Microhabitat associations of terrestrial insectivorous birds in Amazonian rainforest and ...

12 Pages·2013·0.71 MB·English

Journal of Field Ornithology
J.FieldOrnithol.84(1):1–12,2013 DOI:10.1111/jofo.12000
Microhabitat associations of terrestrial insectivorous
birds in Amazonian rainforest and second-growth forests
JeffreyA.Stratford1,3 andPhilipCStouffer2
1DepartmentofHealthandBiologicalSciences,WilkesUniversity,Wilkes-Barre,Pennsylvania18766,USA
2SchoolofRenewableNaturalResources,LouisianaStateUniversityAgriculturalCenter,BatonRouge,Louisiana
70803-6202,USA
Received12January2012;accepted29October2012
ABSTRACT. AcrosstheNeotropics,small-bodiedterrestrialinsectivoresaresensitivetoforestfragmentation
and are largely absent from second-growth forests. Despite their sensitivity to forest structure, the microhabitat
relationshipsofthesebirdshavenotbeenquantified.FromJuly1994toJanuary1995incentralAmazonia,we
characterized habitat at sites where nine species of terrestrial insectivores were observed foraging, as well as at
randomly selected sites in continuous forest and two types of 10–15-yr-old second-growth forest common in
Amazonia(Vismia-andCecropia-dominated).Weusedfactoranalysistofindsuitesofcorrelatedvariables.From
eachfactor,weselectedarepresentativevariablethatwasrelativelyeasytomeasure.WeusedBayesiananalysisto
estimatemeansandstandarddeviationsofthesevariablesforeachspeciesandforeachtypeofhabitat.Allnine
focalspecieswereassociatedwithrangesofmicrohabitatvariables,suchasleaflitterdepthandtreedensities,often
absentinsecond-growthforests.Atleastintheearlystagesofregeneration,neithertypeofsecond-growthforest
providessuitablestructurefortheterrestrialinsectivoresinourstudy.ThelargeleavesofCecropiatreesthatmake
upthethickleaflittermayprecludetheuseofCecropia-dominatedsecondgrowthbyourfocalspecies,manyof
whichmanipulateleaveswhenforaging.TheleaflitterinVismia-dominatedsecondgrowthwasalsothickerthan
sitesusedforforagingbyourfocalspecies.Inaddition,Vismia-dominatedgrowthhadmoresmalltreesandsmall
nonwoody vegetation, perhaps impeding movement by terrestrial birds. In continuous forest, our focal species
foragedinmicrohabitatswithcharacteristicsthatgenerallyoverlappedthoseofrandomlyselectedsites.Thus,our
resultsareconsistentwiththehypothesisthatmicrohabitatdifferencesmakesecond-growthforestsunsuitablefor
ourfocalspecies.
RESUMEN. Asociacio´n de aves insect´ıvoras terrestres con el micro ha´bitat en la selva
Amazo´nicaybosquesdecrecimientosecundario
AlolargodelNeotropico,avesinsect´ıvorasterrestresdetaman˜ocorporalpequen˜osonsensiblesalafragmentacio´n
delbosquesyengranparteesta´nausentesenlosbosquesdecrecimientosecundario.Apesardesusensibilidad
a la estructura del bosque, las relaciones de estas aves con el micro ha´bitat no han sido cuantificadas. Desde
julio de 1994 hasta enero de 1995 en la Amazonia central caracterizamos ha´bitats en lugares en donde nueve
especiesdeavesinsect´ıvorosterrestresfueronobservadasbuscadoalimento,aligualqueenlugaresseleccionados
aleatoriamente en un bosque continuo y en dos tipos de bosques secundarios de 10 y 15 an˜os, comunes en la
Amazonia (Vismia-dominado y Cecropia-dominado). Usamos un ana´lisis factorial para encontrar el conjunto de
variablequesecorrelacionaron.Tambie´nusamosunana´lisisbayesianoparaestimarelpromedioylasdesviaciones
esta´ndar de estas variables para cada especie y cada tipo de ha´bitat. Las nueve especies focales se asociaron con
elementosvariablesdelmicroha´bitat,talescomoprofundidaddelahojarascaydensidaddearboles,usualmente
ausentesenbosquesdecrecimientosecundario.Almenosenlosestadiostempranosderegeneracio´nningunodelos
tiposdecrecimientosecundarioproveeunaestructuraadecuadaparalosinsect´ıvorosterrestresdenuestroestudio.
LaslargashojasdelosarbolesdeCecropiaquecreanunahojarascamasgruesapuedenevitarelusodebosquesde
crecimientosecundariodominadoCecropiaporpartedenuestrasespeciesfocales,muchasdelascualesmanipulan
hojas cuando esta´n buscando alimento. La hojarasca de los bosques de crecimiento secundario dominados por
Vismia tambie´n fue mas gruesa respecto a los lugares usados por nuestras especies focales para buscar alimento.
Adicionalmente,losbosquesdominadosporVismiatuvieronmasarbolespequen˜osypequen˜avegetacio´nnolen˜osa,
quepuedeimpedirelmovimientodelasavesterrestres.Enbosquescontinuos,nuestrasespeciesfocalesbuscaron
alimentoenmicroha´bitatsconcaracter´ısticasquegeneralmentesesuperpusieronconlasdeloslugaresescogidos
aleatoriamente. En consecuencia, nuestros resultados son consistentes con la hipo´tesis que diferencias en micro
ha´bitathacenquelosbosquesdecrecimientosecundarioseanlugaresinadecuadosparanuestrasespeciesfocales.
Key words: Conopophaga, Corythopis, Formicarius, Grallaria,habitat selection, Hylopezus, microhabitat,
Myrmornis,Myrmothera,terrestrialinsectivores,vegetationstructure
Studies of Neotropical birds have revealed that
most small-bodied terrestrial insectivores are
3Corresponding author. Email: jeffrey.stratford@ sensitive to forest fragmentation (Stouffer and
wilkes.edu Bierregaard 1995, Robinson 1999, Stratford
(cid:2)C2013TheAuthors.JournalofFieldOrnithology(cid:2)C2013AssociationofFieldOrnithologists
1
2 J.A.StratfordandP.C.Stouffer
J.FieldOrnithol.
and Stouffer 1999). Other studies have con- ing such microhabitat associations is necessary
firmed the sensitivity of terrestrial insectivores forpredictingresponsestoforestfragmentation,
to fragmentation (Kattan 1992, Renjifo 1999, selective logging, and other activities that alter
Sekercioglu et al. 2002, Lees and Peres 2010), forest structure (Holmes and Robinson 1981,
selective logging (Mason 1996, Aleixo 1999, DeppeandRotenberry2008).
Bicknell and Peres 2010), and other forms of Our objective was to provide a quantitative
habitatmodificationsuchasplantations(Cana- description of the microhabitat associations of
day 1997, Barlow et al. 2007). In addition, nine species of terrestrial insectivores in a well-
most Neotropical insectivorous birds are rarely studied Amazonian forest. By comparing the
foundinyoung(<15yr)secondgrowth(Borges characteristicsofmicrohabitatswherebirdsfor-
and Stouffer 1999, Blake and Loiselle 2001) age to those of randomly selected sites in con-
thatinitiallydevelopswhendeforestedareasare tinuous forest and second-growth sites, we can
abandoned (Borges and Stouffer 1999, Wright gainabetterunderstandingofhabitatselection
andMuller-Landau2006).However,assecond by terrestrial insectivores. Typical of microhab-
growth ages, terrestrial insectivores are more itat studies, we quantified several microhabi-
likely to move through it (Blake and Loiselle tat variables that we believed were potentially
2001, Antongiovanni and Metzger 2005). For important to terrestrial insectivores. However,
example, temporal changes in the abundance collectingthesedatatookconsiderabletimeand
of birds in fragments of Brazil’s Biological Dy- effortsoasecondaryobjectivewastoidentifya
namics of Forest Fragments Project (BDFFP) reducedsetofvariablestorecommendforusein
werefoundtobestronglyinfluencedbytheage futurestudiesofthesespecies.
and type of second-growth matrix surrounding
the fragments (Stouffer and Bierregaard 1995,
METHODS
Stouffer et al. 2006, 2011). Fragments sur-
roundedbyCecropia-dominatedsecondgrowth Study sites. From July 1994 to January
regained more species of birds lost after frag- 1995,wecollectedmicrohabitatdataatsitesthat
mentation than fragments surrounded by Vis- werepartoftheBDFFP,alarge-scale,long-term
mia-dominated second growth (Stouffer and research project sponsored by the Smithsonian
Bierregaard 1995). The area consisting of sec- TropicalResearchInstituteandBrazil’sNational
ond growth is rapidly expanding across the InstituteforAmazonResearch(Bierregaardand
Amazon (Neeff et al. 2006, Foley et al. 2007), Gascon 2001). The continuous forest site is
and understanding how terrestrial insectivores located in terra firme forest ∼60 km north of
respondtothedifferenttypesandagesofsecond Manaus,Brazil(seehttp://pdbff.inpa.gov.br/for
growth is crucial to their conservation (Anton- maps).Annualrainfallaverages2500mmwith
giovanniandMetzger2005,Gardneretal.2007, a distinct rainy season from February to May
Chazdon2008). (Stouffer and Bierregaard 1993). Soils in the
Several hypotheses have been proposed to areaaresandyandnutrientpoor(Lauranceetal.
explain why terrestrial insectivores are sensitive 1999), but tree diversity is exceptionally high
to alteration of forest structure (Stratford and (Oliveira and Mori 1999). At the continuous
Robinson 2005). One hypothesis is that ter- forestsite,canopyheightvaried,butistypically
restrialinsectivoresarecloselyassociatedwitha between30and37m(GasconandBierregaard
particular forest physiognomy and topography 2001). Lianas and vines are common (Roeder
and,ifkeyelementsaremissing,terrestrialinsec- etal.2010)andtheunderstoryisdominatedby
tivoresavoidtheseareas(StratfordandRobinson palmssuchasAstrocaryumspp.andBactrisspp.
2005).Thishypothesisisdifficulttotestbecause (Scariot 1999, de Castilho et al. 2006). Small
themicrohabitats(physiognomy)usedbymost streams,oftenwithsteepbanks,dissectthearea.
terrestrial insectivores have yet to be evaluated, Higher,flatareasorplateausarefoundbetween
withmicrohabitatdefinedasasubsetofhabitat streams (Bueno et al. 2011, Cintra and Naka
(e.g.,continuousforest)withparticularenviron- 2012). Isolated treefalls and blowdowns occur
mental conditions, including vegetation struc- sporadically throughout the site (Nelson et al.
ture(James1971).Duetomicrohabitatprefer- 1994). The continuous forest site is embedded
ences,areaswithinbroadlysuitablehabitatmay within a large forest that is largely intact for
gounusedforaparticularspecies.Understand- hundreds of kilometers with the exception of
MicrohabitatsofAmazonianInsectivores 3
Vol.84,No.1
Manaus, a large urban center. A gridded trail habitats were sampled only where birds were
system was set up at the continuous forest site observed foraging and, to avoid sampling areas
withparalleltrailsspacedevery100m. usedbythesameindividuals,weonlyconsidered
TheBDFFPstudyareaincludeslargepatches individuals observed >500 m from a previous
of second growth (see map in Stratford and observation of a bird of the same species. The
Stouffer 1999). Most of the second growth is site of each initial observation served as the
one of two types that are largely distinct in the center of an 8-m-radius (∼0.02 ha) vegetation
earlystagesofregeneration(Nordenetal.2011). sampling plot. We chose 8-m radius sampling
Patches of second growth we sampled were unitsasacompromisebetweenbeingconsistent
10–15 yr old. At this age, Cecropia dominates withpublishedmethods,i.e.,JamesandShugart
areas that were cut and abandoned, whereas (1970)andMarraandRemsen(1997)used10-
Vismia-dominatedsecondgrowthoccurswhere m-radii sample units, and our desire to finely
the forest was burned before abandonment quantifyforagingmicrohabitatusedbyourfocal
(Mesquita et al. 2001). Floristically, Cecropia- species. In addition, small-scale sampling units
dominated second growth has more plant can capture the vegetation structure associated
speciesandfamiliesthanVismia-dominatedar- withtheedgesandinteriorsoftreefallsintropi-
eas(Mesquitaetal.2001). calforests(Fetcheretal.1985,Uhletal.1988).
Bird and vegetation sampling. Our fo- We quantified vegetation using a modified
cal species were terrestrial insectivores with version of methods described by James and
a range of responses to fragmentation and Shugart(1970).Withineachplot,wemeasured
second-growthforest(BorgesandStouffer1999, 23 variables to quantify vegetation structure
Stratford and Stouffer 1999; Table 1). Sen- and topography. For topography, we noted if
sitivity to fragmentation was determined by the center of a plot was in a stream bed (flat
the probability that a species will go locally areasadjacenttorunningwater)oronastream
extinctafterfragmentation(StratfordandStouf- bank (signs of flooding, such as leaf packs),
fer 1999). We sampled three fragmentation- dry slope (no signs of flooding), or flat plateau
sensitive species that were missing from all or (higherareaswithnoslope).Duetosmallsample
most BDFFP fragments and that did not use sizes,plotswerelatercategorizedassimplyeither
second-growth forest (Wing-banded Antbirds, riparian (stream beds and their occasionally
Myrmornistorquata,VariegatedAntpittas,Gral- floodedbanks)orupland(unfloodedslopesand
laria varia, and Spotted Antpittas, Hy- the higher elevation plateaus). In each plot, we
lopezus macularius), five moderately sensi- counted all trees (woody vegetation > 2 m in
tive species missing from small BDFFP frag- height)andcategorizedthemintofivesizeclasses
ments and that rarely use second-growth based on diameter at breast height (dbh): trees
forest (Ferruginous-backed Antbirds, Myrme- ≤ 7 cm, trees > 7–15 cm, trees > 15–23 cm,
ciza ferruginea, Rufous-capped Antthrushes, trees > 23–30 cm, and trees > 30 cm. There
Formicarius colma, Black-faced Antthrushes, werefewtrees>15cminplotsandhistograms
Formicariusanalis,Chestnut-beltedGnateaters, of counts per plot were highly skewed, so we
Conopophaga aurita, and Ringed Antpipits, usedthreesizeclassesoftreesforanalysis:small
Corythropistorquatus),andThrush-likeAntpit- trees(dbh≤7cm),mediumtrees(dbh>7–15
tas(Myrmotheracampanisona),afragmentation- cm),andlargetrees(dbh>15cm).Wedidnot
tolerant species found in fragments of all sizes identifytreespeciesbecausetreediversityatour
as well as in second-growth forest. Our fo- site is exceptionally high, with more than 200
cal species are present in continuous terra species/haandperhapsasmanyas1000species
firmeforestthroughouttheBDFFP(Cohn-Haft in the area (Prance 1990, Rankin-de-Me´rona
etal.1997,Stouffer2007). et al. 1992). We also counted all palms (Are-
Most birds were observed while we oppor- caceae)>1minheight,andwoodyvinesinthree
tunistically spot-mapped a 500-ha plot in the sizeclasses:vines>0–0.5cmdbh,vines>0.5–
griddedtrailsystematthecontinuousforestsite 2 cm dbh, and vines > 2 cm dbh. We found
(Stouffer 2007). Trails followed compass bear- few vines >0.5 cm dbh, and their histograms
ings, passing through the various topographic of counts per plot were highly skewed, so we
elements in the area, including stream beds, combinedthetwolargersizeclassesofvinesinto
steep stream banks, and flat plateaus. Micro- largevines(dbh>0.5cm).Afterconsolidating
4 J.A.StratfordandP.C.Stouffer
J.FieldOrnithol.
Table1. Morphologicalandbehavioralattributesoftheninefocalspecies.Wealsoindicatefragmentation
sensitivity, or the probability that a species will go locally extinct after fragmentation. Species that are
fragmentation-sensitive will be missing from all fragments, including those ≥ 100 ha in size. Moderately
sensitive species will be missing from the smallest forest fragments, and species that are not sensitive will
befoundinfragmentsofallsizes.Occurrenceofeachspeciesinsecond-growthforestwasbasedonBorges
(1995).
Mass Fragmentation Occursin Foraging
Species Na (g)b sensitivity secondgrowth strategyc
Myrmecizaferruginea 23 26 Moderate Cecropia Surfaceofleaflitter
Ferruginous-backedAntbird
Myrmornistorquata 12 47 Yes Cecropia Tosseslitter
Wing-bandedAntbird
Formicariuscolma 17 47 Moderate Both Surfaceofleaflitter
Rufous-cappedAntthrush
Formicariusanalis 12 62 Moderate No Surfaceofleaflitter
Black-facedAntthrush
Grallariavaria 4 119 Yes Cecropia Surfaceofleaflitter,
VariegatedAntpitta underleaflitter
Hylopezusmacularius 3 44 Yes Cecropia Surfaceofleaflitter
SpottedAntpitta
Myrmotheracampanisona 8 47 No Cecropia Surfaceofleaflitter
Thrush-likeAntpitta
Conopophagaaurita 4 27 Moderate No Surfaceofleaflitter
Chestnut-beltedGnateater
Corythropistorquatus 13 14 Moderate Vismia Undersidesofleaves
RingedAntpipit
aN =numberofsiteswhereeachspecieswasobservedforaging.
bFromDunning(1992).
cBasedonRidgelyandTudor(1994).
thesevariables,weentered15variablesintothe absenceoflivevegetationifvegetationtouched
factoranalysis(Table2). a 1.27-cm-diameter pole with one end placed
In each vegetation plot, an 8-m transect was directly on the sample point. Between 0.5 and
established from the center of the plot to the 3 m, we determined the presence of vegetation
edge in a random direction and a second 8-m if any part of a live plant crossed over an
transectwasestablishedbysubtracting90◦from imaginary line running directly up from the
the original transect. The first direction was samplepoint.Above3m,weusedarangefinder
selectedfromarandomnumbertable(Rohlfand todetermineheightsandsightedthroughatube
Sokal1981).Allnonwoodyplantswithin0.5m with crosshairs. Three evenly spaced hanging
oftransects(i.e.,herbs,grasses,andferns)aswell weightswereplacedinsidethetubetovertically
asallwoodystems<2minheightwerecounted align the tube while the observer straddled the
and placed into two height categories: short point.Whereleaflitterdepthwas<3cmdeep,
plants(height≤1m)andtallplants(height> a pin (38 mm × 0.55 mm) was used to pierce
1–2 m). The total area sampled for plants in leaves until the pin touched soil. The pin was
plots was 15.75 m2. Along the entire length of then removed and the depth of the leaf litter
transects,20pointswererandomlyselectedfrom wasmeasuredtothenearest0.1mmwithdigital
a random number table and, at each point, we calipers. We also counted the number of leaves
measuredleaflitterdepth,countedthenumber the pin pierced. When leaf litter was >3 cm
ofdeadleaves,andnotedthepresenceorabsence deep, we used a 150 mm × 1 mm pin at the
oflivevegetationatfiveheights:<0.5m,>0.5– back end of a dial caliper created by opening
3 m, >3–10 m, >10–20 m, and >20 m. For dial calipers. The pin was pressed through the
heights<0.5m,wedeterminedthepresenceor leavesuntilittouchedsoil.
MicrohabitatsofAmazonianInsectivores 5
Vol.84,No.1
Table 2. Results of factor analysis to identify suites in areas of second growth, we located plots
(factors) of correlated variables for sites where birds at random distances along 500-m trails and
wereobservedforagingandrandomlyselectedsites. random distances within 100 m of the trails.
Weincludedall208samples,includingrandomsites
Trails in second growth were 500 m apart and
in continuous and second-growth forest and sites
were created to sample avian communities in
where focalspecies of birds were observed foraging.
secondary growth (Borges and Stouffer 1999).
Boldednumbersinthesamecolumnrepresentvari-
ableswithloadings>0.50ontoafactor.Underlined To determine the location of points in contin-
variablesarethoseincludedintheBayesiananalysis. uous forest, we randomly selected an intersec-
Removed from the factor analysis were leaf litter tion in the gridded system of trails that runs
depth, trees > 7–15 cm dbh, large vines, number north–south and east–west. From the intersec-
ofVismiastems,andnumberofCecropiastems. tion,werandomlyselectedapointwithin100m
northand100meast.
Variablea Factor1 Factor2 Factor3
Statistical analysis. Using R 2.11.1 (R
LEAFNO 0.538 −0.221 −0.044 DevelopmentCoreTeam2010),weusedfactor
COVHALF −0.912 −0.160 0.113 analysis of the vegetation variables to iden-
COVER10 0.584 0.105 0.201
tify suites (factors) of correlated (redundant)
COVER20 0.625 0.430 0.119
variables for sites where birds were observed
PLANTS1 −0.858 −0.210 −0.013
COVER20+ 0.065 0.798 0.064 foragingandrandomlyselectedsites.Westarted
with six factors and reduced the number until
LGTREE 0.119 0.838 0.164
PALMS 0.131 0.818 0.113 each factor had at least two variables loading
COVER3 −0.088 0.171 0.504 (>0.45) on each factor (Hair et al. 2010). The
PLANTS2 −0.114 0.087 0.625 variables leaf litter depth and medium trees
SMTREE 0.359 0.254 0.779 were removed from the analysis because they
SMVINE 0.290 −0.278 0.537 loaded on the first two and the second and
SSloadings 2.856 2.502 1.653 third factors, respectively. One variable (large
ProportionVar 0.238 0.208 0.138 vines)wasremovedfromthefinalfactoranalysis
CumulativeVar 0.238 0.446 0.584
because it did not load on any of the factors
aLEAFNO: number of dead leaves penetrated by (Hairetal.2010).Fromeachfactor,weselected
a pin; COVHALF: presence or absence of live a single representative variable that could be
vegetation < 0.5 m above ground; COVER10:
easily and accurately measured in the field. We
presence or absence of live vegetation > 3–10 m
decidedtoselectthevariablessmallplants,large
above ground; COVER 20: presence or absence of
livevegetation>10–20maboveground;PLANTS1: trees, and small trees from the three factors for
numberofplants≤1mtall;COVER20+:presence subsequentanalysis.
orabsenceoflivevegetation>20maboveground; We used Bayesian inference to estimate
LGTREE: number of trees with dbh > 15 cm; means, standard deviation, and Bayesian 95%
PALMS: number of palms > 1 m tall; COVER3: credible intervals (Gelman et al. 2003) of the
presence or absence of live vegetation > 0.5–3 m selected subset of variables (small plants, large
aboveground;PLANTS2:numberofplants>1–2 trees, and small trees) and variables removed
mtall;SMTREE:numberoftreeswithdbh≤7cm; fromthefactors(leafdepth,mediumtrees,and
andSMVINE:numberofvineswithdbh≤0.5cm.
largevines). Weused OpenBUGS 3.2.2(Lunn
etal.2000)forallBayesiananalyses.Forcount
variables, we assumed a Poisson distribution of
each observation, but allowed for extra varia-
We also sampled randomly selected points tion around the Poisson mean. For continuous
in continuous forest (N = 44) and in both variables, we assumed a normal distribution
Vismia- (N = 40) and Cecropia-dominated for each observation. We assumed estimates
(N = 28) second-growth forest. Vismia- and of group means were normally distributed and
Cecropia-dominatedsecondgrowthoccurredin useduninformativepriors((cid:2)=0,(cid:3) =0.001),
large(>200ha)patchesinabandonedpastures where (cid:3) is precision and is the inverse of the
between 18 and 38 km from the continuous variance.Wealsouseduninformativepriorsfor
forestsite.Second-growthareaswereinpastures the estimates of group standard deviation. For
abandoned for 10–15 yr and had vegetation eachestimate,weranamillioniterationswitha
at least 2 m in height. To sample vegetation burn-in of 20,000. We estimated means,
6 J.A.StratfordandP.C.Stouffer
J.FieldOrnithol.
standarddeviations,and95%credibleintervals growth also had fewer medium and large trees
forplotswherethestudyspecieswereobserved and large vines than either continuous forest
foraging,forrandomsitesincontinuousforest, or Cecropia-dominated second growth (Figs.
and for random sites in both types of second- 2D–F).
growth forest. Bayesian 95% credible intervals Compared to the continuous forest site,
can be interpreted as standard statistical tests Cecropia-dominated second growth had fewer
(Gelmanetal.2003).Meansandstandarddevi- small plants, with just six small plants/transect
ationsfortheoriginalvariablesusingtraditional (Fig. 2B), but a similar number of small
methodsareavailableinStratford(1997). trees (Fig. 2C) as continuous forest. Ce-
cropia-dominatedsecondgrowthalsohadmore
medium trees than continuous forest sites
RESULTS
(Fig. 2D). Large trees were largely absent from
We quantified the characteristics of 96 sites Cecropia-dominated second growth, with an
where our focal species were observed foraging averageofonelargetreepersample.However,if
and 112 randomly selected sites (continuous largeandmediumtreesizeclasseswerepooled,
forest N = 44, Vismia second growth N = thereweresimilarnumbersoftreesinCecropia-
40, and Cecropia second growth N = 28). All dominatedsecondgrowth(∼21trees/plot)and
observations of foraging birds were in continu- continuousforest(∼18trees/plot).
ous forest except for two Thrush-like Antpittas Topography and microhabitats of sites
observedinCecropia-dominatedsites. used by terrestrial insectivores. Five of
Factor analysis was able to capture 58% of the nine terrestrial insectivores (Rufous-capped
the total variance in the vegetation data in Antthrushes, Thrush-like Antpittas, Spotted
three factors (Table 2). The first factor was Antpittas, Variegated Antpittas, and Chestnut-
associatedwiththegroundandmidstorylayers beltedGnateaters)wereonlyobservedinupland
and accounted for 24% of the total variance. sites(Fig.1).Black-facedAntthrushesweremost
Fromthisfactor,weidentifiedsmallplantsasan associated with riparian habitats, with nearly
elementofthegroundlayerthatwouldbeeasyto one-third (0.31) of all observations in riparian
measure.Thesecondfactorwasassociatedwith areas.
elementsofthecanopyandaccountedfor21% None of the 95% credible intervals for leaf
ofthetotalvariance.Weselectedlargetreesfrom litterdepthatsiteswhereterrestrialinsectivores
this factor as the variable that would describe were observed exceeded those of random sam-
thecanopyandwaseasytomeasure.Thethird ples from continuous forest (Fig. 2A). None of
factor was associated with the midstory and our nine focal species were observed foraging
accounted for 14% of the variance. From this at sites with leaf litter as thick as the leaf
factor, we selected small trees as the variable litter in Cecropia-dominated second growth,
thatwouldbeeasilymeasuredanddescribedthe which was ∼4 cm thicker than the leaf litter
midstory. at sites where our focal species were observed
Microhabitats and topography in foraging. Ferruginous-backed Antbirds, Wing-
second-growth versus continuous forest. banded Antbirds, Rufous-capped Antthrushes,
Riparian sites were found in all three habitats, Black-facedAnttrushes,andVariegatedAntpit-
although second-growth areas had fewer than tas were observed foraging in areas with less
the continuous forest (Fig. 1). The vegetation leaf litter than that in Vismia-dominated sec-
structure of the two types of second growth ond growth (Fig. 2A). Leaf litter depths where
differed from that of continuous forest. Leaf we observed Thrush-like Antpittas, Chestnut-
litter in Vismia- and Cecropia-dominated belted Gnateaters, and Ringed Antpipits forag-
second growth was ∼1 and 4 cm thicker, ing overlapped the leaf litter depth in Vismia-
respectively,thanincontinuousforest(Fig.2A). dominated second growth. Variation in leaf
Structurally, Vismia-dominated second growth litterdepthwhereantpittasandChestnut-belted
had more small plants than either continuous Gnateaters foraged was greater than that where
forest or Cecropia-dominated second growth the other focal species foraged and at random
(Fig. 2B) and more small trees than Cecropia- sitesincontinuousforest(Fig.2A).Amongour
dominated second growth and continuous focalspecies,onlyFerruginous-backedAntbirds
forest (Fig. 2C). Vismia-dominated second and Thrush-like Antpittas differed from each
MicrohabitatsofAmazonianInsectivores 7
Vol.84,No.1
Fig.1. Proportionofsitesthatwereriparian(waterflowingorflooded)andupland(neverflooded)forplots
incontinuousforest,secondgrowthorwherethefocalspecieswereobservedforaging.
other, with Thrush-like Antpittas foraging at Random sites in Vismia-dominated second
sites with deeper leaf litter than Ferruginous- growth had far fewer medium trees than sites
backedAntbirds(Fig.2A). whereallthefocalspecieswereobservedforaging
Thenumbersofsmallplantsinrandomplots (Fig. 2D). For large trees, only sites where
in continuous forest sites and sites in Vismia- Thrush-like Antpittas were observed foraging
dominatedsecondgrowthoverlappedwiththose had fewer large trees than random sites in
oftheforagingsitesofallfocalspecies(Fig.2B). continuous forest (Fig. 2E). Foraging sites of
However, none of the sites where our focal all nine focal species had more large trees than
species were observed foraging had as few randomlyselectedsitesineithertypeofsecond
small plants as the random plots in Cecropia- growth. However, the number of large vines at
dominated second growth. Variation in the sites where most of the focal species foraged
number of small plants at sites where we ob- did not differ from that in the random sites in
servedantpittasandChestnut-beltedGnateaters continuous forest; the only exception was that
foragingwasgreaterthanthatatsiteswherethe therewerefewerlargevinesatsiteswhereRinged
other focal species foraged and at random sites Antpipitsforaged(Fig.2F).Allsiteswherefocal
inthethreeavailablehabitats(Fig.2B). species were observed foraging had more large
The number of small trees at sites where vines than random sites in Vismia-dominated
our focal species foraged was similar to that secondgrowth.
at randomly selected sites in the continuous In general, microhabitats available in sec-
forest (Fig. 2C). There were more small trees ondary growth differed from those available
in Cecropia-dominated second growth than in in continuous forest. The deeper leaf litter in
microhabitatsusedbythetwoantthrushes;oth- both types of second growth was a particularly
erwise, the number of small trees in Cecropia- strikingdifferencethatmaybedirectlyrelevant
dominatedsecondgrowthwassimilartothatat to foraging by terrestrial birds; most of our
sites used by our focal species. The number of focal species preferred the shallower leaf litter
smalltreesinVismia-dominatedsecondgrowth available in continuous forest (Fig. 2A). We
alsoexceeded thenumberofsmalltreesatsites foundasimilarpatternwiththenumberoflarge
used by Chestnut-belted Gnateaters, Ringed trees, with most of our focal species preferring
Antpipits,andthetwoantthrushes.Siteswhere areas of continuous forest with relatively high
thetwospeciesofantthrushesforagedhadfewer numbersoflargetrees(Fig.2E).Othervariables
small trees than sites used by four other focal exhibited more variation among focal species,
species (Ferruginous-banded Antbird, Ringed and characteristics of sites used by our focal
Antpipit, Thrush-like Antpitta, and Variegated species sometimes differed from one or both
Antpitta). typesofsecond-growthforest.
8 J.A.StratfordandP.C.Stouffer
J.FieldOrnithol.
Fig.2. Bayesianestimatesofmeans(circles),standarddeviations(boxes),andcredibleintervals(verticallines)
for (A) leaf litter depth, (B) plants ≤ 1 m tall, (C) small trees (dbh ≤ 7 cm), (D) medium trees (dbh >
7–15cm),(E)largetrees(dbh>15cm),and(F)largevines(dbh>0.5cm)atsiteswhereninespeciesof
terrestrial insectivores were observed foraging and at randomly selected sites in the three types of available
habitat(continuousforestandCecropia-andVismia-dominatedsecondgrowth).Dottedhorizontallinesshow
theupperandlowerboundsofthestandarddeviationsforrandomlyselectedsitesinthecontinuousforest
sitesforcomparisonwithsiteswherebirdswereobservedforagingandrandomlyselectedsitesinVismia-and
Cecropia-dominatedsecondgrowth.
MicrohabitatsofAmazonianInsectivores 9
Vol.84,No.1
DISCUSSION study. Thrush-like Antpittas in our study pre-
ferred microhabitats that had dense understory
We found that most microhabitat charac-
vegetation and fewer large trees, characteristics
teristics of sites where our nine focal species
typical of young treefall gaps (Fetcher et al.
of Neotropical terrestrial insectivores foraged
1985). Thrush-like Antpittas are also found
broadly overlapped those of randomly selected
in forest fragments and second growth; their
sites in continuous forest. However, our focal
association with scrubbier vegetation in con-
species foraged in microhabitats that differed
tinuous forest may allow this species to persist
from those in second-growth forest in several
in fragmented landscapes, at least those that
respects, including leaf litter depth, density of
includesomeforestandsecond-growthareas.
small plants and trees, and density of large
Compared to second growth, microhabitat
trees.Ourfocalspeciesaregenerallyabsentfrom
associations of our focal species in continuous
second-growthareas(BorgesandStouffer1999)
forest were more subtle, with more overlap in
and our results are consistent with the hypoth-
thecharacteristicsofforagingsitesandrandomly
esisthatmicrohabitatdifferencesmakesecond-
selected sites. The density of small nonwoody
growth forests unsuitable for our focal species.
plants, for instance, was more variable at sites
Inparticular,thethickleaflitterofVismia-and
used by our focal species than at randomly
Cecropia-dominated second growth may inter-
selected sites, but reasons for such a difference
fere with normal foraging behaviors. Although
are unclear. Thedensities ofmediumand large
StoufferandBierregaard(1995)andBorgesand
trees in plots where birds foraged were similar
Stouffer(1999)foundthatourfocalspeciesmay
amongspeciesandtothoseofrandomlyselected
use Cecropia-dominated second growth more
sites in continuous forest. In addition, the leaf
readily than Vismia-dominated second growth,
litter depth at sites where our focal species
Cecropia leaves are typically 30–40 cm across
foragedwassimilartothatatrandomlyselected
(Parolin 2002) and their presence in the leaf
sites in continuous forest. Our focal species
litter may impede foraging behavior or even
also preferred drier sites, which were available
terrestrialmovement.Thiswouldbeparticularly
throughoutthecontinuousforestsite.
trueforspeciesthatforagebyactivelytossingleaf
Thetwoantthrushspeciesinourstudywere
litter, such as Wing-banded Antbirds. Ringed
associated with sites with fewer small trees,
Antpipits, which glean from live leaves as they
whereas Variegated Antpittas and Ferruginous-
walk,mayalsofindCecropia-dominatedsecond
backedAntbirdswereassociatedwithsiteswith
growthsuboptimalforforagingbecauseplants<
moresmalltrees.Forlargevines,onlysitesused
1minheightweresparseinthishabitat.
by Ringed Antpipits differed from randomly
Our focal species may also avoid second-
selectedsites,usingsiteswithrelativelyfewlarge
growth forests due to microclimate conditions
vines. Although the reasons for these apparent
that are correlated with vegetation structure
preferences are unclear, these subtle microhab-
or edaphic conditions. For example, Karr and
itat associations might explain the patchiness
Freemark (1983) found that understory birds
of distributions in continuous forest. Stouffer
in Panama were associated with specific mi-
(2007), for example, studied the same focal
croclimate conditions and changed their use
species as in our study and found that they
of the forest during the year, indicating the
were patchily distributed in the 100-ha plot
relative importance of microclimate compared
extensivelysearchedinourstudy,with,onaver-
to vegetation. In the tropics, the near-ground
age,two-thirdsofthestudyplotunoccupiedby
microclimate of second-growth forests is both
particularspecies.InNorthAmericandeciduous
hotteranddrierthanthatincontinuousforests
forests, the distributions of terrestrial insecti-
(Fetcheretal.1985,UhlandKauffman1990),
vores are closely tied to microhabitat features
andsuchenvironmentalconditionsmayexceed
(Holmes and Robinson 1988). In Neotropical
thephysiologicaltolerancesofourfocalspecies
forests, terrestrial insectivores and other under-
(StratfordandRobinson2005).
storybirdshavebeenfoundtoshowpreferences
Microhabitatcharacteristicsmayalsoexplain
forparticularrangesofsoilcomposition(Bueno
whyThrush-likeAntpittas,associatedwithlarge
et al. 2011, Pomara et al. 2012), and topology
treefalls in continuous forest (Stouffer 2007),
andforeststructure(MarraandRemsen1997),
were able to use second-growth forests in our
which are potentially confounded (Cintra and
10 J.A.StratfordandP.C.Stouffer
J.FieldOrnithol.
Naka2012).Tobetterunderstandrelationships theDirectoroftheLouisianaStateUniversityAgricultural
between microhabitat characteristics and the Centerasmanuscriptnumber2012-241-7682.
distribution of terrestrial insectivores, experi-
mental studies involving habitat manipulations LITERATURECITED
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