64 01..32 04..23 00..9132 17..03 01..30 08..90 00..78 07..52 00..19 10..95 00..3799 47..00((00..3849)) 80..00*((10..0003)) 28..00((01..1010)) xxx PR
strip LDievaedppaalmlmbbaasasallaareraea 00..10 00..00 00..10 00..00 00..20 00..10 22..50 00..2397 00..20 00..10 00..50 00..30 00..50 00..20 02..56 00..7297 64..00((00..6394)) 36..00((00..2609)) 48..00((01..3040)) (200 ES
s 8 S
for LDievaedlilaiannaabbaasasallaarereaa 00..60 00..20 00..40 00..20 00..80 00..30 13..28 00..5155 10..00 00..30 00..90 00..70 00..50 00..10 10..92 00..3992 47..00((00..3849)) 88..00((11..0000)) 46..00((00..3649)) )x
un Pioneerbasalarea 0.1 0.1 0.4 0.2 0.6 0.2 2.7 0.26 0.1 0.1 0.4 0.1 0.2 0.1 2.4 0.30 5.5(0.49) 8.0(1.00) 5.0(0.49) xx
de Water-lovingbasalarea 0.1 0.1 0.0 0.0 0.0 0.0 2.0 0.37 0.3 0.1 1.0 0.5 0.4 0.2 2.9 0.24 3.0(0.20) 0.0*(0.03) 0.0*(0.03) –x
rs x
to ComparisonsaremadeusingKruskal–WallisandMann–Whitneytests. x
r
e * p<0.05.
y
b ** p<0.01.
ir
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ARTICLE IN PRESS
BIOLOGICAL CONSERVATION xxx (2008) xxx–xxx 5
communitiescomposedofmanynon-vocalandsecretivespe- farandcontrol)foreachforestremnanttype(terrafirmeand
cies (Karr, 1981; Stouffer and Bierregaard, 1995; Barlow and riparian) were compared using sample-based rarefaction
Peres,2004;Barlowetal.2007b).Captureratesmaynotaccu- curvesproducedinEstimateS7.5(Colwell,2005).Thestructure
rately represent relative species abundances (Remsen and and composition of communities were examined with non-
Good,1996),butourestimatesaresupportedbythestrongpo- metric multi-dimensional scaling (MDS) ordinations using
sitivecorrelationbetweentheabundanceofspeciessurveyed Bray-Curtis similarity matrices based on square-root trans-
independentlybymistnetsandpoint-countsinthesamere- formedandstandardisedabundancedata,and presence/ab-
gion (Barlow et al., 2007b). Nevertheless, particular caution sence data. Differences between sampling treatments were
should be applied to estimates of species richness, as mist assessedusinganalysesofsimilarities(ANOSIM),theidentity
nets tend to be more effective in more disturbed habitats, ofspeciescontributingthemosttoanydifferenceswasdeter-
where birds fly closer to the ground (Blake and Loiselle, minedbyananalysisofpercentagesimilarities(SIMPER),and
2001;Barlowetal.,2007b). the influence of environmental parameters on community
structurewasassessedusingtheBIOENVprocedure.Allcom-
2.3. Vegetationsampling munity analyses were conducted using Primer (v.5) (Clarke
andWarwick,2001).
Trees and lianas were sampled in each of the 24 avifaunal Specieswereassignedtodietaryandforagingguildsfollow-
samplingsites,usingastandardproceduredescribedbyBar- ing Terborgh et al. (1990), with additional information from
lowetal.(2002).Treeswereincludedinasampleifmorethan RidgleyandTudor(1989,1994)andHilty(2002),andcategorised
50%oftheirtrunkwaswithin5mofthecentreofthetran- accordingtotheirdegreeofhabitatspecialisationandsensitiv-
sect. We measured all dead and live standing trees P10cm itytodisturbance(Stotzetal.,1996).Inaddition,bothmist-net
DBH and lianas P5cm in a 10·1000m plot established at andpoint-countdatafromanindependentstudy(Barlowetal.,
each site, recording whether species were palms, early pio- 2007b)wereexaminedusingIndicatorSpeciesAnalysisinPC-
neers (mainly Cecropia spp. and Vismia spp.) and/or typical ORD(McCuneandMefford,1999).ThisanalysisusestheIndVal
of water-logged soils (e.g. Iriartea exorrhiza and Mauritia procedure(DufreneandLegendre,1997;McGeochandChown,
spp.).Wecalculatedbasalareaexcludingthelargesttreefrom 1998)toidentifyspeciesthatarecharacteristicofcontinuous
eachsampletoremovethepotentialbiasfromthestochastic primaryforestandthematrixhabitats(secondaryforestand
presence of single large trees in relatively small forest plots Eucalyptus plantations). This method combines measures of
(although results using all the data remained quantitatively bothhabitatspecificity(throughpatternsofabundance)and
very similar). Canopy cover and understorey density were habitat fidelity (through patterns of presence–absence), pro-
measured at each mist-netting location, using a spherical ducingapercentageindicatorvalue(IndVal)foreachspecies
densitometer and 2.5m graded pole, respectively, following –i.e.tobecharacteristicofacertainland-usetypeaspecies
Barlowetal.(2002). has to be found reliably and almost exclusively within that
land-use. Dufrene and Legendre, (1997) random reallocation
2.4. Land-coveranalysis procedureofsiteswithinsitegroupswasusedtotestthesignif-
icanceoftheIndValmeasureforeachspecies.
Ageographicinformationsystem(GIS)wasusedtoquantify DatafromBarlowetal.(2007b)werealsousedtocompare
the land-use composition surrounding each sampling site. birdcommunitiesfromforeststripstothosefoundinthewider
Site locations were recorded using a handheld GPS receiver landscapemosaicatJaribut,inthiscase,thepoint-countdata
(Garmin eTrex) and a semi-supervised land-cover classifica- wereomittedtoensureacommonmethodologyandlevelof
tion,withground-truthingbasedonourintimateknowledge samplingeffort.Ourapproachtoassessingpatternsofpoten-
of the landscape, was developed from a combination of tialconservationvaluewaslimitedbyknowledgeoftheviabil-
land-usedataprovidedbyJariCeluloseS.Aanda2003Land- ity of populations sampled within the strips. Recording the
sat7(30-mpixel)image.Buffersof1kmwerecreatedaround presenceofabirdspecies,eveninlargenumbers,withinafor-
thecentralpointofeachavifaunalsamplingsitebeforeper- eststripmasksthefactthatitmaysufferfromadepletedlevel
forminganintersectoverlaywithland-uselayerscontaining offitnessorbreedingsuccess.Nevertheless,intheabsenceof
dataonmajorland-covertypes(oldandyoungplantationfor- more detailed population or physiological data, patterns of
est, old and young secondary forest, closed-canopy primary occupancyandabundanceprovideavaluableproxyofthepo-
forest,opencanopyforest,floodedareas,naturalsavannahs tentialtheseareashaveforthepersistenceofnativespecies
andhumansettlements)toprovideabuffermeasureofcon- inanotherwisehostilelandscape.Moreover,weareinterested
nectivity(MoilanenandHanski,2006). in documenting broad patterns of avifaunal diversity and
abundancebetweendifferentforeststripsandthesurrounding
2.5. Dataanalysis matrix,andnotingeneratingspecificconclusionsaboutthe
suitabilityoftheseareasforindividualspecies.
Wecombinedcapturedatafromthestandard432net-hours
conductedateachsamplingsite.Becauseoftheconsistentdif- 3. Results
ferencesinthewidthsanddistancetreatmentsinterrafirme
andriparianstripsweavoideddirectcomparisonsofthetwo 3.1. Habitatandlandscapestructure
habitattypes,andanalysedthemseparatelywhenassessing
theimportanceofdistancefrom continuous forest. Patterns Local vegetation structure was broadly similar in terra firme
of species richness in the three sampling treatments (near, and riparian forest strips (Table 1), although riparian
Please cite this article in press as: Hawes, J. et al., The value of forest strips for understorey birds ..., Biol. Conserv. (2008),
doi:10.1016/j.biocon.2008.06.017
ARTICLE IN PRESS
6 BIOLOGICAL CONSERVATION xxx (2008) xxx–xxx
remnantshadasignificantlyhigherbasalareaoftreespecies munities significantlydistinct from those ofcontinuous pri-
thatareassociatedwithwater-loggedsoils,andahighertree mary forest (Fig. 3, Table 2). SIMPER analysis showed that
basalareain‘near’sitesthaninthe‘near’sitesofterrafirme terra firme ‘far’sites were most evidently distinct from terra
remnants. In addition ’Far’ sites within riparian remnants firmeforestcontrolsduetohigherabundancesofspeciessuch
hadmoreprimaryforestwithina1-kmbufferthanthosein asPectoralSparrow(Arremontaciturnus),ReddishHermit(Phae-
terrafirmeremnants(Table1). thornis ruber), and Guianan Slaty Antshrike (Thamnophilus
Withineachtypeofforeststrip,therewerenosignificant punctatus),andlowerabundancesofWhite-crownedManakin
differences in vegetation structure between continuous pri- (Dixiphia pipra). By contrast, riparian ‘far’ sites had higher
maryforestandthestrips(Table1).Unsurprisingly,measures abundances of White-bearded Manakin (Manacus manacus),
ofthewiderlandscapecompositionvariedwithlengthalong Wedge-billed Woodcreeper (Glyphorynchus spirurus), and Ruf-
thestrips.Almosttheentirematrixadjacenttoallthestrips ous-breasted Hermit (Glaucis hirsuta), and lowerabundances
was under Eucalyptus plantation, and 1-km buffers around of Dusky-throated Antshrike (Thamnomanes ardesiacus) than
‘far’sites in both terra firme and riparian remnant strips re- riparianforestcontrols(seeS1–2inSupplementarymaterial).
tainedasignificantlylowerpercentageofprimaryforestcover
than‘near’sites(Table1). 3.3. Potentialvalueofforeststripsfornativeforestbirds
3.2. Avifaunalsampling The pattern of bird abundance between treatments and
according to different species classes was similar whether
Wecapturedatotalof1910birdsfrom117species.Site-level weconsideredcategoriesbasedonthedisturbance-sensitivity
capturesrangedfrom32to117individuals,andthenumber classes of Stotz et al. (1996), or groups of species that were
ofspeciesobservedpersiterangedfrom14to44.Similarnum- identifiedas characteristicofspecificforest typesintheJari
bersofbirdindividuals(967and943)andspecies(93and89) landscapebytheIndValprocedure(Barlowetal.2007b).There
werecapturedinterrafirmeandriparianforesttypes,respec- was a large overlap in these two independent classification
tively(seeAppendix).Thespeciesrichnessofterrafirmestrips methods(Table3).Forexample,17ofthe24speciesidentified
wassignificantlylowerthanthatrecordedincontinuousterra ascharacteristicofprimaryforestwereclassedbyStotzetal.
firmeforestcontrols,whileriparianstripsandriparianforest (1996) as being highly disturbance-sensitive. Similarly, 16 of
sites embedded within continuous forest displayed similar the17speciesfoundtobecharacteristicofsecondaryforest
levelsofbirdspeciesrichness(Fig.2).Thetwotypesofforest arecategorisedasspeciesofmediumorlowsensitivitytodis-
strip(terrafirmeandriparian)hosteddistinctbirdcommunities turbanceandallfivespeciesfoundtobecharacteristicofEuca-
when analysed using both abundance (ANOSIM: R=0.31, lyptusplantationsarespeciesoflowsensitivity(seeTable3for
p<0.003)andpresence/absencedata(R=0.33,p=0.001),and details).
these differences were independent of sampling location Incomparisontocontinuousprimaryforest,highlydistur-
(Near: R=0.75, p=0.029; Far: R=0.542, p=0.029; Control: bance-sensitivebirds(asclassifiedbyStotzetal.,1996)were
R=0.427,p=0.029). found in significantly lower abundances in terra firme rem-
There was no statistically significant difference between nants,butnotinriparianremnants(Fig.4).However,allsam-
thespeciesrichnessof‘near’and‘far’sites,forbothterrafirme ples from forest strips supported fewer birds that are
andriparianremnants(Fig.2).However,aninfluenceofstrip characteristicofprimaryforest(asidentifiedbytheIndValpro-
lengthoncommunitystructureandcompositionwasdetected cedure)thantheprimaryforestcontrols,whiledemonstrating
forbothremnanttypes;ineachcaseonly‘far’siteshadcom- a higher abundance of species that are characteristic of
Fig.2–Sample-basedspeciesrarefactioncurves(rescaledbynumberofindividuals)forthethreesampletreatmentsin(a)
terrafirme,and(b)riparianforeststrips.Dottedlinesindicate95%confidenceintervalsforcontinuousprimaryforest.
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Fig.3–Multi-dimensionalscalingplot(basedonabundancedata)ofthebirdcommunitiesforthethreesampletreatmentsin
(a)terrafirmeand(b)riparianforeststrips.
Table2–ANOSIMresultsshowingthechangeincommunitystructurewithincreaseddistanceintothematrixalongthe
foreststrip
Pair-wisetests Terrafirmeremnants Riparianremnants Bothremnanttypes
(globalR=0.38,p=0.04) (globalR=0.26,p=0.034) (globalR=0.197,p=0.008)
R p R p R p
Control·near 0.365 0.114 0.24 0.057 0.174 0.067
Control·far 0.771 0.029* 0.552 0.029* 0.506 0.002*
Near·far 0.125 0.257 0.042 0.457 0.075 0.845
* p<0.05.
secondaryforest(Fig.4).AlthoughEucalyptusplantationsdom- uousforest(bothin‘near’ripariansites).Examiningindividual
inated the matrix, species characteristic of this forest type species responses demonstrates differences in the extent to
wererecordedatlowabundancesinallsamplesitesandnone which different species utilise the forest strips, with some
ofthestripsamplessupportedthesespeciesin significantly taxabeingcommonlyfoundoutsidecontinuousforest,includ-
greaternumbersthancontinuousprimaryforest,irrespective ing Plain-brown Woodcreeper (Dendrocincla fuliginosa), Blue-
of how far the remnants extended into the matrix (Table 3, crowned Motmot (Momotus momota), and Long-tailed Hermit
Fig. 4). Consequently the assemblages of birds found in the (Phaethornis superciliousus), while others were largely limited
remnantsmuchmorecloselyreflectsamplesfromcontinuous tocontrolsites,includingWhite-plumedAntbird(Pithysalbi-
forestthansamplesfromtheadjoiningmatrix.Thisresultis frons)andWhite-neckedThrush(Turdusalbicollis)(Table3).
furthersupportedbytheordinationplotcombiningallsam-
plingsitesfromthis study withthosefrom ourearlierwork 4. Discussion
inthewiderlandscape(Barlowetal.2007b)(Fig.5).Thesere-
sultsthereforesupportourfirstbutnotoursecondhypothesis, 4.1. Useofriparianandterrafirmeforeststripsbyforest
bydemonstratingthatbirdcommunitiessampledinremnant birds
foreststripsaredistinctfromthosesampledincontinuousfor-
estcommunities,butasaresultofbecomingincreasinglysim- The importance of vegetation structure in determining pat-
ilar(withincreaseddistanceintothematrix)tocommunities terns of species diversityand abundance iswell established
sampledin secondaryforest sitesrather than samplesfrom (MacArthur et al., 1966; Henein and Merriam, 1990), yet the
thesurroundingmatrixofEucalyptusplantations. role of forest type in determining the use of remnant strips
Ofthe13foraginganddietaryguildscaptured,onlythree by native forest biota has received little attention. Riparian
exhibited significantly depleted abundances in the forest forestsarewelldocumentedasareasofhighspeciesrichness
strips. Terra firme strips supported fewer arboreal dead-leaf (NaimanandDe´camps,1997;Bennett,2003)partlyduetothe
insectivores(v2=7.55,p=0.023)andfewerarborealfrugivores additionalpresenceofaquaticspeciesandalsothediversity
(v2=7.20,p=0.027)thansitesincontinuousterrafirmeforest. ofhabitatstheycontain.Asfarasbirdspeciesareconcerned
In addition, ant-following insectivores were virtually absent theymayalsoofferparticularbenefitsduetothepresenceof
fromallforeststrips,beingrecordedonlytwiceoutsidecontin- water-loving plant species such as ac¸a´ı (Euterpe oleracea),
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Table3–AbundanceinforeststripsofspeciesidentifiedbytheIndValprocedure(DufreneandLegendre1997)as
characteristicofprimary,secondaryandplantationforest
Species Guilda Sensb Numberofindividualscaptured
Terrafirme Riparian
Control Near Far Control Near Far
Speciescharacteristicofprimaryforest
Pithysalbifrons IAF High 6 8 2
Gymnopithysrufigula IAF Med 2 6
Hylophilusmuscicapinus IAG High 1
Myrmotherulamenetriesii IAG High 2 3 1 1
Hylophylaxpoecilinota IAG Med 2 1 5 1 7
Dendrocinclafuliginosa IAS High 2 3 6 8 2 5
Lipaugusvociferans IAS High 2
Thamnomanesardesiacus IAS High 10 3 12 10 4
Thamnophilusmurinus IAS High 2 2
Tolmomyiasassimilis IAS High 1
Momotusmomota IAS Med 2 4 1 5
Tolmomyiaspoliocephalus IAS Med 1
Xiphorhynchuspardalotus IBS High 2 1 7 3 3
Glyphorynchusspirurus IBS Med 30 36 37 38 33 45
Formicariuscolma ITG High 2 1
Sclerurusrufigularis ITG High 2 5 3
Formicariusanalis ITG Med
Dixiphiapipra FA High 20 5 1 13 6 7
Pipraerythrocephala FA High 10 10 2 4 4 10
Ramphastosvitellinus FA High 1 1 2
Schiffornisturdinus FA High 4 1
Geotrygonmontana GT Med 9 2 1 4 1
Phaethornisbourcieri NA High 5
Phaethornissuperciliosus NA High 36 22 26 29 32 27
Turdusalbicollis OA Med 7 6 3
Total 152 85 77 160 99 119
Speciescharacteristicofsecondaryforest
Cercomacratyrannina IAG Low 9 10 5
Thamnophiluspunctatus IAG Low 3 4 20 2 2
Thryothoruscoraya IAG Low 10 9 12 3 8
Lophotriccusgaleatus IAS Med 1 1
Automolusochrolaemus IDL Med 1 1 3
Percnostolarufifrons ITG High 11 21 23 8 8 12
Myrmecizaatrothorax ITG Low 1 7 7
Myrmoborusleucophrys ITG Med 1 13 1
Manacusmanacus FA Low 9 9 20 4 29 33
Machaeropteruspyrocephalus FA Med 1
Cryptrelluserythropus GT Low 1
Phaethornisruber NA Med 6 9 29 4 11 8
Saltatormaximus OA Low 3 1 1
Arremontaciturnus OA Med 2 24 30 1 10
Cyanocompsacyanoides OA Med 7 7 5 5 5 6
Mionectesoleagineus OA Med 14 9 7 9 13 14
Turdusfumigatus OA Med 3 2
Myrmotheracampanisoma ITG High
Tarabamajor IAG Low
Total 73 103 169 32 83 108
Speciescharacteristicofeucalyptusplantations
Tolmomyiasflaviventris IAS Low 2
Volatiniajacarina GT Low 1
Amaziliafimbriata NA Low 2 3 3 1 3 4
Coerebaflaveola NA Low 2 2 1
Glaucishirsuta NA Low 8 4 10 7 38 21
Anthracothoraxnigricollis NA Low
Camptostomaobsoletum IAG Low
Cyclarhisgujanensis IAG Low
Myiophobusfasciatus IAS Low
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Table3–(continued)
Species Guilda Sensb Numberofindividualscaptured
Terrafirme Riparian
Control Near Far Control Near Far
Troglodytesaedon IAG Low
Myiopagisgaimardii IAG Med
Polytmustheresiae NA Med
Total 10 10 17 8 42 25
a IAF=insectivoreant-following,IAG=insectivorearborealgleaning,IAS=insectivorearborealsallying,IBS=insectivorebark-searching,IDL–
insectivore dead leaf, ITG=insectivore terrestrial gleaning, FA=frugivore arboreal, GT=gramnivore terrestrial, NA=nectivore arboreal,
OA=omnivorearboreal.
b Stotzetal.(1996).Disturbance-sensitivityclasses:high,medium(med)andlow.
Fig.4–Changesintheabundanceofbirdsgroupedbysensitivitytodisturbanceandpreferredforesttypeforterrafirmeand
riparianforeststrips.SignificancewascalculatedusingKruskal–Wallistests:*=<0.05,**=<0.01.
whichareimportantresourcesforfrugivorousbirds(Moegen- riparian and terra firme forest strips for forest birds in our
burgandLevey,2003). study region. Nevertheless, we are able to demonstrate that
Duetopotentiallyconfoundinglandscapefactors,weare the two types of remnant forest strip hosted distinct bird
unable to provide a direct comparison of the suitability of communities, both of which closely reflected samples from
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Working on patterns of bird diversity in Australian pine
plantations,Tubelisetal.(2007)recentlyinvokedthe‘‘penin-
sulareffect’’–abiogeographicphenomenonthatresultsina
decreaseinspeciesrichnessfromthebasetothetipofapen-
insular–tohelpexplainlocalscalechangesinthenumberof
birdspeciesoccupyingsmall‘‘peninsulars’’ofnativeEucalyp-
tus forest. The results of our study for terra firme strips are
qualitatively similar to that found by Tubelis et al. (2007),
suggestingthatthisphenomenonmaybewidespreadinhu-
man-dominated forest landscapes, although the underlying
mechanism to explain the process occurring in our study
remainsunclear.
One explanation for this decline in disturbance-sensitive
andprimaryforestcharacteristicspecies(andtheassociated
increase in species characteristic of secondary forest) with
increasing strip length could be changes in local vegetation
structure and condition (Laurance et al., 2006a). Similar
replacements of bird communities have been found follow-
ing habitat degradation by fireand selective logging (Barlow
and Peres, 2004; Barlow et al., 2006) that are, in turn,
Fig.5–Multi-dimensionalscalingplot(basedonabundance
strongly related to changes in local habitat structure (e.g.
data)ofthebirdcommunitiesinforeststripsinrelationto
Mason, 1996; Barlow et al., 2002; Barlow and Peres, 2004).
birdcommunitiesfromthesurroundinglandscape.
However, our data do not give support to this explanation,
Trianglesrepresentsitesin‘near’(grey),‘far’(white)and
as the ‘‘secondarisation’’ of the bird community appears to
primarycontinuousforestcontrolsites(black)forterrafirme
have occurred independently of changes in our measured
(downwardpointingtriangles)andriparian(upward
forest structure variables. For example, variables identified
pointingtriangles)foreststrips.Additionalsymbolsshow
from previous studies as important in structuring Amazo-
continuousprimary(blackcircles),secondary(whitecircles)
nianavifauna,suchaslivetreebasalarea,understoreyden-
andplantationforestsites(whitesquares)fromBarlowetal.
sity and canopy cover (e.g. Barlow and Peres, 2004) did not
(2007b).
differ significantly with strip length (although our sample
sizes were low, very few of these comparisons even ap-
continuous primary forest, implying thatthese two typesof proached significance, see Table 1), and therefore are unli-
forest strip may provide a complementary service for the kely to explain the observed differences in bird
conservation of these species in plantation landscapes (see communities sampled in ‘near’ and ‘far’strip sites. Further-
alsoBakeretal.,2006). more, the BIOENVanalysis conducted in this study showed
that these variables were also very poorly correlated with
4.2. Foreststriplengthandtheinfluenceofthematrix changesinbirdcommunitystructure(seeS3inSupplemen-
tary material).
Increases in the length of forest strips and isolation from The lack of any observed changes in sampled bird com-
neighbouringcontinuousforesthasbeenassociatedwithde- munities in association with changes in vegetation vari-
clinesintherichnessandabundanceofprimaryforestbirds ables, as reported for small forest fragments elsewhere in
inbothconnected(LeesandPeres,2008)andunconnectedor Amazonia (Laurance et al., 2002, 2006a,b), could be due to
poorly connected remnants (Ferraz et al., 2003; Stoufferand bufferingofthestripsbythesurroundinglandscapematrix.
Bierregaard,1995;StratfordandStouffer,1999;Antongiovanni Matrix habitats consisting of secondary forest have been
andMetzger,2005).Anegativeeffectofforeststriplengthon shown to be important in mitigating against the loss of for-
the abundance of forest interior species has been found for est species in isolated Amazonian fragments (Antongiovan-
othervertebrategroupstoo(e.g.arborealmarsupials;Linden- ni and Metzger, 2005; Stouffer et al., 2006). The matrix in
mayeretal.,1993),suggestingthatthiseffectmaybegeneral. Jari, however, is principally composed of Eucalyptus planta-
There is also increasing evidence to show that disturbance- tions, and while some forest species were lost in the ‘far’
sensitivespecies(e.g.theant-followerguild)mayonlyenter sites,wealsofoundverylimitedevidenceofashifttowards
shortdistancesintosilviculturalhabitatsorcrosssmallforest a bird community characteristic of Eucalyptus. For example,
gaps(Robertsetal.,2000;Lauranceetal.,2004;Lauranceand onlyfiveofthe12speciesthatwereknowntobecharacter-
Gomez,2005;Barlowetal.,2007b).Indemonstratingalossof istic of Eucalyptusplantationswereever recorded in the for-
disturbance-sensitive species and species characteristic of est strips, and only two species were recorded frequently
primaryforest,withincreasingdistancefromcontinuousfor- (Table3).Thesewerebothspeciesofhummingbird(theRuf-
est,ourresultsfurtherstrengthenthesefindingsandaddsup- ous-breasted Hermit, Glaucis hirsuta; and the Glittering-
porttothemanagementrecommendationforminimisingthe throated Emerald, Amazilia fimbriata), which are wide-rang-
length of forest strips (connected or unconnected) when ing and known to persist in a variety of habitats (Stouffer
attemptingtodesignmorefunctionallyconnectedlandscapes and Bierregaard, 1995). This shows that disturbance caused
(WilsonandLindenmayer,1995). by increased isolationfrom continuous primary forest with-
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