What Can Mixed‐Species Flock Movement Tell Us About the Value Of

BIOTROPICA 50(4): 664–673 2018 10.1111/btp.12557

What can mixed-species ﬂock movement tell us about the value of Amazonian secondary forests? Insights from spatial behavior

Karl Mokross1,2,3,5 , Jonathan R. Potts4, Cameron L. Rutt2,3, and Philip C. Stouffer2,3 1 Departamento de Ecologia, Universidade Estadual Paulista ‘Julio de Mesquita Filho’, Av. 24-A, 1515, Bela Vista, 13506-900 Rio Claro, SP, Brasil 2 School of Renewable Natural Resources, Louisiana State University, 227 RNR building, Baton Rouge, LA 70803-6202, USA 3 Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas da Amazonia,^ Manaus 69011, Amazonas, Brazil 4 School of Mathematics and Statistics, University of Sheffield, G27c Hicks Building, Hounsfield Road, Sheffield, UK

ABSTRACT The value of secondary forest for rain forest species remains an important question for conservation in the 21st century. Here, we describe the spatial behavior of understory mixed-species flocks in a heterogeneous landscape in central Amazonia. Understory mixed- species flocks represent a diverse, highly organized component of the rich Amazonian avifauna. We recorded movements within 26 flock home ranges in primary forest, secondary forest, interfaces between forest types, and forest fragments. We describe frequency and movement orientation in relation to forest edges, movement patterns and proportion of use between secondary and primary forest, the relation between home range sizes and vegetation height, and home range configuration. Flocks visited only a small portion of forest edges, and showed a tendency for moving parallel to edges next to less-developed secondary forest. Movement patterns in secondary forests did not show significant differences compared to primary forests. Time spent in secondary forests increased in proportion to mean canopy height. Flocks were consistently present in secondary forests where vegetation height averaged over 15 m, but home ranges were nearly twice as large compared to primary forest. Home range limits tended to be aligned with disturbed vegetation, essen- tially rearranging a territorial configuration normally adjusted by topography. The spatial behavior of this important subset of the Ama- zonian avifauna shows that secondary forests are tolerated above a certain development threshold, but perceived as suboptimal habitat until canopy height closely matches primary forests.

Abstract in Portuguese is available with online material.

Key words: Amazon; animal movement; biological dynamics of forest fragments project; forest fragmentation; heterogeneous landscapes; mixed-species ﬂocks; secondary forests.

HOW VALUABLE ARE SECONDARY FORESTS AND WHAT ROLE WILL THEY example, highly mobile species with large home ranges, as seen in st PLAY IN 21 -CENTURY CONSERVATION? Recent paradigm shifts in a considerable number of forest bird species (Terborgh et al. conservation biology have prompted an increase in the perceived 1990, Stouffer 2007, Johnson et al. 2011), may move between value of secondary forests (Chazdon et al. 2009, Marris 2009, adjacent habitats. Thus, despite being detected in secondary for- Didham 2011). Nonetheless, it is challenging to objectively quan- ests, some species still depend on primary forest (Jirinec et al. tify their contribution to species conservation. Understanding 2011). how species interact with disturbed or regenerating environments It is estimated that 70% of today’s forests are within 1 km requires detailed behavioral information, a remarkable challenge of forests edges (Haddad et al. 2015) and secondary forests are in species-rich ecosystems. A general framework for determining usually embedded within heterogeneous landscapes (Neeff et al. the conservation value of secondary forests derives from species 2006). Much insight may be gained from understanding how indi- counts and the proportions of species unique to primary forests viduals perceive and deal with these altered landscape features. (Barlow et al. 2010). These assessments usually implement sta- Habitat use patterns emerge from decision-making processes at tionary-sampling inventories (Barlow et al. 2007, Dent & Wright fine temporospatial scales (Jones 2001, Moorcroft & Barnett 2009, Gardner et al. 2009), and have provided important 2008, Potts et al. 2014a), and behavioral data in landscape ecology advancements to our understanding of altered habitats. Yet, these has been proposed as a promising way to refine predictive mod- methodologies provide no information on habitat use, establish- els (Lima & Zollner 1996, Grimm et al. 2006, Moorcroft et al. ment of stable home ranges or territorial configuration. For 2006, Carter et al. 2015). Birds compose a significant portion of the highly mobile Received 23 August 2017; revision accepted 10 March 2018. species in tropical forests, and understory insectivores are known 5Corresponding author; e-mail: [email protected] to be particularly sensitive to habitat changes (Stouffer & 664 ª 2018 The Association for Tropical Biology and Conservation Mixed-species Flocks and Secondary Forests 665

Bierregaard 1995). Among this vulnerable guild, mixed-species north of the city of Manaus, Brazil. It is a structurally heteroge- flocks may provide a representative study case. Mixed-species neous patchwork of continuous primary forest, forest fragments flocking behavior is a worldwide occurrence. It exists within an of different sizes, and adjoining secondary forests of varying ages ecological margin of advantages provided by foraging enhance- and structure (Mesquita et al. 2001) (Fig. 1). For practical report- ment and predator avoidance (Sullivan 1984, Dolby & Grubb ing, we define well-developed secondary forest as having a 1999, Goodale & Kotagama 2005, Martinez & Zenil 2012), and canopy cover with mean height >15 m and less-developed sec- penalties due to competition, kleptoparasitism, and higher ondary growth as a thin canopy cover ≤15 m, typically dominated demands in movement rate (Munn 1986, Darrah & Smith 2013). by trees of the genus Vismia (Borges & Stouffer 1999), with lit- Understory flocks in Amazonian terra firme forests are recog- tle-developed understory. These thresholds have been determined nized as a system led by the cinereous antshrike, Thamnomanes cae- from field observations at the study site. Details on the history sius (or its sister species T. schystogynus in parts of Bolivia and of this landscape can be found in (Bierregaard et al. 2001). Peru). There is a core of about eight species with overlapping territories, represented by one territorial reproductive pair per flock DATA COLLECTION.—We collected data between June 2009 and (Munn & Terborgh 1979). Outside this core, about 20 species August 2011. Mixed-species flock territories were located in five join these flocks frequently, and a much higher number of species habitat configuration types: primary forest (interior and edge); 100- have been recorded joining these aggregations sporadically (Pow- ha fragments (interior and edge); 10-ha fragments; secondary for- ell 1985, Jullien & Thiollay 1998). Up to 65 species may be est, and primary–secondary forest mix, which are areas consisting detected in a single flock over the course of a day (Martınez et al. of strips of primary forest not wide enough to fully accommodate 2013). Flocking species are known to be heavily forest-dependent, a flock home range (Table 1 and Fig. 1). Flock activity is conspicu- are reluctant to cross-roads (Develey & Stouffer 2001) and disap- ous, enabling them to be followed on foot (Mokross et al. 2014). pear in selectively logged forests and small fragments (Thiollay The observer (KM) maintained a distance of 15–20 m from the 1997, Barlow et al. 2006). Some core species have been detected core of activities. As flocks moved, the observer’s positions were in secondary forest (Borges & Stouffer 1999), but it is not known recorded at 30-sec intervals with a handheld GPS unit (Garmin if they participate in aggregations or form stable territories. Terri- Vista HCX), but for these analyses, we used data at 2-min intervals tory area usually averages 8 ha which may remain quite stable to reduce noise on turning angle values. over decades in pristine areas (Jullien & Thiollay 1998, Martınez et al. 2013). Core species gather in the same location every day at TRAJECTORY ANALYSIS.—We quantified duration and distance of dawn and actively forage throughout their territory, eventually forays into secondary forest in each habitat configuration type. returning to the vicinity of the gathering point, where individuals Due to significant effects of forest edges on water vapor deficit, roost within about 50 m from each other (Potts et al. 2014a). temperature, and foliage density within approximately 20 m from Approaches to spatial behavior are mainly based on utiliza- the border (Kapos 1989, Laurance 2002), we defined a 40-m- tion distributions generated from animal location records (Sea- wide zone which included 20 m on each side of the forest border man & Powell 1996) and are useful for a depiction of spatial and is henceforth called the edge buffer. To test if flocks align their activity within home ranges and their boundaries. For example, movement steps to forest edges, we gathered the absolute angles some forest-dependent species avoid proximity to forest edges, of all relocations inside edge buffers and compared them to for- limiting home ranges to forest interior (Hansbauer et al. 2010). est edge angles through a Rayleigh test of uniformity (V0 test) in Yet, in the absence of edge avoidance, it is still possible that the CircStats R package (Batschelet 1981, Lund & Agostinelli more refined spatial behaviors, such as path direction, are 2001). affected. Trajectory patterns may reflect a species’ decision-mak- Trajectory partition and classification were performed with ing process and how it perceives certain landscape features the modpartltraj function in the AdehabitatLT library (Calenge (Giuggioli & Bartumeus 2010). et al. 2008). We defined three movement behaviors from parame- In this study, we assess the spatial behavior of mixed-species ters based on field observations (Table S1): (1) area-restricted flocks in a heterogeneous landscape in central Amazonia asking behavior (ARB), that is, when flocks foraged at speeds of about the following: (1) What types of vegetation are avoided by flocks? 3 m/min with tight turning angles (i.e., >90o); (2) normal behavior, We measure trajectory orientation in relation to forest borders, that is, when flocks foraged at about 9 m/min, noticeably dislo- and we use a Bayesian partitioning of Markov models to classify cating forward, but turning with constant frequency; and (3) fast trajectories in primary forest, forest edges, and secondary forest. behavior, that is, when flock speed was about 17 m/min with And (2), how do flocks apportion their activity in primary and similar turning patterns to normal behavior. We only used trajecto- secondary forest when both are available? We also examine how ries with more than 50 relocations and analyzed the proportions home range shape and size are related to vegetation height. of these movement modes in the three main landscape elements: primary forest (PF), secondary forest (SF), and edge buffers METHODS (ED). To probe flock behavior in more detail, we created a finer classification within these landscape elements: primary continuous STUDY SITE.—The study was conducted at the Biological Dynam- forest (CF), primary–secondary forest mix (MIX), 100-ha frag- ics of Forest Fragments Project (BDFFP), located about 80 km ments (100 ha) and 10-ha fragments (10 ha). Edges were 666 Mokross et al.

FIGURE 1. (A) Map of the BDFFP. White boxes represent areas where flocks were sampled. (B) LIDAR coverage of one of these areas (Dimona ranch) and examples of home ranges of flocks in different landscape elements. From left to right: 10-ha fragment (yellow), secondary forest (violet), primary-secondary forest mix (white) and 100-ha fragment. Flocks are generally absent in areas of scrubby vegetation (light gray), such as the buffers around fragments. The flock with a red asterisk was considered unstable as it was not detected in subsequent sampling periods. Darker colors represent areas of taller vegetation based on Lidar data.

subdivided into soft edges (S), where forest edges transition to derived from kernels, and we used intervals ranging from 99% well-developed secondary forests, usually a gradient within (entire home range area) to 10% (areas of highest location densi- 5–20 m; and hard edges (H), where primary forest meets less- ties) for these analyses (Fig. 2). developed secondary forest, usually within 5 m or less. Secondary To quantify the proportion of time spent in second growth, forest was subdivided into well-developed secondary forest (Wd) we counted the number of positions in primary and secondary and less-developed secondary forest (Ld) (Table S2). We obtained forest. To quantify the percentage of area in secondary forest, we the proportion of movement modes and tested the differences in used the 99% isopleth. To test if there was a relationship between each landscape feature using multinomial regression through the secondary forest use and vegetation height, we used a linear mlogit package in R. model (lm) in R software (R Development Core Team 2016) (Fig. 2). HOME RANGES NEXT TO SECONDARY FORESTS.—To map the propor- To measure mean vegetation height, we used a Light Detec- tions of home ranges that were in secondary forest, which parts tion and Ranging (Lidar) canopy height model (CHM) (Specifica- were used more frequently, and the total area, we recorded flock tions in SM), and generated the zonal statistics for the vegetation positions and created quadratic kernels via Geospatial Modeling located inside each isopleth (Table S3). Environment (GME) software (Beyer 2012) (kernel parameters in To test if vegetation height influences the shapes of home SM). The standard descriptors of home ranges are isopleths range kernels (i.e., if there is a correlation between vegetation Mixed-species Flocks and Secondary Forests 667

TABLE 1. Understory mixed-species flocks sampled in the study. Habitat types are as follows: 100-ha/edge: flocks located in 100-ha fragments with contact to edge; 100-ha/interior: flocks located in 100-ha fragments located at the center of the fragment, surrounded by neighboring flocks and having with no contact with forest edge; 10-ha: flocks located in 10-ha fragments, their home ranges are surrounded by forest edges; prim./sec.: flocks located in areas with a patches of primary and secondary forest; primary edge: flocks located in areas of primary forest that interface with secondary forest; primary interior: flocks in primary forest with no contact to forest edge; secondary forest: flocks in which the entire home range occupies secondary forest. Total hours sampled, and total hours sampled in the dry season.

Total Area Flock Habitat type Total Hours Hours (dry)

Dimona Cap II* Second growth 23 23 FIGURE 2. Depiction of a flock home range (FL_IB) adjacent to secondary Cap_N Second growth 20 20 forest. Home range is represented by isopleths ranging from 10% (areas of Central 100-ha/interior 101 61 highest use density) to 99% (edges of home range). Black dots are locations Dim_10 ha 10-ha 121 81 taken at 30-second intervals. The section of home range occupying secondary Ig_cmp_flk Prim./sec. 83 43 forest is shaded in dark gray. Red line shows the edge between primary and Lake_flk 100-ha/border 20 20 secondary forest. Height of individual trees appears in green, with darker South_Central 100-ha/interior 20 20 green representing taller trees. Notice that flock home range cores (>50%) are Southwest 100-ha/border 20 20 located in primary forest. W400 100-ha/border 39 39 Colosso Col_10 ha 10-ha 95 55 Col_cabfrioI Primary border 20 20 a > 0 that significantly improves the fit of the model to the data. Col_Cap1 ha Second growth 86 46 We used a maximum likelihood approach, seeking to find the Florestal Fl_a Prim. /sec. 21 21 x |a alpha that minimizes the sum of ln[f( n )] over a set of indepen- Fl_I_b Primary border 20 20 fi x x ... x dent xes n. This sum is the log-likelihood function l( 1, , N Fl_II Primary border 74 34 |a x ... x fi ) where 1, , N is the set of independent xes being used Fl_III Primary border 21 21 for the test. For this analysis, we used the Lidar set that encom- ~ Gaviao Gav_10_ha Primary interior 20 20 passes the Dimona flocks (Table 1), which was the best-sampled ~ Gaviao_I Primary interior 22 22 area. Because each flock gathers at the same point at the start of ~ Gaviao_II Primary interior 20 20 each day, each day’s path of motion within the territory is inde- Km37 Km37_III Primary interior 20 20 pendent of the previous days’. This daily resetting allows us to Km37_V Primary interior 17 17 fl † assume that a recorded ock position one day is independent Porto Alegre PA_10 ha 10-ha 23 23 x † from a position recorded on another day, so we let each n be a PA1 100-ha/border 12 12 fl † randomly selected position from a single ock on a single day. PA2 100-ha/border 7 7 † To avoid bias from the random selection, we considered all possi- PA3 100-ha/border 10 10 x ... x † ble sets of such positions 1, , N and took the average of the PA4 100-ha/interior 5 5 x ... x |a various values of l( 1, , N ). We denoted this average by L Total 941 700 (x1,..., xN|a). *Unstable flock - see text. Additionally, we also tested if home range area was corre- † Flocks in Cecropia secondary forest without Lidar coverage for which we lated with mean vegetation height by using the same measuring could analyze vegetation height. approach, but using entire home ranges for flocks located entirely in primary forest or secondary forest. height and areas where flocks concentrate activities), we averaged RESULTS canopy height values in 10 9 10 m squares due to the high small-scale variance and constructed a model of space use. The A total of 26 flocks were recorded, compiling 941 h of obser- probability of using a particular square x is modelled to be pro- vation in six different landscape compositions (min. = 0.05 h, portional to f(x|a) = exp[aC(x)], where C(x) is the canopy height max. = 10.4 h, mn = 3.9 h, se = 2.6 h) (Table 1, Table S7). and a is a model parameter. The null model is a = 0, meaning Three flocks were recorded in three 10-ha fragments. Nine that any square is as equally likely to be used as any other. We flocks in two 100-ha fragments, of which six were in contact tested this against the alternative hypothesis that there is some with an edge. Two flocks in primary–secondary forest mix and 668 Mokross et al.

development stage, while flocks in 100-ha fragments showed higher activity and spent more time in better-developed secondary forests. Flocks in primary–secondary forest mix showed a much higher activity and exhibited large maximum foray distances in secondary forest. Lastly, primary forest flocks next to well-developed secondary forests spent a high percentage of time in such forays, but did not cover distances as great as in primary–secondary forest mix. To assess the movement patterns inside landscape features, 121 different trajectories were analyzed (Fig. 4). The multinomial model was statistically significant (Likelihood ratio test: chi- squared test 2138.7, P < 0.001); but magnitude range was small, mostly between À0.5 and 1, with the exception of fast movements in 10-ha forests and along hard edges (Fig. 5, Table S6). Fast movements increased slightly in young secondary forests compared to older second growth, but their overall proportions were not consistently higher than what is predicted for primary forest and edges.

HOME RANGE ANALYSES.—All flocks located near edges entered FIGURE 3. Trajectory angles in relation to forest edges for a 10-ha fragment secondary forest, and time spent there was correlated with the fl ock (Dimona). North and south edges are highlighted in blue, while east mean vegetation height in secondary forest (R2 = 0.519, and west facing edges are highlighted in red. The rose diagrams indicate the F1,8 = 8.64, P = 0.0187) (Figs. 6A, and S6A). Despite higher use distribution of directions for each edge set, highlighted in the same color in well-developed secondary forests, flock home range cores code. remained in primary forest (Table 2 and Fig. 2). The only exception was recorded next to the best-developed area of secondary three flocks entirely within secondary forest. Finally, nine flocks forest, where the home range core for one flock was located on were entirely located in primary forest, of which four had con- the forest edge (Table 2, Fig. S5). Despite this, the area used in tact to forest edge. No flocks were found in 1-ha fragments secondary forest was not correlated with mean vegetation height 2 (Table 1). Each 10-ha fragment held one flock home range, (R = 0.221, F1,8 = 2.274, P = 0.17). while 100-ha fragments held about 10 (Figs. 1, and S3). Flocks There were also flocks inhabiting secondary forest, but the in primary–secondary forest mix centered their home ranges in one found in the least-developed area of secondary forest was primary forest and extended their margins into secondary for- not consistently present throughout the sampling period. It was est (Fig. S4). found in June 2010 led by one female Thamnomanes caesius.The same individual alongside a male was seen in October 2010, but TRAJECTORY ANALYSES.—Flocks tended to avoid, or quickly cross neither was found in May 2011 after several visits to their former areas with clear understory, such as temporary ponds, even gathering area. after water subsided (Fig. S1) and usually circled around large Total home range area showed a negative correlation to 2 forest gaps (Figs. S2A,C, S3A, S4, and S5). On rare occasions, mean vegetation height (R = 0.31, F1,8 = 7.638, P = 0.013) they quickly crossed open areas of up to 25 m. Overall, flocks (Figs. 6B, and S6B). The smallest home range was 6.7 ha in an generally did not enter vegetation below 5 m in height. Four area of primary forest with an average canopy height of 23.4 m, of ten flocks showed significant Rayleigh test values for tests while the largest home range was 17.1 ha, in an area of sec- on perpendicularity along forest edges, all of them being hard ondary forest with an average canopy height of 13.1 m. forest edges (Fig. 3) (Table S4). In such cases, flocks foraged Flock kernel shapes responded to the layout of anthro- along forest edges for lengths up to 30 m, with individuals pogenic features (Fig. S7). The response of home range shapes moving up to 10 m into secondary forest. Forest edges were and layout to vegetation, the value of a that maximizes L not used uniformly. Some sections were frequently used, while (x1,..., xN|a), is a = 0.065. Using the likelihood ratio test, the others were not visited at all (Figs. S2, S3, and S5). Flocks P-value associated with rejecting the null hypothesis in favor of adjacent to well-developed second growth did not move paral- the hypothesis that canopy height is a predictor of space use lel to forest edges, but concentrated their foraging at edge buf- is P = 0.0000033. Regarding edge effects on home range fers. shapes, this value of alpha means that if an area of primary Flock activity in secondary forests consisted mainly of for- forest of 30 m height is next to a 10 m tall secondary forest, ays. Average times and distances in secondary forest are listed in flocks near the boundary between the two will be 3.7 times the online Supporting Information (Table S5). Flocks in 10-ha more likely to be found in the primary forest (i.e.,: exp[0.065* fragments showed little activity in secondary forests regardless of (30–10)]). Mixed-species Flocks and Secondary Forests 669

A B

FIGURE 4. (A) Example of a trajectory that was partitioned using the partmodltraj function. The blue triangle represents the beginning of the trajectory and the red square the end. The ﬂock enters secondary forest, eventually returning to primary forest while changing its movement patterns. Vegetation is shown by a Lidar-derived canopy height model, where darker shades represent taller vegetation. Movement models are color-coded: Area-restricted behavior (ARB) in blue, normal movement modes in yellow, fast movements are in red. This frame is a subset of the trajectories in the following panel. (B) Primary–secondary forest mix (Ig. Cmp. Flk). (C) Primary–secondary forest mix (FLIA). (D) 10 ha-fragment (Dimona).

DISCUSSION studies in the same area (Develey & Stouffer 2001); however, the fact that few flocks visited edges and only small sections were Fine-scale spatial behavior has provided an unprecedented view frequently used suggests that it is not optimal habitat and may of how secondary forests are perceived by an important set of only offer resources under specific conditions. It has been shown the understory avifauna in central Amazonia. Despite being that flocks are more likely to move into lower terrain such as found using secondary forests, there is strong evidence that it is stream valleys (Potts et al. 2014a) and edge segments that over- a suboptimal habitat for flocking species until forest structure lapped with these topographical features were frequently visited approaches primary forests. (Figs. S2, and S3). The behavior of moving short distances Trajectories revealed that flocks avoided short vegetation. between primary and secondary forest along forest edges may be Occasionally, flocks remained stationary or skirted edges before due to arthropod spillover from primary forest (Lucey & Hill quickly crossing open areas. This indicates that less-developed 2011). While movement parallel to edges tended to disappear secondary forests may be perceived as unfavorable, either due to near well-developed secondary forest, flock activity was still con- fewer resources, higher depredation risk, or a combination of the centrated within primary forest limits (Fig. S5). This suggests that two. Areas that are occasionally flooded, even when dry, were while trajectories normalize with secondary forest development, also bypassed, possibly due to the sparser understory. In fact, overall space use is still affected. these temporary lagoons, a common feature in terra firme forests, Flocks near edges showed reluctance to crossover to sec- have a noticeable effect on flock space use and should be taken ondary forests. Some species such as Thamnomanes caesius, Xiphor- into account when considering their spatial behavior. hynchus pardalotus, and Xenops minutus were more prone to enter The fact that flocking species could move and forage so less-developed secondary forest than other species, such as Myr- close to forest edges indicates some tolerance to edge habitat. motherula longipennis, M. menetriesii, and Thamnomanes ardesiacus, This finding was not surprising given results from previous which tended to avoid less-developed secondary forests. 670 Mokross et al.

During this process, individuals usually maintained some degree Element PF ED SF of movement, traveling along the forest edge. These processes partially explain the parallel, rectilinear movements near hard Type CF 10ha 100ha MIX Ld Wd S H PF average ED average SF average edges and suggest some form of collective decision-making for habitat use even when T. caesius, which typically leads flock fl ABR movements, tries to lead the ock into secondary forest. Flock 41 12 34 47 51 22 37 37 33 37 37 composition influence on space use, however, remains to be properly quantified. fl Fast We expected ocks to move faster and in more rectilinear 16 45 11 7 9 46 16 9 20 23 12 fashion in secondary forests with more sinuous trajectories and slower movements in primary forests. Differences in movement Normal mode proportions were not stark, but some movement patterns 44 43 55 46 40 42 47 54 47 41 51 appeared to be associated with particular landscape elements. For example, fast and rectilinear bouts were recorded in secondary FIGURE 5. Prediction from the multinomial model on the proportions (rep- forests and inside 10-ha fragments. The mechanisms determining resented as percentages) of movement modes inside each landscape element. different movement behaviors, however, may not be effectively PF: Primary forest, ED: Edge (20 m at each side of forest-secondary forest explained by forest height variables alone, and may be influenced interface), SF: Secondary forest. Under PF, the types are CF: Continuous for- by finer variables such as understory vegetation structure, flock est, 10 ha: 10 ha-forest fragment, 100 ha: 100 ha-forest fragment, MIX: pri- composition, and the presence of potential predators. It is also mary–secondary forest mix. ED types are S: soft edges and H: hard edges. important to note that the number of flocks in certain habitat SF types are Wd: Well-developed secondary forest and Ld: Less-developed types, such as well-developed secondary forests, soft forest edges secondary forest. Blue color represent partitions categorized as Area-Restricted is relatively small. Therefore, more information should be gath- Behavior, red Colors indicate Fast movement behavior and Yellow is Normal ered to increase certainty about drawn inferences. movement behavior. The bars with black outlines represent the averaged pro- Flock use of secondary forest responded strongly to devel- portions of movement modes in each landscape element. opment stage. It is important to note that flocks still anchored their territory cores in primary forest until vegetation reached an average height of 23 m, which is close to the mean height of pri- Occasionally, T. caesius entered secondary forests, while individu- mary forest (~25 m). While we acknowledge that mean vegetation als from other species would remain inside primary forest near height may not be the proximal cause determining space use, this the edge. If the majority of the aggregation remained in primary metric seems to efficiently summarize vegetation structure and forest, it would return. If the majority of the flock entered sec- other properties relevant to birds (Hinsley et al. 2002, Hyde et al. ondary forest, some species would still remain behind and 2006, Clawges et al. 2008). A possible explanation lies in prey would rejoin the flock only when it returned to primary forest. density, which may respond to vegetation density due to

50 20 A B R² = 0,51 Cap1ha FL_IA 40 FLIII FL_II

F Gav_II S

n Cap_N Col10ha i FL_IB SouthCentral t FL_IA

n Central e 30 W400 p s FL_II Km37_III e Igcmpflk Igcmpflk FL_III m

i Lake t 10

f Gav10 Gav_I o

Col10ha e Area (ha) Dim10ha g SW a 20 t

n FL_IB

e CaboFrio c r e P 5 10 W400 SW Dim10ha R² = 0,31 Lake

0 0 51015202530 10 15 20 25 30 Mean vegetation height in SF Mean vegetation height (m)

FIGURE 6. (A) Flocks adjacent to secondary forest: relation between time spent in secondary forest and mean vegetation height of second growth. (B) Relation- ship between total home range area and mean canopy height. Mixed-species Flocks and Secondary Forests 671

TABLE 2. Percentage of time mixed-species ﬂocks spent in secondary forest. First column shows kernel isopleths from complete home ranges (99%) to areas of most intense use, or home range core areas (10%). Cells are color-coded: higher percentages of time in secondary forest are darker. Flock IDs ordered from lowest to highest percentage of total home range area in second growth.

microclimatic conditions buffering and available substrate (Kapos that certain flocks may eventually be pushed into suboptimal 1989, Laurance & Gomez 2005, Ewers & Banks-Leite 2013, habitat under certain habitat configurations. This is reinforced by Potts et al. 2014a). Considering its importance to a significant the observation of depauperate and unstable flocks in poorly number species, invertebrate density and its relation to structural developed secondary forests. The mechanisms underlying the conditions in the landscape remains a poorly studied and neces- intermittent occupation of these areas remain to be investigated, sary line of inquiry. and may be related to a lack of resources, predation, or both. Our results suggest that during forest regeneration, flocks Lastly, even large and nearly equilateral fragments (100 ha) are incorporate secondary forest beyond previous vegetation borders, bound to have up to 70% of flocks in contact with an edge, as hypothesized by Powell et al. (2016). Our results partially cor- which may have impacts on demographic processes and territorial roborate this model, but with one important difference: While dynamics. time spent in secondary forests increases with its development, In summary, Amazonian mixed-species flocks tolerate sec- there is no clear relation between vegetation height and area of ondary forests, but they seem to comprise suboptimal habitat secondary forest that is used. Area seems to be largely influenced resulting in a rearrangement of territories in the landscape. Spatial by terrain and territorial interactions. It is likely that pressure behavior only becomes roughly equivalent to primary forest after from neighbors inside large fragments pushes flocks near borders mean vegetation height reaches 23 meters or more with a well- to secondary forests, while flocks eventually establishing in sec- preserved understory. It is important to highlight that composi- ondary forest contain territorial boundary expansion. Our previ- tion data from the same study area show flocks to be less cohe- ous work modeling flock spatial behavior suggests that these sive even in well-developed secondary forests, implying that flock interactions are an important aspect on flock space use (Potts composition and participation may take much longer to recover et al. 2014b). than spatial behavior (Mokross et al. 2014). Adding further evidence to the scarcity of resources in secondary forests, flocks located in secondary forests occupy much ACKNOWLEDGMENTS larger areas, effectively reducing densities by half when compared to pristine areas. The inverse relationship between territory size We are thankful for the logistical support from the BDFFP. and resource, as well as habitat structure and resource density, Field support was provided by J. Lopes, J. de Deus F. Faria, C. has been explored and described in this system as well as with L. da Silva, A. M. dos Reis, A. Nunes, P. Hendrigo, E. L. Ret- other species (Huxley 1934, Litvaitis et al. 1986, Jullien & Thiollay roz, B. Souza, A. C. Vilela, and M. Campos. M. Lewis, M. C. 1998), but the possibility of other factors influencing territory Cortes,^ M. Cohn Haft, J. D. Wolfe, E. I. Johnson, L. L. Powell size, such as predation risk and intruder pressure (Adams 2001, and two anonymous reviewers provided valuable comments. Willems & Hill 2009), should also be considered. Funding for the research was provided by US National Science Flock home range layout was strongly affected by the layout Foundation grant LTREB-0545491, the National Institute of of disturbed areas. Flock home range layout in primary forests Food and Agriculture, U.S. Department of Agriculture, McIntire seems to be mainly set by topography, but in altered areas, vege- Stennis project number 94327, and by the AOU 2010 research tation takes precedence. This is an important consideration, given award. This article represents publication no. 735 in the BDFFP 672 Mokross et al.

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