Bird Communities in Two Types of Anthropogenic Successional Vegetation in Central Amazonia’

The Condor 101:529-536 0 The Cooper Ornithological Society 1999

BIRD COMMUNITIES IN TWO TYPES OF ANTHROPOGENIC SUCCESSIONAL VEGETATION IN CENTRAL AMAZONIA’

SBRCIO HENRIQUE BORGES~ Institute National de Pesquisas da AmazBnia, C.P. 478, Manaus, Amazonas, Brazil

PHILIP C. STOUFFER Department of Biological Sciences, Southeastern Louisiana University, Hammond, LA 70402-0736

Abstract. When primary forest in central Amazonia is cut and abandoned,the plant successionis dominated by Cecropia spp., whereas when it is cut and burned for pastures, the regrowth vegetation is dominated by Vismia spp. The bird communities of these two regrowth forest types were sampled at six sites (9-13 years old) using mist-nets and observations. Bird speciesrichness was similar between the two forest types. Cecropia regrowth, however, was richer for strictly forest bird species than was Vismia regrowth. Mixed-flock species and ant-following birds were significantly more abundantin the Cecropiu second growth, whereas nonforest insectivores and omnivores were more common in Vismia regrowth. The type of regrowth was found to influence bird speciescomposition in the study sites. These results suggestthat the type of human disturbancehas an important role in determining the bird communitiesthat occupy early successionalareas in central Amazonia. Kev words: Amazon, ant-followinn birds, Cecropia, human disturbance, secondary forest birds: tropical birds, Vismia: -

INTRODUCTION ary growth? Is the similarity in bird assemblages In central Amazonia, bird community studies affected by the type of regrowth? Are there dif- have been concentrated in primary forest and ferences in species richness and abundance of forest fragments, mostly in conjunction with the birds among sites? Do bird guilds differ in spe- Biological Dynamics of Forest Fragments Pro- cies composition and abundance in the two types ject (BDFFP), a large-scale experimental project of secondary forest? on the effects of fragmentation on forest communities including birds, mammals, and plants METHODS (Bierregaard and Lovejoy 1989, Bierregaard et We selected three sites in Cecropia-dominated al. 1992, Stouffer and Bierregaard 1995a, second growth (hereafter CSG) and three sites 1995b). During the process of establishing the in Vismia-dominated second growth (hereafter BDFFP study sites on large private farms, ex- VSG) in study areas of the BDFFP (see Ferreira tensive areas of primary forest were cleared, and and Laurance 1997 for map of the study sites). in some cases burned. The process of clearing The sites selected have undergone different instigated two major types of regrowth: a Cec- management practices and differ in age and flo- ropia-dominated community that normally re- ristic composition (Table 1). Vegetation in Co- generates in the absence of fire, and a Vismia- loss0 and Florestal sites was periodically cut and dominated community that regenerates where burned until 1985. Because of this intense man- fire was frequently used to manage these grass- agement and periodic use by cattle, these sites lands. contained large areas of pasture devoid of sec- This study compared the bird community of ondary vegetation. At Dimona, secondary veg- these two types of successional forest. We de- etation was not periodically controlled by fire. scribe general patterns in species richness and Some small areas of primary forest, mostly as- abundance considering the following questions: sociated with streams, are present in the Cec- What bird speciesoccur in each type of second- ropiu site at Dimona. All net lines were sepa- rated by at least 1 km, except in Colosso and ’ ’ Received 1 December 1997. Accepted 25 March Florestal where the nets lines were separatedby 1999. 300 m. 2 Current address: Fundacao Vitoria Amazonica, casa07, Quadra Q, Morada do Sol, Manaus, AM, Bra- The rainfall in central Amazonia is seasonal, zil, 69080-510, e-mail: [email protected] with a dry season from July to October and a

w91 530 SkRGIO HENRIQUE BORGES AND PHILIP C. STOUFFER

TABLE 1. Featuresof study sites of secondary growth types in Amazonia, Brazil. Fire indicates that primary vegetationis burned.Management indicates whether the areais cut, burned,and used by cattle.

Secondary Agea Canopy height (m) Sites growth types (in years) (mean + SD) Fire Management

Dimona Vismia 9 7.6 -e 1.6 yes moderateb c010ss0 Vismia 13 5.3 k 3.2 yes intensec Florestal Vismia 13 5.4 _f 3.0 yes intense Dimona Cecropia 12 17.4 ? 3.4 no no Port0Alegre Cecropia 10 17.0 + 3.7 no no Cidade Powell Cecropia 10 15.5 5 3.4 no no

aYears since the last management acuvities. b Occasional burning. c Annual burning.

wet season from November to June (Stouffer DATA ANALYSIS and Bierregaard 1993). The field work described Birds observed flying over the study sites (vul- here extended from late March (mid-wet season) tures, swallows, and swifts) and nocturnal spe- to mid October (late dry season) in 1993. cies were not considered in the comparison between the two types of regrowth. We classified MIST-NET CAPTURES AND OBSERVATIONS birds as forest and nonforest speciesas proposed At each site, we used 30 mist-nets (36 mm by Cohn-Haft et al. (1997). We used a G-test mesh, 12 X 2 m) arranged in two parallel net- with William’s correction for sample size, for lines, with 15 nets in each line. In each case the testing associations between numbers of cap- net lines were located at two distancesfrom pri- tures, species richness, and vegetation types. mary forest-50 and 250 m. Two days of field Only species or groups of species with more than 10 individuals captured were considered in work were expended in each sampling period at the comparisons between types of secondary each site totaling 72 days of field work. The nets growth. The distance of net-lines from primary were open from 6:00 to 14:00, and the study forest had no effect on total number of species sites were visited at monthly intervals. The total (captured and observed) (Wilcoxon test, Z = sampling effort was 17,280 net-hours equally -0.4, P > 0.5), speciescaptured (Z = 0.1, P > distributed between types of second growth. 0.5), and individuals captured (Z = - 1.7, P > Birds were given individually numbered alumi- 0.05). Thus, unless otherwise indicated, we num bands. Compared with the bird list includ- pooled data from the two net-lines in each study ing captures and observations in each study site, site. In multiple comparisons we adjusted the nets sampled 55% (range 45-61.5%) and 47% significance level by Scheffe’s correction factor, (range 44-52.5%) of the bird species recorded dividing the significance level assumed (P < in VSG and CSG, respectively. Relative abun- 0.05) by the number of comparisons. dance measurements were based only on net Because the number of captures differed be- samples. tween sites, the comparison of understory bird In addition to the mist-net samples, we used speciesrichness was standardizedby rarefaction binoculars and a tape recorder to note all species curves. This method generatesan expected num- heard or observed in the sites. Tape playback ber of species for a standard sample size (Lud- was important for identification of some species. wig and Reynolds 1988). Following recommen- In addition to our previous experience at the dations by James and Rathbun (1981), we stan- sites, tape recording and local lists of birds by dardized the sample size by the site with the other workers at BDFFP study sites (Stotz and lowest number of captures. Bierregaard 1989, Cohn-Haft et al. 1997) facil- We performed cluster analysis with Sorensen itated identifications. Sampling effort dedicated distance measure and group averaging as to general observations was similar in each weighting procedures to represent the relation- study site and occurred principally between ships of bird species assemblages in the sites 06:OO and 15:O0. (McCune and Mefford 1995). Each net-line was BIRDS IN SECONDARY GROWTH IN AMAZONIA 531

160

._z 8 120 5? 2 100

1 80

0 10 20 30 40 50 60 70 80

160 , Cumulative days of observations

* 140 .z 8 120 ,a

.g 60 % 3 40 g u 20

0 100 200 300 400 500 600 700 800 900 1000

Cumulative number of captures

FIGURE 1. Curvesof species-samplingeffort includingobserved (A) and captured(B) birds. considered as a sampling unit for the cluster an- thor). The cumulative curves of observed and alyses. Values are reported as means + SD. captured species (Fig. 1) indicate that sampling was not complete. However, based on previous RESULTS studies in the area (Bierregaard and Lovejoy SPECIESRICHNESS AND ABUNDANCE 1989), most of the relatively common speciesin Combining captures and observations, we re- understorywere captured. corded 177 bird species on the study sites The total number of species at the Cecropia (check-list available by request from first au- sites was 141, whereas 123 species were en- 532 StiRGIO HENRIQUE BORGES AND PHILIP C. STOUFFER

+ Vismia sites + Cecropia sites

0 100 200 300 400 500 600 Number of captures FIGURE 2. Rarefractioncurves for the secondarygrowth bird species.The standardsample size is 380 captures with 63 speciesfrom Cecropia sites and 64 for Vismia sites. countered on Vismia sites. There was no signif- analyzed these guilds in terms of species rich- icant difference in species richness of captured ness and abundance between secondary forest birds between VSG (45.5 ? 9.0 species) and types (Table 3). The number of speciesin some CSG (44.6 + 7.0). When observed specieswere bird guilds differed between secondary forest included in the total speciesrichness calculation, types. Ground insectivores, especially Formica- CSG sites are slightly richer than VSG sites (94 riidae, were more species-rich in CSG (eight vs. + 5.5 vs. 83 +- 5 species). Rarefaction analysis four), but the sample sizes were too small for also showed that the understory of the two types statistical analysis. Some species in this group, of second growth presents little difference in such as Thrush-like Antpitta (Myrmothera cam- species richness (Fig. 2). However, CSG is sig- panisona), Ferruginious-backed Antbird (Myr- nificantly richer in forest bird speciesthan VSG meciza ferruginea), and Spot-winged Antbird (137 vs. 106 species;G, = 4.2, P < 0.05). Some (Schistocichla leucostigma), were not recorded forest birds were recorded in only one type of in VSG. In contrast, two other species in this second growth with 54 speciesrestricted to CSG guild, Black-throated Antbird (Myrmeciza atro- and 22 speciesrestricted to VSG. thorax) and Ringed Antpipit (Corythopis tor- We captured 928 individuals (excluding re- quata), were recorded only in VSG. The nucle- captures and same day captures). Ten species ar-speciesof the mixed-flocks (Cinereous Antsh- contribute with 53.5% of all captures, with the rike Thamnomanes caesius) and the three spe- White-plumed Antbird dominating captures in cies of specialized ant-followers (Willis and both types of second growth (Table 2; scientific Oniky 1978) were found in the two types of sec- names in Table 2 unless otherwise noted). Sig- ondary growth. Army ants also were observed nificantly more individuals were captured in in both types of regrowth. Mixed flocks were CSG than in VSG (546 vs. 382) (G, = 29.10, P rarely seen in the study sites. The specieslisted < 0.01). as understory insectivores represent a heteroge- GUILDS neous group which precludes any generaliza- We grouped birds into guilds based on food hab- tions. However, the number of species in the its, foraging substrate,habitat, and behavior, and Bucconidade family merits attention. In VSG BIRDS IN SECONDARY GROWTH IN AMAZONIA 533

TABLE 2. Number of captures of the 10 most commonly TABLE 3. Number of species (observed + captured) and captured species in each type of secondarygrowth. The captures in the two types of secondary growth grouped by rankingposition for eachhabitat is listedin parentheses. guilds. The numbers with asterisks (*) are significantly different (G-test, P < 0.006, adjusted by Scheffi’s correction

Species CSG VSG factor for multiple comparisons). White-plumed Antbird Number (Pithys albifrons) 82 (1) 48 (1) of species Number of captures Black-headed Antbird Guildsa VSG CSG VSG CSG (Percnostolarujifrons) 44 (2) 12 (6) Rufous-throatedAntbird Frugivores (Gymnopithysrujigula) 40 (3) 11(7) ground 5 5 2 4 White-crowned Manakin understory 13 10 75 62 (Pipra pipru) 30 (4) 37 (2) canopy 11 20 3 1 Warbling Antbird Insectivores (Hypocnemiscantator) 30 (5) 7 (10) McConnell’s Flycatcher ground 4 8 8 18 (Mionectesmacconnelli) 19 (6) 17 (4) understory 26 31 129* 201* Mouse-Colored Antshrike canopy 13 12 2 12 (Thamnophilusmurinus) 18 (7) 9 (8) open areas 7 2 10 0 White-flanked Antwren barkh 5 8 7 12 (Myrmotherula axillaris) 18 (8) 8 (9) mixed-flocks” 9 11 29* 65* Buff-throated Foliage-gleaner ant-followers 3 3 65* 128* (Automolusochrolaemus) 16 (9) 24 (3) Omnivores Long-tailed Hermit ground 2 3 4 1 13 (10) (Phaethomis superciliosus) 14 (5) understory 1 1 2 4 canopy 7 13 1 1 open areas 7 1 6 0 only Black Nunbird (Monasa atru), a common Nectarivores/insectivores 5 8 24 44 forest edge species, was observed. In contrast, Predators 2 3 2 1 five species of this family were recorded in Granivores 3 1 3 1 CSG. Open area insectivores/omnivores and gra- Piscivores 0 1 0 1 nivorous species were almost exclusively found a Guild designawn follows Karr et al. (1990). Stouffer and Bierregard (1995b), Powell (1989). and personal observations. in VSG (17 vs. 4 species, respectively, G, = 8.5, h Does not mclude speaes that follow mixed flocks and army ants. P < 0.01). c Included understory and canopy flocks. Some guilds present differences in relative abundance between the two types of secondary abundance between the two types of secondary growth (Table 3). Insectivores show the most regrowth, all being more abundant in CSG. significant differences in relative abundance be- These species included five understory insecti- tween the secondary growth types. In the ant- vores of Thamnophilidae family (Black-headed following guild, only White-chinned Woodcree- Antbird, Rufous-throated Antbird, White- per (Dendrocincla merula) was equally abun- plumed Antbird, Warbling Antbird, and White- dant in the two types of secondary growth. The flanked Antwren), a woodcreeper (Wedge-billed Cinereous Antshrike, the nuclear-species of the Woodcreeper Glyphorhynchus spirurus), a forest mixed flocks, also was captured in similar fre- wren (Wing-banded Wren Microcerculus bam- quency among secondary growth types. Ground bla), and a hummingbird (Fork-tailed Wood- insectivores that walk rather than fly were rarely nymph Thalurania furcatu). The antbird species captured. Nets do not provide a good indication include two obligate ant-followers (White- of the relative abundance of these species. Nev- plumed Antbird and the Rufous-throated Ant- ertheless, field observations indicate that these bird) and two solitary species commonly found species are more common in CSG. For example, along forest edges: Warbling Antbird and Black- Thrush-like Antpitta is a ground insectivore headed Antbird (Willis 1982, Stouffer and Bier- commonly heard in CSG, but was never detected regaard 1995b). in VSG sites. Although there was a significant difference in RELATIVE ABUNDANCE OF SPECIES: VSG VS. number of captures of White-flanked Antwren CSG between second growth types, the abundance of Of 33 species for which there were sufficient this species was probably underestimated in captures, 8 showed significant differences in VSG sites. This species was frequently observed 534 SERGIO HENRIQUE BORGES AND PHILIP C. STOUFFER

DISTANCE hEASURE ble 1). Moreover, a floristic study conducted in ,044 ,332 620 907 1.195 the same area showed that CSG was richer in

Calossoi.VSG) plant speciesthan VSG (Williamson et al. 1998),

Floreslal(VSG) which may also promote higher bird species

Colosso(VSG) richness (Rotenberry 1985). Therefore, plant species diversity and vegetation structure can Dimma (VSG) partially explain the differences in bird abun- Dimm (VSG) dance and species diversity between the two Polto Aleg~e (CSG) types of secondary forests. Cii Pow.% (CSG) Apparently, the origin of vegetation succes- Porta A&E (CSG) sion and consequently the habitat structurein the Wade Powell (CSG) study sites are influenced by the severity of land Flonsral (VSG) management. More severe management, includ- Dimom (CSC) ing periodically cutting and burning, results in a

Dimma (CSG) more depauperate bird fauna. Alternatively, the secondary forests with lower grazing pressure FIGURE 3. Dendrogram of cluster analysis of study sites. Groups of net-lines (sampling units) were are colonized by several typical forest bird spe- groupedby their similarity in bird speciescomposition. cies. The smaller the distance between pairs of sampling The age of secondary forestsalso may explain units, the more similar they are in speciescomposition. the differences in bird abundance and composition in the study areas. Studies in secondary forest bird communities in Costa Rica showed that in familial groups of five individuals foraging in bird species richness and abundance change the canopy of VSG where they cannot be sam- through time with forest succession (Loiselle pled by nets. With the exception of White- and Blake 1994). The age of our sites varied flanked Antwren, all species cited above also slightly (Table l), but this can only partially ex- were detected by song and observations in the plain the changes in bird community at the sec- lowest stratum of the secondary growth, where ondary forests sites studied. they should have been well sampled by nets. Some patterns of differential use of secondary forest by bird guilds were expected based on AVIFAUNAL SIMILARITY BETWEEN SITES previous reports on the effects of fragmentation Three major groups emerged from the cluster and the type of secondary growth around the analysis and with the exception of two sites (one fragments on the bird community (Stouffer and net-line in Port0 Alegre and one in Florestal), all Bierregaard 1995a, 1995b, Bierregaard and net-lines were grouped by the type of secondary Stouffer 1997). Ant-following birds are very growth (Fig. 3). The first group included two sensitive to habitat disturbance (Canaday 1995). net-lines in very disturbed VSG sites. The re- Species of this group are the first to disappear maining VSG and CSG sites were separatedby from forest fragments (Biemegaard and Lovejoy two major groups. This clustering pattern indi- 1989). On Barro Colorado Island, the ant-fol- cates that the structure of bird communities is lower birds declined after the island was isolat- affected by the type of second growth, despite ed, and some species became locally extinct, sites showing no great differences in species possibly due to their inability to cross the water richness. Moreover, the sites in VSG were more barrier separating the island from the mainland heterogeneousin speciescomposition than CSG, (Willis 1974). a result probably associated with the manage- The mixed-species flocks disintegrate after ment of the sites. forest fragmentation (Bierregaard and Lovejoy 1989). Although the flocks as a unit disintegrate, DISCUSSION individual speciesreact in different ways to hab- SPECIES RICHNESS AND COMPOSITION itat disturbance (Bierregaard and Lovejoy 1989, Higher forest bird species richness in CSG was Stouffer and Bierregaard 1995b, this study). The expected based on the greater vegetation com- nuclear-species of flocks (Cinereous Antshrike) plexity of this secondary forest. The canopy in is relatively common in both types of secondary CSG is on average twice as high as in VSG (Ta- forests studied. Conversely, Myrmotherula spp. BIRDS IN SECONDARY GROWTH IN AMAZONIA 535

(excepted M. axilluris), common in primary for- sity (Saunders and Hobbs 1991). In designing ests mist-net samples (Stouffer and Bierregaard corridors, it is important to consider many eco- 1995b, Cohn-Haft et al. 1997), are extremely logical factors like dominant tree speciesand the rare in the secondary growth. landscape of the corridor (Lindenmayer and Nix Why do speciesthat composed this guild dif- 1993). Our study shows that primary-forest bird fer in abundance among types of secondary for- speciescan use the secondary forest, principally est? We did not investigate the proximate causes that dominated by Cecropia. We captured sev- of avoidance or preference for a particular veg- eral birds originally banded in forest fragments etation type, but some hypotheses can be dis- indicating that some species can move through cussed. All species with consistent differences or utilize secondary forest habitats. in abundance between secondary forests are in- Furthermore, the type of secondary forest af- sectivores.Hence we expect differences in avail- fected the use of forest fragments by birds in ability of insects present in the two types of for- our study sites. Several species that had disap- est. peared in fragments, returned years later, prin- Another criterion of bird habitat selection are cipally when the surrounding grassland was microclimate conditions. Activity patterns of un- dominated by Cecropia regrowth (Stouffer and derstory birds are influenced by moisture gra- Bierregaard 1995b). In contrast, fragments sur- dients with some speciesmore active in dry and rounded by Vismia remained depauperate in others in moist sites (Karr and Freemark 1983). terms of bird species richness (Stouffer and Although no microclimate data were collected in Bierregaard 1995b). Hence, we recommended the study sites, the VSG appears to be hotter, the use of Cecropia species as one of the dom- dryer, and brighter than CSG. Birds with higher inant tree species in the vegetation of wildlife capture rates in CSG are speciestypically found corridors in the Amazon. The Cecropia species in dark and moist understory in forest interior. provide some desired key characteristicsfor re- Physiological tolerance of these speciesmay ex- storing landscape, including sufficient shade to plain their association with CSG, a habitat that eliminate grasses and weeds, as well as small appearsmore similar in microclimate to the pri- and medium-sized fruits to attract a wide range mary forest than is VSG. of frugivores and potentially seed-dispersingan- imals (Lamb et al. 1997). Cecropia spp. are CONSERVATION IMPLICATIONS promising species in management programs de- Large blocks of primary forest in the tropics are signed for landscape restoration. cut and burned for agriculture. Due to a variety of circumstancesincluding soil quality, climate, ACKNOWLEDGMENTS and changes in government policy, these areas We are gratefulto Bill Magnusson, Gislene Ganade, are, in most cases, abandoned and occupied by and Claude Gascon for suggestionsabout the experimental design, and Joninhas, Seu Lulu, Flexa, Piaui, successionalvegetation. The history of our study and Cachorro for indispensable help with the field sites follows a similar model of occupation, use, work. Mario Cohn-Haft and Rita Mesquita helped us and abandonment. This study suggeststhat bird with valuable discussionsabout this manuscript. We communities in secondary forest are affected in- are in debt to The Biological Dynamics of Forest Frag- ments Project for providing the infrastructureof this directly by how previous land use history influ- study.This study was supportedby CAPES and CNPq ences vegetation succession. The more severe grants. We thank Gary Childers, SoutheasternLouisi- management practices,especially periodic use of ana University, for providing all infrastructureneces- fire, apparently have more negative impact on sary for data analyses. Two anonymous reviewers, the bird community, particularly for forest bird Walter D. Koenig, Renato Cintra, Edwin 0. Willis, Roberto Cavalcanti, and Richard Bierregaardreviewed species. Less severe land use is preferable over the first version of this manuscript and contributed devastation of extensive areas of forest for un- with important and constructivecomments. Thanks to sustainable agricultural projects. Research in al- Claude Gascon, Bill and Susan Laurance, and Cecilia ternative productive use of secondary forest can Hanne for helping correct the manuscript.This article is No. 230 of the Biological Dynamics of ForestsFrag- diminish the pressure on undisturbed primary ments Project technical series. forest. One conservation strategy currently discussed LITERATURE CITED is the use of corridors connecting forest frag- BIERREGAARD,R. 0.. AND T E. LOVEJOY. 1989. Effects ments for the maintenance of biological diver- of fragmentation on amazonian understory bird 536 StiRGIO HENRIQUE BORGES AND PHILIP C. STOUFFER

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