Journal of Field Ornithology - Louisiana State University of Field Ornithology C 2013 Association of Field Ornithologists C 1 Journal of Field Ornithology. 2 J. A. Stratford and P

J. Field Ornithol. 84(1):1–12, 2013 DOI: 10.1111/jofo.12000

Microhabitat associations of terrestrial insectivorousbirds in Amazonian rainforest and second-growth forests

Jeffrey A. Stratford1,3 and Philip C Stouffer2

1Department of Health and Biological Sciences, Wilkes University, Wilkes-Barre, Pennsylvania 18766, USA2School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, Louisiana

70803-6202, USA

Received 12 January 2012; accepted 29 October 2012

ABSTRACT. Across the Neotropics, small-bodied terrestrial insectivores are sensitive to forest fragmentationand are largely absent from second-growth forests. Despite their sensitivity to forest structure, the microhabitatrelationships of these birds have not been quantified. From July 1994 to January 1995 in central Amazonia, wecharacterized habitat at sites where nine species of terrestrial insectivores were observed foraging, as well as atrandomly selected sites in continuous forest and two types of 10–15-yr-old second-growth forest common inAmazonia (Vismia- and Cecropia-dominated). We used factor analysis to find suites of correlated variables. Fromeach factor, we selected a representative variable that was relatively easy to measure. We used Bayesian analysis toestimate means and standard deviations of these variables for each species and for each type of habitat. All ninefocal species were associated with ranges of microhabitat variables, such as leaf litter depth and tree densities, oftenabsent in second-growth forests. At least in the early stages of regeneration, neither type of second-growth forestprovides suitable structure for the terrestrial insectivores in our study. The large leaves of Cecropia trees that makeup the thick leaf litter may preclude the use of Cecropia-dominated second growth by our focal species, many ofwhich manipulate leaves when foraging. The leaf litter in Vismia-dominated second growth was also thicker thansites used for foraging by our focal species. In addition, Vismia-dominated growth had more small trees and smallnonwoody vegetation, perhaps impeding movement by terrestrial birds. In continuous forest, our focal speciesforaged in microhabitats with characteristics that generally overlapped those of randomly selected sites. Thus, ourresults are consistent with the hypothesis that microhabitat differences make second-growth forests unsuitable forour focal species.

RESUMEN. Asociacion de aves insectıvoras terrestres con el micro habitat en la selvaAmazonica y bosques de crecimiento secundario

A lo largo del Neotropico, aves insectıvoras terrestres de tamano corporal pequeno son sensibles a la fragmentaciondel bosques y en gran parte estan ausentes en los bosques de crecimiento secundario. A pesar de su sensibilidada la estructura del bosque, las relaciones de estas aves con el micro habitat no han sido cuantificadas. Desdejulio de 1994 hasta enero de 1995 en la Amazonia central caracterizamos habitats en lugares en donde nueveespecies de aves insectıvoros terrestres fueron observadas buscado alimento, al igual que en lugares seleccionadosaleatoriamente en un bosque continuo y en dos tipos de bosques secundarios de 10 y 15 anos, comunes en laAmazonia (Vismia-dominado y Cecropia-dominado). Usamos un analisis factorial para encontrar el conjunto devariable que se correlacionaron. Tambien usamos un analisis bayesiano para estimar el promedio y las desviacionesestandar de estas variables para cada especie y cada tipo de habitat. Las nueve especies focales se asociaron conelementos variables del micro habitat, tales como profundidad de la hojarasca y densidad de arboles, usualmenteausentes en bosques de crecimiento secundario. Al menos en los estadios tempranos de regeneracion ninguno de lostipos de crecimiento secundario provee una estructura adecuada para los insectıvoros terrestres de nuestro estudio.Las largas hojas de los arboles de Cecropia que crean una hojarasca mas gruesa pueden evitar el uso de bosques decrecimiento secundario dominado Cecropia por parte de nuestras especies focales, muchas de las cuales manipulanhojas cuando estan buscando alimento. La hojarasca de los bosques de crecimiento secundario dominados porVismia tambien fue mas gruesa respecto a los lugares usados por nuestras especies focales para buscar alimento.Adicionalmente, los bosques dominados por Vismia tuvieron mas arboles pequenos y pequena vegetacion no lenosa,que puede impedir el movimiento de las aves terrestres. En bosques continuos, nuestras especies focales buscaronalimento en micro habitats con caracterısticas que generalmente se superpusieron con las de los lugares escogidosaleatoriamente. En consecuencia, nuestros resultados son consistentes con la hipotesis que diferencias en microhabitat hacen que los bosques de crecimiento secundario sean lugares inadecuados para nuestras especies focales.

Key words: Conopophaga, Corythopis, Formicarius, Grallaria,habitat selection, Hylopezus, microhabitat,Myrmornis, Myrmothera, terrestrial insectivores, vegetation structure

3Corresponding author. Email: [email protected]

Studies of Neotropical birds have revealed thatmost small-bodied terrestrial insectivores aresensitive to forest fragmentation (Stouffer andBierregaard 1995, Robinson 1999, Stratford

C©2013 The Authors. Journal of Field Ornithology C©2013 Association of Field Ornithologists

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2 J. A. Stratford and P. C. Stouffer J. Field Ornithol.

and Stouffer 1999). Other studies have con-firmed the sensitivity of terrestrial insectivoresto fragmentation (Kattan 1992, Renjifo 1999,Sekercioglu et al. 2002, Lees and Peres 2010),selective logging (Mason 1996, Aleixo 1999,Bicknell and Peres 2010), and other forms ofhabitat modification such as plantations (Cana-day 1997, Barlow et al. 2007). In addition,most Neotropical insectivorous birds are rarelyfound in young (<15 yr) second growth (Borgesand Stouffer 1999, Blake and Loiselle 2001)that initially develops when deforested areas areabandoned (Borges and Stouffer 1999, Wrightand Muller-Landau 2006). However, as secondgrowth ages, terrestrial insectivores are morelikely to move through it (Blake and Loiselle2001, Antongiovanni and Metzger 2005). Forexample, temporal changes in the abundanceof birds in fragments of Brazil’s Biological Dy-namics of Forest Fragments Project (BDFFP)were found to be strongly influenced by the ageand type of second-growth matrix surroundingthe fragments (Stouffer and Bierregaard 1995,Stouffer et al. 2006, 2011). Fragments sur-rounded by Cecropia-dominated second growthregained more species of birds lost after frag-mentation than fragments surrounded by Vis-mia-dominated second growth (Stouffer andBierregaard 1995). The area consisting of sec-ond growth is rapidly expanding across theAmazon (Neeff et al. 2006, Foley et al. 2007),and understanding how terrestrial insectivoresrespond to the different types and ages of secondgrowth is crucial to their conservation (Anton-giovanni and Metzger 2005, Gardner et al. 2007,Chazdon 2008).

Several hypotheses have been proposed toexplain why terrestrial insectivores are sensitiveto alteration of forest structure (Stratford andRobinson 2005). One hypothesis is that ter-restrial insectivores are closely associated with aparticular forest physiognomy and topographyand, if key elements are missing, terrestrial insec-tivores avoid these areas (Stratford and Robinson2005). This hypothesis is difficult to test becausethe microhabitats (physiognomy) used by mostterrestrial insectivores have yet to be evaluated,with microhabitat defined as a subset of habitat(e.g., continuous forest) with particular environ-mental conditions, including vegetation struc-ture (James 1971). Due to microhabitat prefer-ences, areas within broadly suitable habitat maygo unused for a particular species. Understand-

ing such microhabitat associations is necessaryfor predicting responses to forest fragmentation,selective logging, and other activities that alterforest structure (Holmes and Robinson 1981,Deppe and Rotenberry 2008).

Our objective was to provide a quantitativedescription of the microhabitat associations ofnine species of terrestrial insectivores in a well-studied Amazonian forest. By comparing thecharacteristics of microhabitats where birds for-age to those of randomly selected sites in con-tinuous forest and second-growth sites, we cangain a better understanding of habitat selectionby terrestrial insectivores. Typical of microhab-itat studies, we quantified several microhabi-tat variables that we believed were potentiallyimportant to terrestrial insectivores. However,collecting these data took considerable time andeffort so a secondary objective was to identify areduced set of variables to recommend for use infuture studies of these species.

METHODS

Study sites. From July 1994 to January1995, we collected microhabitat data at sites thatwere part of the BDFFP, a large-scale, long-termresearch project sponsored by the SmithsonianTropical Research Institute and Brazil’s NationalInstitute for Amazon Research (Bierregaard andGascon 2001). The continuous forest site islocated in terra firme forest ∼60 km north ofManaus, Brazil (see http://pdbff.inpa.gov.br/ formaps). Annual rainfall averages 2500 mm witha distinct rainy season from February to May(Stouffer and Bierregaard 1993). Soils in thearea are sandy and nutrient poor (Laurance et al.1999), but tree diversity is exceptionally high(Oliveira and Mori 1999). At the continuousforest site, canopy height varied, but is typicallybetween 30 and 37 m (Gascon and Bierregaard2001). Lianas and vines are common (Roederet al. 2010) and the understory is dominated bypalms such as Astrocaryum spp. and Bactris spp.(Scariot 1999, de Castilho et al. 2006). Smallstreams, often with steep banks, dissect the area.Higher, flat areas or plateaus are found betweenstreams (Bueno et al. 2011, Cintra and Naka2012). Isolated treefalls and blowdowns occursporadically throughout the site (Nelson et al.1994). The continuous forest site is embeddedwithin a large forest that is largely intact forhundreds of kilometers with the exception of

Vol. 84, No. 1 Microhabitats of Amazonian Insectivores 3

Manaus, a large urban center. A gridded trailsystem was set up at the continuous forest sitewith parallel trails spaced every 100 m.

The BDFFP study area includes large patchesof second growth (see map in Stratford andStouffer 1999). Most of the second growth isone of two types that are largely distinct in theearly stages of regeneration (Norden et al. 2011).Patches of second growth we sampled were10–15 yr old. At this age, Cecropia dominatesareas that were cut and abandoned, whereasVismia-dominated second growth occurs wherethe forest was burned before abandonment(Mesquita et al. 2001). Floristically, Cecropia-dominated second growth has more plantspecies and families than Vismia-dominated ar-eas (Mesquita et al. 2001).

Bird and vegetation sampling. Our fo-cal species were terrestrial insectivores witha range of responses to fragmentation andsecond-growth forest (Borges and Stouffer 1999,Stratford and Stouffer 1999; Table 1). Sen-sitivity to fragmentation was determined bythe probability that a species will go locallyextinct after fragmentation (Stratford and Stouf-fer 1999). We sampled three fragmentation-sensitive species that were missing from all ormost BDFFP fragments and that did not usesecond-growth forest (Wing-banded Antbirds,Myrmornis torquata, Variegated Antpittas, Gral-laria varia, and Spotted Antpittas, Hy-lopezus macularius), five moderately sensi-tive species missing from small BDFFP frag-ments and that rarely use second-growthforest (Ferruginous-backed Antbirds, Myrme-ciza ferruginea, Rufous-capped Antthrushes,Formicarius colma, Black-faced Antthrushes,Formicarius analis, Chestnut-belted Gnateaters,Conopophaga aurita, and Ringed Antpipits,Corythropis torquatus), and Thrush-like Antpit-tas (Myrmothera campanisona), a fragmentation-tolerant species found in fragments of all sizesas well as in second-growth forest. Our fo-cal species are present in continuous terrafirme forest throughout the BDFFP (Cohn-Haftet al. 1997, Stouffer 2007).

Most birds were observed while we oppor-tunistically spot-mapped a 500-ha plot in thegridded trail system at the continuous forest site(Stouffer 2007). Trails followed compass bear-ings, passing through the various topographicelements in the area, including stream beds,steep stream banks, and flat plateaus. Micro-

habitats were sampled only where birds wereobserved foraging and, to avoid sampling areasused by the same individuals, we only consideredindividuals observed >500 m from a previousobservation of a bird of the same species. Thesite of each initial observation served as thecenter of an 8-m-radius (∼0.02 ha) vegetationsampling plot. We chose 8-m radius samplingunits as a compromise between being consistentwith published methods, i.e., James and Shugart(1970) and Marra and Remsen (1997) used 10-m-radii sample units, and our desire to finelyquantify foraging microhabitat used by our focalspecies. In addition, small-scale sampling unitscan capture the vegetation structure associatedwith the edges and interiors of treefalls in tropi-cal forests (Fetcher et al. 1985, Uhl et al. 1988).

We quantified vegetation using a modifiedversion of methods described by James andShugart (1970). Within each plot, we measured23 variables to quantify vegetation structureand topography. For topography, we noted ifthe center of a plot was in a stream bed (flatareas adjacent to running water) or on a streambank (signs of flooding, such as leaf packs),dry slope (no signs of flooding), or flat plateau(higher areas with no slope). Due to small samplesizes, plots were later categorized as simply eitherriparian (stream beds and their occasionallyflooded banks) or upland (unflooded slopes andthe higher elevation plateaus). In each plot, wecounted all trees (woody vegetation > 2 m inheight) and categorized them into five size classesbased on diameter at breast height (dbh): trees≤ 7 cm, trees > 7–15 cm, trees > 15–23 cm,trees > 23–30 cm, and trees > 30 cm. Therewere few trees >15 cm in plots and histogramsof counts per plot were highly skewed, so weused three size classes of trees for analysis: smalltrees (dbh ≤ 7 cm), medium trees (dbh > 7–15cm), and large trees (dbh > 15 cm). We did notidentify tree species because tree diversity at oursite is exceptionally high, with more than 200species/ha and perhaps as many as 1000 speciesin the area (Prance 1990, Rankin-de-Meronaet al. 1992). We also counted all palms (Are-caceae) >1 m in height, and woody vines in threesize classes: vines > 0–0.5 cm dbh, vines > 0.5–2 cm dbh, and vines > 2 cm dbh. We foundfew vines >0.5 cm dbh, and their histogramsof counts per plot were highly skewed, so wecombined the two larger size classes of vines intolarge vines (dbh > 0.5 cm). After consolidating


Table 1. Morphological and behavioral attributes of the nine focal species. We also indicate fragmentationsensitivity, or the probability that a species will go locally extinct after fragmentation. Species that arefragmentation-sensitive will be missing from all fragments, including those ≥ 100 ha in size. Moderatelysensitive species will be missing from the smallest forest fragments, and species that are not sensitive willbe found in fragments of all sizes. Occurrence of each species in second-growth forest was based on Borges(1995).

Mass Fragmentation Occurs in ForagingSpecies N a (g)b sensitivity second growth strategyc

Myrmeciza ferruginea 23 26 Moderate Cecropia Surface of leaf litterFerruginous-backed Antbird

Myrmornis torquata 12 47 Yes Cecropia Tosses litterWing-banded Antbird

Formicarius colma 17 47 Moderate Both Surface of leaf litterRufous-capped Antthrush

Formicarius analis 12 62 Moderate No Surface of leaf litterBlack-faced Antthrush

Grallaria varia 4 119 Yes Cecropia Surface of leaf litter,Variegated Antpitta under leaf litter

Hylopezus macularius 3 44 Yes Cecropia Surface of leaf litterSpotted Antpitta

Myrmothera campanisona 8 47 No Cecropia Surface of leaf litterThrush-like Antpitta

Conopophaga aurita 4 27 Moderate No Surface of leaf litterChestnut-belted Gnateater

Corythropis torquatus 13 14 Moderate Vismia Undersides of leavesRinged Antpipit

aN = number of sites where each species was observed foraging.bFrom Dunning (1992).cBased on Ridgely and Tudor (1994).

these variables, we entered 15 variables into thefactor analysis (Table 2).

In each vegetation plot, an 8-m transect wasestablished from the center of the plot to theedge in a random direction and a second 8-mtransect was established by subtracting 90◦ fromthe original transect. The first direction wasselected from a random number table (Rohlf andSokal 1981). All nonwoody plants within 0.5 mof transects (i.e., herbs, grasses, and ferns) as wellas all woody stems <2 m in height were countedand placed into two height categories: shortplants (height ≤ 1 m) and tall plants (height >1–2 m). The total area sampled for plants inplots was 15.75 m2. Along the entire length oftransects, 20 points were randomly selected froma random number table and, at each point, wemeasured leaf litter depth, counted the numberof dead leaves, and noted the presence or absenceof live vegetation at five heights: <0.5 m, >0.5–3 m, >3–10 m, >10–20 m, and >20 m. Forheights <0.5 m, we determined the presence or

absence of live vegetation if vegetation toucheda 1.27-cm-diameter pole with one end placeddirectly on the sample point. Between 0.5 and3 m, we determined the presence of vegetationif any part of a live plant crossed over animaginary line running directly up from thesample point. Above 3 m, we used a rangefinderto determine heights and sighted through a tubewith crosshairs. Three evenly spaced hangingweights were placed inside the tube to verticallyalign the tube while the observer straddled thepoint. Where leaf litter depth was <3 cm deep,a pin (38 mm × 0.55 mm) was used to pierceleaves until the pin touched soil. The pin wasthen removed and the depth of the leaf litterwas measured to the nearest 0.1 mm with digitalcalipers. We also counted the number of leavesthe pin pierced. When leaf litter was >3 cmdeep, we used a 150 mm × 1 mm pin at theback end of a dial caliper created by openingdial calipers. The pin was pressed through theleaves until it touched soil.


Table 2. Results of factor analysis to identify suites(factors) of correlated variables for sites where birdswere observed foraging and randomly selected sites.We included all 208 samples, including random sitesin continuous and second-growth forest and siteswhere focal species of birds were observed foraging.Bolded numbers in the same column represent vari-ables with loadings >0.50 onto a factor. Underlinedvariables are those included in the Bayesian analysis.Removed from the factor analysis were leaf litterdepth, trees > 7–15 cm dbh, large vines, numberof Vismia stems, and number of Cecropia stems.

Variablea Factor1 Factor2 Factor3

LEAFNO 0.538 −0.221 −0.044COVHALF −0.912 −0.160 0.113COVER10 0.584 0.105 0.201COVER20 0.625 0.430 0.119PLANTS1 −0.858 −0.210 −0.013COVER20+ 0.065 0.798 0.064LGTREE 0.119 0.838 0.164PALMS 0.131 0.818 0.113COVER3 −0.088 0.171 0.504PLANTS2 −0.114 0.087 0.625SMTREE 0.359 0.254 0.779SMVINE 0.290 −0.278 0.537SS loadings 2.856 2.502 1.653Proportion Var 0.238 0.208 0.138Cumulative Var 0.238 0.446 0.584aLEAFNO: number of dead leaves penetrated bya pin; COVHALF: presence or absence of livevegetation < 0.5 m above ground; COVER10:presence or absence of live vegetation > 3–10 mabove ground; COVER 20: presence or absence oflive vegetation > 10–20 m above ground; PLANTS1:number of plants ≤ 1 m tall; COVER20+: presenceor absence of live vegetation > 20 m above ground;LGTREE: number of trees with dbh > 15 cm;PALMS: number of palms > 1 m tall; COVER3:presence or absence of live vegetation > 0.5–3 mabove ground; PLANTS 2: number of plants > 1–2m tall; SMTREE: number of trees with dbh ≤ 7 cm;and SMVINE: number of vines with dbh ≤ 0.5 cm.

We also sampled randomly selected pointsin continuous forest (N = 44) and in bothVismia- (N = 40) and Cecropia-dominated(N = 28) second-growth forest. Vismia- andCecropia-dominated second growth occurred inlarge (>200 ha) patches in abandoned pasturesbetween 18 and 38 km from the continuousforest site. Second-growth areas were in pasturesabandoned for 10–15 yr and had vegetationat least 2 m in height. To sample vegetation

in areas of second growth, we located plotsat random distances along 500-m trails andrandom distances within 100 m of the trails.Trails in second growth were 500 m apart andwere created to sample avian communities insecondary growth (Borges and Stouffer 1999).To determine the location of points in contin-uous forest, we randomly selected an intersec-tion in the gridded system of trails that runsnorth–south and east–west. From the intersec-tion, we randomly selected a point within 100 mnorth and 100 m east.

Statistical analysis. Using R 2.11.1 (RDevelopment Core Team 2010), we used factoranalysis of the vegetation variables to iden-tify suites (factors) of correlated (redundant)variables for sites where birds were observedforaging and randomly selected sites. We startedwith six factors and reduced the number untileach factor had at least two variables loading(>0.45) on each factor (Hair et al. 2010). Thevariables leaf litter depth and medium treeswere removed from the analysis because theyloaded on the first two and the second andthird factors, respectively. One variable (largevines) was removed from the final factor analysisbecause it did not load on any of the factors(Hair et al. 2010). From each factor, we selecteda single representative variable that could beeasily and accurately measured in the field. Wedecided to select the variables small plants, largetrees, and small trees from the three factors forsubsequent analysis.

We used Bayesian inference to estimatemeans, standard deviation, and Bayesian 95%credible intervals (Gelman et al. 2003) of theselected subset of variables (small plants, largetrees, and small trees) and variables removedfrom the factors (leaf depth, medium trees, andlarge vines). We used OpenBUGS 3.2.2 (Lunnet al. 2000) for all Bayesian analyses. For countvariables, we assumed a Poisson distribution ofeach observation, but allowed for extra varia-tion around the Poisson mean. For continuousvariables, we assumed a normal distributionfor each observation. We assumed estimatesof group means were normally distributed andused uninformative priors (� = 0, � = 0.001),where � is precision and is the inverse of thevariance. We also used uninformative priors forthe estimates of group standard deviation. Foreach estimate, we ran a million iterations with aburn-in of 20,000. We estimated means,


standard deviations, and 95% credible intervalsfor plots where the study species were observedforaging, for random sites in continuous forest,and for random sites in both types of second-growth forest. Bayesian 95% credible intervalscan be interpreted as standard statistical tests(Gelman et al. 2003). Means and standard devi-ations for the original variables using traditionalmethods are available in Stratford (1997).

RESULTS

We quantified the characteristics of 96 siteswhere our focal species were observed foragingand 112 randomly selected sites (continuousforest N = 44, Vismia second growth N =40, and Cecropia second growth N = 28). Allobservations of foraging birds were in continu-ous forest except for two Thrush-like Antpittasobserved in Cecropia-dominated sites.

Factor analysis was able to capture 58% ofthe total variance in the vegetation data inthree factors (Table 2). The first factor wasassociated with the ground and midstory layersand accounted for 24% of the total variance.From this factor, we identified small plants as anelement of the ground layer that would be easy tomeasure. The second factor was associated withelements of the canopy and accounted for 21%of the total variance. We selected large trees fromthis factor as the variable that would describethe canopy and was easy to measure. The thirdfactor was associated with the midstory andaccounted for 14% of the variance. From thisfactor, we selected small trees as the variablethat would be easily measured and described themidstory.

Microhabitats and topography insecond-growth versus continuous forest.Riparian sites were found in all three habitats,although second-growth areas had fewer thanthe continuous forest (Fig. 1). The vegetationstructure of the two types of second growthdiffered from that of continuous forest. Leaflitter in Vismia- and Cecropia-dominatedsecond growth was ∼1 and 4 cm thicker,respectively, than in continuous forest (Fig. 2A).Structurally, Vismia-dominated second growthhad more small plants than either continuousforest or Cecropia-dominated second growth(Fig. 2B) and more small trees than Cecropia-dominated second growth and continuousforest (Fig. 2C). Vismia-dominated second

growth also had fewer medium and large treesand large vines than either continuous forestor Cecropia-dominated second growth (Figs.2D–F).

Compared to the continuous forest site,Cecropia-dominated second growth had fewersmall plants, with just six small plants/transect(Fig. 2B), but a similar number of smalltrees (Fig. 2C) as continuous forest. Ce-cropia-dominated second growth also had moremedium trees than continuous forest sites(Fig. 2D). Large trees were largely absent fromCecropia-dominated second growth, with anaverage of one large tree per sample. However, iflarge and medium tree size classes were pooled,there were similar numbers of trees in Cecropia-dominated second growth (∼21 trees/plot) andcontinuous forest (∼18 trees/plot).

Topography and microhabitats of sitesused by terrestrial insectivores. Five ofthe nine terrestrial insectivores (Rufous-cappedAntthrushes, Thrush-like Antpittas, SpottedAntpittas, Variegated Antpittas, and Chestnut-belted Gnateaters) were only observed in uplandsites (Fig. 1). Black-faced Antthrushes were mostassociated with riparian habitats, with nearlyone-third (0.31) of all observations in riparianareas.

None of the 95% credible intervals for leaflitter depth at sites where terrestrial insectivoreswere observed exceeded those of random sam-ples from continuous forest (Fig. 2A). None ofour nine focal species were observed foragingat sites with leaf litter as thick as the leaflitter in Cecropia-dominated second growth,which was ∼4 cm thicker than the leaf litterat sites where our focal species were observedforaging. Ferruginous-backed Antbirds, Wing-banded Antbirds, Rufous-capped Antthrushes,Black-faced Anttrushes, and Variegated Antpit-tas were observed foraging in areas with lessleaf litter than that in Vismia-dominated sec-ond growth (Fig. 2A). Leaf litter depths wherewe observed Thrush-like Antpittas, Chestnut-belted Gnateaters, and Ringed Antpipits forag-ing overlapped the leaf litter depth in Vismia-dominated second growth. Variation in leaflitter depth where antpittas and Chestnut-beltedGnateaters foraged was greater than that wherethe other focal species foraged and at randomsites in continuous forest (Fig. 2A). Among ourfocal species, only Ferruginous-backed Antbirdsand Thrush-like Antpittas differed from each


Fig. 1. Proportion of sites that were riparian (water flowing or flooded) and upland (never flooded) for plotsin continuous forest, second growth or where the focal species were observed foraging.

other, with Thrush-like Antpittas foraging atsites with deeper leaf litter than Ferruginous-backed Antbirds (Fig. 2A).

The numbers of small plants in random plotsin continuous forest sites and sites in Vismia-dominated second growth overlapped with thoseof the foraging sites of all focal species (Fig. 2B).However, none of the sites where our focalspecies were observed foraging had as fewsmall plants as the random plots in Cecropia-dominated second growth. Variation in thenumber of small plants at sites where we ob-served antpittas and Chestnut-belted Gnateatersforaging was greater than that at sites where theother focal species foraged and at random sitesin the three available habitats (Fig. 2B).

The number of small trees at sites whereour focal species foraged was similar to thatat randomly selected sites in the continuousforest (Fig. 2C). There were more small treesin Cecropia-dominated second growth than inmicrohabitats used by the two antthrushes; oth-erwise, the number of small trees in Cecropia-dominated second growth was similar to that atsites used by our focal species. The number ofsmall trees in Vismia-dominated second growthalso exceeded the number of small trees at sitesused by Chestnut-belted Gnateaters, RingedAntpipits, and the two antthrushes. Sites wherethe two species of antthrushes foraged had fewersmall trees than sites used by four other focalspecies (Ferruginous-banded Antbird, RingedAntpipit, Thrush-like Antpitta, and VariegatedAntpitta).

Random sites in Vismia-dominated secondgrowth had far fewer medium trees than siteswhere all the focal species were observed foraging(Fig. 2D). For large trees, only sites whereThrush-like Antpittas were observed foraginghad fewer large trees than random sites incontinuous forest (Fig. 2E). Foraging sites ofall nine focal species had more large trees thanrandomly selected sites in either type of secondgrowth. However, the number of large vines atsites where most of the focal species forageddid not differ from that in the random sites incontinuous forest; the only exception was thatthere were fewer large vines at sites where RingedAntpipits foraged (Fig. 2F). All sites where focalspecies were observed foraging had more largevines than random sites in Vismia-dominatedsecond growth.

In general, microhabitats available in sec-ondary growth differed from those availablein continuous forest. The deeper leaf litter inboth types of second growth was a particularlystriking difference that may be directly relevantto foraging by terrestrial birds; most of ourfocal species preferred the shallower leaf litteravailable in continuous forest (Fig. 2A). Wefound a similar pattern with the number of largetrees, with most of our focal species preferringareas of continuous forest with relatively highnumbers of large trees (Fig. 2E). Other variablesexhibited more variation among focal species,and characteristics of sites used by our focalspecies sometimes differed from one or bothtypes of second-growth forest.


Fig. 2. Bayesian estimates of means (circles), standard deviations (boxes), and credible intervals (vertical lines)for (A) leaf litter depth, (B) plants ≤ 1 m tall, (C) small trees (dbh ≤ 7 cm), (D) medium trees (dbh >7–15 cm), (E) large trees (dbh > 15 cm), and (F) large vines (dbh > 0.5 cm) at sites where nine species ofterrestrial insectivores were observed foraging and at randomly selected sites in the three types of availablehabitat (continuous forest and Cecropia- and Vismia-dominated second growth). Dotted horizontal lines showthe upper and lower bounds of the standard deviations for randomly selected sites in the continuous forestsites for comparison with sites where birds were observed foraging and randomly selected sites in Vismia- andCecropia-dominated second growth.


DISCUSSION

We found that most microhabitat charac-teristics of sites where our nine focal speciesof Neotropical terrestrial insectivores foragedbroadly overlapped those of randomly selectedsites in continuous forest. However, our focalspecies foraged in microhabitats that differedfrom those in second-growth forest in severalrespects, including leaf litter depth, density ofsmall plants and trees, and density of largetrees. Our focal species are generally absent fromsecond-growth areas (Borges and Stouffer 1999)and our results are consistent with the hypoth-esis that microhabitat differences make second-growth forests unsuitable for our focal species.In particular, the thick leaf litter of Vismia- andCecropia-dominated second growth may inter-fere with normal foraging behaviors. AlthoughStouffer and Bierregaard (1995) and Borges andStouffer (1999) found that our focal species mayuse Cecropia-dominated second growth morereadily than Vismia-dominated second growth,Cecropia leaves are typically 30–40 cm across(Parolin 2002) and their presence in the leaflitter may impede foraging behavior or eventerrestrial movement. This would be particularlytrue for species that forage by actively tossing leaflitter, such as Wing-banded Antbirds. RingedAntpipits, which glean from live leaves as theywalk, may also find Cecropia-dominated secondgrowth suboptimal for foraging because plants <1 m in height were sparse in this habitat.

Our focal species may also avoid second-growth forests due to microclimate conditionsthat are correlated with vegetation structureor edaphic conditions. For example, Karr andFreemark (1983) found that understory birdsin Panama were associated with specific mi-croclimate conditions and changed their useof the forest during the year, indicating therelative importance of microclimate comparedto vegetation. In the tropics, the near-groundmicroclimate of second-growth forests is bothhotter and drier than that in continuous forests(Fetcher et al. 1985, Uhl and Kauffman 1990),and such environmental conditions may exceedthe physiological tolerances of our focal species(Stratford and Robinson 2005).

Microhabitat characteristics may also explainwhy Thrush-like Antpittas, associated with largetreefalls in continuous forest (Stouffer 2007),were able to use second-growth forests in our

study. Thrush-like Antpittas in our study pre-ferred microhabitats that had dense understoryvegetation and fewer large trees, characteristicstypical of young treefall gaps (Fetcher et al.1985). Thrush-like Antpittas are also foundin forest fragments and second growth; theirassociation with scrubbier vegetation in con-tinuous forest may allow this species to persistin fragmented landscapes, at least those thatinclude some forest and second-growth areas.

Compared to second growth, microhabitatassociations of our focal species in continuousforest were more subtle, with more overlap inthe characteristics of foraging sites and randomlyselected sites. The density of small nonwoodyplants, for instance, was more variable at sitesused by our focal species than at randomlyselected sites, but reasons for such a differenceare unclear. The densities of medium and largetrees in plots where birds foraged were similaramong species and to those of randomly selectedsites in continuous forest. In addition, the leaflitter depth at sites where our focal speciesforaged was similar to that at randomly selectedsites in continuous forest. Our focal speciesalso preferred drier sites, which were availablethroughout the continuous forest site.

The two antthrush species in our study wereassociated with sites with fewer small trees,whereas Variegated Antpittas and Ferruginous-backed Antbirds were associated with sites withmore small trees. For large vines, only sites usedby Ringed Antpipits differed from randomlyselected sites, using sites with relatively few largevines. Although the reasons for these apparentpreferences are unclear, these subtle microhab-itat associations might explain the patchinessof distributions in continuous forest. Stouffer(2007), for example, studied the same focalspecies as in our study and found that theywere patchily distributed in the 100-ha plotextensively searched in our study, with, on aver-age, two-thirds of the study plot unoccupied byparticular species. In North American deciduousforests, the distributions of terrestrial insecti-vores are closely tied to microhabitat features(Holmes and Robinson 1988). In Neotropicalforests, terrestrial insectivores and other under-story birds have been found to show preferencesfor particular ranges of soil composition (Buenoet al. 2011, Pomara et al. 2012), and topologyand forest structure (Marra and Remsen 1997),which are potentially confounded (Cintra and


Naka 2012). To better understand relationshipsbetween microhabitat characteristics and thedistribution of terrestrial insectivores, experi-mental studies involving habitat manipulationsare needed. Habitat alteration caused by firesand selective logging may, however, offer someinsight. Our focal species and other terrestrialinsectivores are known to be sensitive to theimpact of fire and low-intensity logging (Barlowet al. 2002, 2006, Barlow and Peres 2004),which may alter leaf litter depth and the densityof nonwoody plants, but have less of an impacton the canopy.

A second objective of our study was to pro-duce a smaller, more efficiently sampled set ofvegetation variables for use in future studies ofother terrestrial insectivores. From our initial26 vegetation variables, we identified six thatcaptured the variation in vegetation structure.Characterizing vegetation based on six variablesshould significantly reduce the time needed tosample each site, from the 1–2 h we required to30 min or less. We are not suggesting that thesesix variables actually determine if birds will bepresent or absent, only that we identified vege-tation characteristics associated with selection offoraging habitat by the birds. More importantcausal factors might be prey availability, foragingefficiency, or predator avoidance, which areinfluenced by vegetation structure. As long asthe correlative relationship between an easilymeasured variable (such as the density of largetrees) is consistent with a causal factor (such asprey density), measurement of vegetation struc-ture is useful for describing essential elementsof the habitat that must be maintained for thepersistence of terrestrial insectivores. Becauseour study species or their close relatives arefound throughout Neotropical rainforests fromMexico to Argentina, we hope our approachand results will be broadly applicable to theirconservation.

ACKNOWLEDGMENTS

We thank G. Rompre and M. Bugdal for helpful com-ments on the manuscript, M. Orme and M. McMarthyfor their help with analysis, and Flecha for many hours offield assistance. The BDFFP is managed and supportedby the Instituto Nacional de Pesquisas da Amazonia andthe Smithsonian Institution. This is publication 607 ofthe BDFFP Technical Series and 26 of the AmazonianOrnithology Technical Series of the INPA ZoologicalCollections Program. The manuscript was approved by

the Director of the Louisiana State University AgriculturalCenter as manuscript number 2012-241-7682.

LITERATURE CITED

ALEIXO, A. 1999. Effects of selective logging on a birdcommunity in the Brazilian Atlantic forest. Condor101: 537–548.

ANTONGIOVANNI, M., AND J. P. METZGER. 2005. Influ-ence of matrix habitats on the occurrence of insec-tivorous bird species in Amazonian forest fragments.Biological Conservation 122: 441–451.

BARLOW, J., L. A. M. MESTRE, T. A. GARDNER, AND C.A. Peres. 2007. The value of primary, secondary andplantation forests for Amazonian birds. BiologicalConservation 136: 212–231.

———, AND C. A. PERES. 2004. Avifunal responses tosingle and recurrent wildfires in Amazonian forests.Ecological Applications 14: 1358–1373.

———, ———, L. M. P. HENRIQUES, P. C. STOUFFER,AND J. M. WUNDERLE. 2006. The responses ofunderstory birds to forest fragmentation, loggingand wildfires: an Amazonian synthesis. BiologicalConservation 128: 182–192.

BARLOW, J. T., T. HAUGAASEN, AND C. A. PERES. 2002.Effect of ground fires on understory bird assemblagesin Amazonian forests. Biological Conservation 105:157–169.

BICKNELL, J., AND C. A. PERES. 2010. Vertebrate pop-ulation responses to reduced-impact logging in aneotropical forest. Forest Ecology and Management259: 2267–2275.

BIERREGAARD, R. O., Jr., AND C. GASCON. 2001. The bio-logical dynamics of forest fragments project: overviewand history of a long-term conservation project. In:Lessons from Amazonia: the ecology and conserva-tion of a fragmented forest (R. O. Bierregaard, Jr., C.Gascon, T. E. Lovejoy, and R. Mesquita, eds.), pp.5–12. Yale University Press, New Haven, CT.

BLAKE, J. G., AND B. A. LOISELLE. 2001. Bird-assemblagesin second-growth and old-growth forests, Costa Rica:perspectives from mist nets and point counts. Auk118: 304–326.

BORGES, S. H. 1995. Comunidade de aves em dois tiposde vegetacao secundria da Amazonia central. M. S.thesis, Universidade Federal do Amazonas, Manaus,Brazil.

———, AND P. C. STOUFFER. 1999. Bird communities intwo types of anthropogenic successional vegetationin central Amazonia. Condor 101: 529–536.

BUENO, A. S., R. S. A. BRUNO, T. P. PIMENTEL, T. N.M. SANAIOTTI, AND W. E. MAGNUSSON. 2011. Thewidth of riparian habitats for understory birds in anAmazonian forest. Ecological Applications 22: 722–734.

CANADAY, C. 1997. Loss of insectivorous birds along agradient of human impact in Amazonia. BiologicalConservation 77: 63–77.

CHAZDON, R. L. 2008. Beyond deforestation: restoringforests and ecosystem services on degraded lands.Science 320: 1458–1460.

CINTRA, R., AND L. N. NAKA. 2012. Spatial varia-tion in bird community composition in relation totopographic gradient and forest heterogeneity


in a central Amazonian rainforest. InternationalJournal of Ecology 2012: 435671, doi:10.1155/2012/435671.

COHN-HAFT, M., A. WHITTAKER, AND P. C. STOUFFER.1997. A new look at the “species-poor” centralAmazon: the avifauna north of Manaus, Brazil.Ornithological Monographs 48: 205–236.

dE CASTILHO, C. V., W. E. MAGNUSSON, R. N. O. DEARAUJO, R. C. C. LUIZAO, A. P. LIMA, AND N.HIGUCHI. 2006. Variation in aboveground tree livebiomass in a central Amazonian forest: effects of soiland topography. Forest Ecology and Management234: 85–96.

DEPPE, J. L., AND J. T. ROTENBERRY. 2008. Scale-dependent habitat use by fall migratory birds: vege-tation structure, floristics, and geography. EcologicalMonographs 78: 461–487.

DUNNING, J. B. 1992. CRC handbook of avian masses.CRC Press, Boca Raton, FL.

FETCHER, N., S. F. OBERBAUER, AND B. R. STRAIN.1985. Vegetation effects on microclimate in lowlandtropical forest in Costa Rica. International Journal ofBiometeorology 29: 145–155.

FOLEY, J. A., G. P. ASNER, M. H. COSTA, M. T. COE, R.DEFRIES, H. K. GIBBS, E. A. HOWARD, S. OLSON,J. PATZ, N. RAMANKUTTY, AND P. SNYDER. 2007.Amazonia revealed: forest degradation and loss ofecosystem goods and services in the Amazon Basin.Frontiers in Ecology and the Environment 5: 25–32.

GARDNER, T. A., J. BARLOW, L. W. PARRY, AND C.A. PERES. 2007. Predicting the uncertain future oftropical forest species in a data vacuum. Biotropica39: 25–30.

GASCON, C., AND R. O. BIERREGAARD. 2001. The biolog-ical dynamics of forest fragments project. In: Lessonsfrom Amazonia: the ecology and conservation of afragmented forest (R. O. Bierregaard, C. Gascon, T.E. Lovejoy, AND R. Mesquita, eds.), pp. 31–42. YaleUniversity Press, New Haven, CT.

GELMAN, A., J. B. CARLIN, H. S. STERN, AND D. B. RUBIN.2003. Bayesian data analysis. Chapman & Hall/CRCPress, Boca Raton, FL.

HAIR, J. F., Jr., W. C. BLACK, AND B. BABIN. 2010. Mul-tivariate data analysis. Prentice Hall, Upper SaddleRiver, NJ.

HOLMES, R. T., AND S. K. ROBINSON. 1981. Treespecies preferences of foraging insectivorous birds in anorthern hardwoods forest. Oecologia 48: 31–35.

———, AND ———. 1988. Spatial patterns, foragingtactics, and diets of ground-foraging birds in anorthern hardwoods forest. Wilson Bulletin 100:377–394.

JAMES, F. C. 1971. Ordinations of habitat relation-ships among breeding birds. Wilson Bulletin 83:215–236.

———, AND H. H. SHUGART, Jr. 1970. A quantitativemethod of habitat description. Audubon Field Notes24: 727–736.

KARR, J. R., AND K. E. FREEMARK. 1983. Habitat selec-tion and environmental gradients: dynamics in the“stable” tropics. Ecology 64: 1481–1494.

KATTAN, G. H. 1992. Rarity and vulnerability—the birdsof the Cordillera Central of Columbia. ConservationBiology 6: 64–70.

LAURANCE, W. F., P. M. FEARNSIDE, S. G. LAURANCE,P. DELAMONICA, T. E. LOVEJOY, J. RANKIN-DEMERONA, J. Q. CHAMBERS, AND C. GASCON.1999. Relationship between soils and Amazon forestbiomass: a landscape-scale study. Forest Ecology andManagement 118: 127–138.

LEES, A. C., AND C. A. PERES. 2010. Habitat and life his-tory determinants of antbird occurrence in variable-sized Amazonian forest fragments. Biotropica 42:614–621.

LUNN, D. J., A. THOMAS, N. BEST, AND D.SPIEGELHALTER. 2000. WinBUGS—a Bayesian mod-elling framework: concepts, structure, and ex-tensibility. Statistics and Computing 10: 325–337.

MARRA, P. P., AND J. V. J. REMSEN. 1997. Insights intothe maintenance of high species diversity in theNeotropics: habitat selection and foraging behaviorin understory birds of tropical and temperate forests.Ornithological Monographs 48: 445–484.

MASON, D. 1996. Responses of Venzuelan understorybirds to selective logging, enrichments strips, andvine cutting. Biotropica 28: 296–309.

MESQUITA, R. C. G., K. ICKES, G. GANADE, AND G. B.WILLIAMSON. 2001. Alternative successional path-ways in the Amazon Basin. Journal of Ecology 89:528–537.

NEEFF, T., R. LUCAS, J. SANTOS, E. BRONDIZIO, AND C.FREITAS. 2006. Area and age of secondary forestsin Brazilian Amazonia 1978–2002: an empiricalestimate. Ecosystems 9: 609–623.

NELSON, B. W., V. KAPOS, J. B. ADAMS, W. J. OLIVEIRA,O. P. G. BRAUN, AND I. L. D. AMARAL. 1994. Forestdisturbance by large blowdowns in the BrazilianAmazon. Ecology 75: 853–858.

NORDEN, N., R. C. G. MESQUITA, T. V. BENTOS, R. L.CHAZDON, AND G. B. WILLIAMSON. 2011. Contrast-ing community compensatory trends in alternativesuccessional pathways in central Amazonia. Oikos120: 143–151.

OLIVEIRA, A. A. D., AND S. A. MORI. 1999. A centralAmazonian terra firme forest. I. High tree speciesrichness on poor soils. Biodiversity and Conservation8: 1219–1244.

PAROLIN, P. 2002. Life history and environment ofCecropia latiloba in Amazonian floodplains. RevistaBiologıa Tropical 50: 531–545.

POMARA, L. Y., K. RUOKOLAINEN, H. TUOMISTO, ANDK. R. YOUNG. 2012. Avian composition co-varieswith floristic composition and soil nutrient concen-tration in Amazonian upland forests. Biotropica 44:545–553.

PRANCE, G. T. 1990. The floristic composition ofthe forests of central Amazonian Brazil. In: FourNeotropical rainforests (A. H. Gentry, ed.), pp. 112–140. Yale University Press, New Haven, CT.

RANKIN-DE-MERONA, J. M., G. T. PRANCE, R. W.HUTCHINGS, M. F. D. SILVA, W. A. RODRIGUES, ANDM. E. UEHLING. 1992. Preliminary results of a large-scale tree inventory of upland rain forest in the centralAmazon. Acta Amazonica 22: 493–534.

R DEVELOPMENT CORE TEAM. 2010. R: A language andenvironment for statistical computing. R Foundationfor Statistical Computing, Vienna.


RENJIFO, L. M. 1999. Composition changes in a suban-dean avifauna after long-term forest fragmentation.Conservation Biology 13: 1124–1139.

RIDGELY, R. S., AND G. TUDOR. 1994. The birds of SouthAmerica, vol. II: The suboscine passerines. Universityof Texas, Austin, TX.

ROBINSON, W. D. 1999. Long-term changes in theavifauna of Barro Colorado Island, Panama: a tropicalforest isolate. Conservation Biology 13: 85–97.

ROEDER, M., D. HOLSCHER, AND I. D. K. FERRAZ. 2010.Liana regeneration in secondary and primary forestsof central Amazonia. Plant Ecology and Diversity 3:165–174.

ROHLF, F. J., AND R. R. SOKAL. 1981. Statistical tables.W. H. Freeman, New York, NY.

SCARIOT, A. 1999. Forest fragmentation effects on palmdiversity in central Amazonia. Journal of Ecology 87:66–76.

SEKERCIOGLU, C. H., P. R. EHRLICH, G. C. DAILY, D.AYGEN, D. GOEHRING, AND R. F. SANDI. 2002. Dis-appearance of insectivorous birds from tropical forestfragments. Proceedings of the National Academy ofSciences USA 99: 263–267.

STOUFFER, P. C. 2007. Density, territory size, and long-term spatial dynamics of a guild of terrestrial insec-tivorous birds near Manaus, Brazil. Auk 124: 291–306.

———, AND R. O. BIERREGAARD, Jr. 1993. Spatial andtemporal abundance patterns of Ruddy Quail-Doves(Geotrygon montana) near Manaus, Brazil. Condor95: 896–903.

———, AND ———. 1995. Use of Amazonian forest

fragments by understory insectivorous birds. Ecology76: 2429–2445.

———, ———, C. STRONG, AND T. E. LOVEJOY. 2006.Long-term landscape change and bird abundancein Amazonian rainforest fragments. ConservationBiology 20: 1212–1223.

———, E. I. JOHNSON, R. O. BIERREGAARD, Jr., ANDT. E. LOVEJOY. 2011. Understory bird communitiesin Amazonian rainforest fragments: species turnoverthrough 25 years post-isolation in recovering land-scapes. PLoS ONE 6: e20543.

STRATFORD, J. A. 1997. The effects of forest fragmenta-tion on terrestrial insectivorous birds in central Ama-zonas, Brazil. M.S. thesis, Southeastern LouisianaUniversity, Hammond, LA.

———, AND W. D. ROBINSON. 2005. Gulliver travelsto the fragmented tropics: geographic variation inmechanisms of avian extinction. Frontiers in Ecologyand the Evironment 3: 85–92.

———, AND P. C. STOUFFER. 1999. Local extinctionsof terrestrial insectivorous birds in a fragmentedlandscape near Manaus, Brazil. Conservation Biology13: 1416–1423.

UHL, C., K. CLARK, N. DEZZEO, AND P. MAQUIRINO.1988. Vegetation dynamics in Amazonian treefallgaps. Ecology 69: 751–763.

———, AND J. B. KAUFFMAN. 1990. Deforestation, firesusceptibility, and potential tree responses to fire inthe eastern Amazon. Ecology 71: 437–449.

WRIGHT, S. J., AND H. C. MULLER-LANDAU. 2006. Thefuture of tropical forest species. Biotropica 38: 287–301.

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