Comparative Foraging Behavior Between Solitary and Flocking Insectivores in a Neotropical Forest: Does Vulnerability Matter?

Home , Amazonian antshrike, Black nunbird, Collared gnatwren, Cymbilaimus, Fasciated antshrike, Flocking (behavior)

ORNITOLOGIA NEOTROPICAL 14: 47–65, 2003 © The Neotropical Ornithological Society

COMPARATIVE FORAGING BEHAVIOR BETWEEN SOLITARY AND FLOCKING INSECTIVORES IN A NEOTROPICAL FOREST: DOES VULNERABILITY MATTER?

Jean-Marc Thiollay

Laboratoire d’Ecologie, E.N.S., 46 rue d’Ulm, 75230 Paris cedex 05, France. E-mail: [email protected]

Resumen. – Comportamiento comparativo de alimentación entre insectívoros solitarios y en bandadas en una selva Neotropical: es una cuestión de vulnerabilidad? – Las bandadas mixtas de especies de aves insectívoras son una característica común en las selvas tropicales. Dos hipótesis han sido propuestas para explicar este comportamiento social: mejorar la obtención del alimento y la defensa antipredatoria. Este trabajo señala el comportamiento alimenticio y la selección del hábitat de especies en bandadas vs especies solitarias, para evaluar si su vulnerabilidad respectiva a los predadores podría estar relacionada con su facilidad a formar bandadas. Cuando las aves se están alimentando, su mayor vulnerabilidad es su visibilidad, su grado de vigilancia y la protección u ocultamiento provisto por la vegetación que las rodea. Seleccioné los 37 insectívoros más comunes y representativos de una selva lluviosa Neotropical y los dividí en tres grupos iguales según su grado de formar bandadas. Durante 944 ataques > 1 min, medí la detectabilidad y vigilancia de aves individuales. Comparadas con las aves que se alimentan solitarias o participan ocasionalmente en bandadas, las especies obligadas a bandadas fueron más detectables, menos vigilantes y más fácil de ser susceptibles a ataques por predadores. Ellas usaron técnicas más activas de forrajeo que fueron menos compatibles con la vigilancia sostenida y más conspicuas. Ellas también usaron sustratos menos protegidos y de un nivel riesgoso medio. De tales sitios de forrajeo, ninguno apareció suficientemente abierto para permitir un radio seguro de detección y escape, ni bastante denso que provea inaccesibilidad, ocultamiento o refugio. Los resultados sugieren que la aparente vulnerabilidad a la predación de al menos miembros obligados de bandadas puede ser determinante, más que una mera consecuencia o su comportamiento de bandada. Las bandadas pueden dar la protección antipredador necesaria para ellas para usar sin peligro su riesgoso comportamiento de forrajeo y hábitat. En resumen, los forrajeadores solitarios pueden tener sitios de forrajeo y comportamiento seguro, comparados con las especies obligadas a bandadas, las cuales deben forrajear en bandadas para retener el síndrome de comportamiento de riesgo, mientras los eventuales podrían tener comportamientos intermedios o adaptables y de esta manera variables, pero no beneficios esenciales para unirse en bandadas. Abstract. – Mixed-species flocks of insectivorous birds are a common feature of tropical forests. Two hypotheses have been proposed to explain this social behavior: feeding enhancement and antipredator defense. This paper points out the comparative foraging behavior and habitat selection of flocking vs solitary species, to assess whether their respective vulnerability to predators could be related to their flocking propensity. When birds are foraging, their major components of vulnerability are their conspicuousness, their degree of vigilance and the protection or concealment provided by the surrounding vegetation. I selected the 37 most common and representative insectivores of a primary Neotropical rain forest understory and divided them into three equal groups according to their flocking propensity. During 944 contin- uous > 1-min feeding bouts, I measured the detectability and vigilance of individual birds. Compared to solitary foragers or occasional flock participants, obligate flock members were more detectable, less vigi-

47 THIOLLAY lant, and more likely to be susceptible to attacks by stalking predators. They used more active foraging techniques that were both less compatible with sustained vigilance and made them more conspicuous. They also used less protective substrates and the more risky mid-level of open understory. Such foraging sites looked neither open enough to allow a safe radius of detection and escape, nor dense enough to provide inaccessibility, concealment, or refuge. The results suggested that the apparent vulnerability to predation of at least obligate flock members may be a determinant, more than a mere consequence, of their flocking behavior. Flocking may afford the antipredator protection necessary for them to use safely enough their risky foraging behaviors and habitats. In short, solitary foragers would have relatively safe foraging sites and behaviors, compared to obligate flock species which should forage in flocks to retain their risky behavioral syndrome, while facultative attendants may have intermediate or adaptable behaviors and thus derive variable, but not essential benefits from joining flocks. Accepted 22 July 2002. Key words: Neotropics, rain forest, foraging, mixed-species flocking, predation risk, vigilance, vulnerability.

INTRODUCTION uals, learning foraging techniques, substrates or patch quality and minimizing duplication Feeding in flocks is a widespread behavior effects (Krebs 1973, Krebs & Davies 1987, among animals, especially birds (Barnard Ekman & Hake 1988, Sasvari 1992, Master et 1983, Morse 1985, Faaborg 1988). How for- al. 1993, Giraldeau et al. 1994). aging birds may increase their fitness by join- There are many types of flocking behav- ing flocks in spite of increased costs due to iors that may have different origins, determi- higher detectability and competition has nants and functions. Most studies have stirred intense debates (Pulliam 1973, Powell considered monospecific groups in open hab- 1974, Bertram 1978, Hutto 1987, Terborgh itats (e.g., Caraco 1979, Popp 1988, Cresswell 1990). 1994) or winter flocks of tits in temperate for- Two major hypotheses have been pro- ests (e.g., Morse 1970, 1977, Ekman 1979, posed. The first one claims that flocking may 1987, Smith & Buskirk 1988, Rollfinke & enhance predator avoidance from an earlier Yahner 1991, Suhonen 1993). In tropical for- detection and warning of predators through ests, beside monospecific social groups, mul- cumulative vigilance of several individuals. tispecific associations of foraging birds range Additional benefits may be derived from a from large canopy flocks to opportunistic higher potential for mobbing predators, from aggregations of frugivores and specialized a confusion and dilution effect during attacks army ant followers at ground level (Moynihan or from a patchy distribution reducing 1962, Buskirk 1976, Willis & Oniki 1978, Thi- encounter rates with predators (Willis 1973, ollay & Jullien 1998). I shall concentrate here Curio 1976, Morse 1977, Elgar 1989). The on the permanent mixed species flocks of second hypothesis postulates that birds in insectivores in mid-understory levels of tropi- flocks may derive feeding benefits from cal forests (Buskirk et al. 1972, Wiley 1980, reduced scanning rates and more time spent Munn 1985, Munn & Terborgh 1979, Graves searching for food (Lazarus 1972, Powell & Gotelli 1993, Stotz 1993, Poulsen 1996, Jul- 1985, Popp 1988), from cryptic prey dis- lien & Thiollay 1998). Previous authors, per- placed by neighbors, if not kleptoparasitism sonal experience and a local study (Thiollay & (Brosset 1969, Erard 1987), and from facilita- Jullien 1998) have all shown that understory tion of food finding through information Neotropical forest insectivorous species can transfer, such as following successful individ- be divided into species that 1) either rarely if

48 VULNERABILITY IN MIXED-SPECIES FLOCKS ever join mixed flocks, or 2) occasionally and Keys & Dugatkin 1990, Lima & Dill 1990, even consistently do so, but still also forage Suhonen 1993, Cimprich & Grubb 1994, on their own, or 3) are obigate members of Farnshaw 1995). If flocking was primarily an such flocks, almost never foraging alone. Is antipredator defence, it should increase in there any common trait whose variation cases of higher conspicuousness, lower vigi- among the three groups would explain this lance, and/or lack of concealment. As a behavioral difference? The feeding behavior working hypothesis, I tested the influence of of obligate flock members will be compared habitat selection and behavioral characteris- with that of species only occasionally joining tics of different species on their flocking pro- such flocks and with solitary foragers. The pensity in a tropical rain forest where aim of this study is not to test directly the foraging in mixed flocks was prominent. antipredator value of flocking behavior but to emphasize the behavioral characteristics of METHODS species foraging in flocks compared to those of solitary species using similar resources in Study area the same habitat. The working hypothesis All data were obtained in the Nouragues Nat- was that species or individuals whose forag- ural Reserve, 100 km south of Cayenne, ing behavior and/or habitat structure made French Guiana (04°05N-52°41W). The area them most vulnerable to predators should was uniformly covered with primary lowland forage in flocks, whereas species least vulner- (50–200 m a.s.l.) tropical rain forest. The able or individuals in low-risk situations could study area was described in Thiollay (1989), avoid the costs of flocking and adopt solitary the bird community in Thiollay (1994), the foraging habits. different categories of feeding associations in The risk of predation, or vulnerability to Thiollay & Jullien (1998), the social and for- predators, may arise from three interrelated aging behaviors of mixed flocks in Jullien & factors: 1) Conspicuousness of foraging Thiollay (1998) and the diurnal raptor com- behavior: in the gloomy rainforest under- munity, including the most significant preda- story, movements make birds often more tors of adult birds at least by day, in Thiollay conspicuous than do size or color pattern; 2) (1989). An undulating relief and numerous Degree of vigilance: interspecific differences small streams (mean annual rainfall: 3500 may come from the relative ability to be vigi- mm) diversified the forest types. The domi- lant when actually foraging; if scanning and nant 40–50 m high mature forest with an searching for prey are incompatible, a bird open understory, on well drained slopes and becomes vulnerable when it forages and vigi- plateaus, often gave way to naturally dis- lance periods are at the expense of foraging turbed stands with lower, more irregular and time; 3) Safety of habitat structure: a bird is denser undergrowth (Table 1). Tree fall gaps presumably less vulnerable either in a dense and palm swamps were not sampled because vegetation that provides concealment and they were rarely used by local flocks. refuge, or in an open forest because of an increased detection distance. Such relation- Species selection ships between foraging behavior, exposure of I selected, among the local forest bird com- foraging sites, habitat structure or degree of munity, as many as possible common, small vigilance and flocking tendency have already to medium-sized, primary forest understory been stressed mostly in temperate passerines insectivores (37 species), representative of the (Barnard & Stephens 1983, Ekman 1987, main foraging techniques, substrates and

49 THIOLLAY

TABLE 1. Main habitat and foraging behavior of solitary foragers (overall occurrence in mixed flocks in the study area = 0–11%, Thiollay & Jullien 1998).

a b c d Group F0 Sample Habitat Foraging Speed White-tailed Trogon (Trogon viridis) 86(14) A 3 Strike-foliage Still 1 (0.1) Blue-crowned Motmot (Momotus momota) 113(14) A 2 Strike-litter Still 1 (0.3) Yellow-billed Jacamar (Galbula albirostris) 139(14) A 2 Sally-air Still 1 (0.2) White-chested Puffbird (Malacoptila fusca) 63 (10) A 2 Sally-air Still 1 (< 0.1) Mouse-colored Antshrike (Thamnophilus murinus) 57 (21) B 3 Glean-foliage Active 1 (6.7) Warbling Antbird (Hypocnemis cantator) 91 (53) B 1 Glean-foliage Active 2 (7.0) Spot-winged Antbird (Percnostola leucostigma) 18 (11) B 1 Glean-litter Active 1 (3.3) Spot-backed Antbird (Hylophylax naevia) 33 (19) B 1 Glean-litter Active 1 (1.9) Scale-backed Antbird (Hylophylax poecilonota) 68 (20) A 1 Strike-litter Still 2 (0.7) Golden-crowned Spadebill (Platyrinchus coronatus) 25 (10) A 2 Strike-foliage Still 2 (0.3) Ruddy-tailed Flycatcher (Terenotriccus erythrurus) 32 (15) B 3 Sally-air Still 2 (0.7) Collared Gnatwren (Microbates collaris) 20 (12) B 1 Glean-litter Active 3 (14.4) aContinuous foraging periods measured: cumulative length in min (number of bouts involved). bForest type and openness: A = high mature forest with open understory and closed canopy; B = moderately disturbed and denser stands + small gaps; C = low dense stands with vine tangles and broken canopy. Height of foraging birds: 1 = < 2 m; 2 = 2–10 m; 3 = (4)10–25 m cMain prey capture techniques (see text). Substrates: Foliage = leaves and branchlets; tangles = vine tangles and dense branches or lianas; epiphytes = from mosses to bromeliads and/or clumps of dead leaves; litter includes ground cover and low vegetation; air: flying insects; bark = on branches or trunks and any dead wood from twigs to logs. dStill: 1 = slow (= 1 move/min); 2 = quick (2–6 moves/min); Active: 1 = slow (4–10 moves/min); 2 = moderate speed (12–18 moves/min); 3 = fast (= 20 moves/min). In parentheses = hops/flights ratio. See methods for additional definitions. microhabitat uses, and for which I obtained The taxa sampled included the most regular >10 suitable foraging records. These species insectivores seen at mid-level of this primary were divided into 3 sets according to their forest understory. All terrestrial species, flocking propensity, i.e., the proportion of all woodpeckers, and canopy birds were foraging individuals of each species observed excluded. Other candidates were too rare or in mixed flocks in a previous large sample of elusive. Only in 2 species, a woodcreeper and randomly encountered birds (data in Thiollay an antwren, was the sample suitable to com-

& Jullien 1998): group F0= 12 species rarely if pare birds foraging alone and in flocks. ever joining flocks; group F1 = 13 occasional, if not regular participants in mixed flocks, but Sampling technique also often feeding alone; group F2 = 12 obli- I searched for birds by walking slowly gate understory flock members foraging through the forest over an area of several almost only in association with mixed flocks hundred hectares during 2 years. Different (see Tables 1–3). A flock was defined as a last- areas were surveyed on successive days, ing aggregation of > 5 individuals of > 2 spe- between sunrise and sunset during the main cies, and only the permanent mixed-species breeding seasons (February–April and Sep- flocks of insectivores in the forest understory tember–November 1993–1994, Tostain et al. were considered (Jullien & Thiollay 1998). 1992). Because searches were at random, over

50 VULNERABILITY IN MIXED-SPECIES FLOCKS

TABLE 2. Foraging behavior of occasional flocks participants (occurrence in mixed flocks: 22–55%).

a b c d Group F1 Sample Habitat Foraging Speed Black Nunbird (Monasa atra) 68 (13) A 3 Strike-foliage Still 1 (0.1) Ruddy Foliage-gleaner (Automolus rubiginosus) 21 (10) C 1 Search-litter Active 2 (18.8) Wedge-billed Woodcreeper (Glyphorhynchus spirurus) 42 (30) A 3 Search-bark Active 3 ( 14.5) Fasciated Antshrike (Cymbilaimus lineatus ) 33 (18) C 2 Glean-tangles Active 1 (15.7) Amazonian Antshrike (Thamnophilus amazonicus) 30 (14) C 2 Glean-tangles Active 2 (11.0) Rufous-bellied Antwren (Myrmotherula guttata) 49 (30) A 1 Glean-litter Active 2 (5.7) Dot-winged Antwren (Microrhopias quixensis) 19 (12) C 2 Glean-tangles Active 3 (13.3) Gray Antbird (Cercomacra cinerascens) 31 (17) B 3 Glean-tangles Active 2 (16.9) McConnell's Flycatcher (Mionectes macconnelli) 35 (15) A 1 Sally-air Still 2 (0.7) Olivaceus Flatbill (Rhynchocyclus olivaceus) 17 (10) A 3 Strike-foliage Still 2 (0.3) Coraya Wren (Thryothorus coraya) 23 (15) C 2 Glean-tangles Active 3 (33.6) Long-billed Gnatwren (Ramphocaenus melanurus) 22 (11) B 3 Glean-tangles Active 3 (43.7) Fulvous-crested Tanager (Tachyphonus surinamus) 25 (13) B 3 Glean-foliage Active 1 (2.1) a–dsee Table 1. the whole area, crossing all forest types and (> 200 m apart) and on different days. This recording any bird encountered, I assumed minimized the risk to record twice the same that existing habitat types, flock sizes and individual, and I assumed that samples were behaviors were adequately represented in the reasonably independent. overall sample of foraging bouts. If conspicu- Eventually, a subset of 944 foraging peri- ous birds were more readily detected, then ods (1921 min), all fitting the above restrictive this applied to all three categories. conditions, was used to analyze the behavior Only actively foraging birds, that did not of 37 species. Sample periods lasted 200– appeared to be aware of, or distracted from 1800 s for large sit-and-wait predators and foraging by my presence, were selected and 60–240 s for other taxa. Habitat variables, then used as focal individuals (Altmann 1974) position of the bird, flock size, visibility and followed as long as possible. Records of for- foraging behavior were recorded once at the aging events, using 10 x 42 binoculars, tape beginning of each individual sampling period, recorder, and digital stopwatch, began = 5 s while movements, scans, prey attacks, sub- after the individual was detected. Observa- strate used and prey size were counted over tions lasted = 60 s, and ceased when the bird all the observation period. Only birds in adult departed, or became not fully visible, or plumage were recorded, pooling males and stopped foraging (e.g., resting, preening, call- females. All durations were in seconds. ing, interacted with other birds or manipu- lated a prey item for > 10 s). Scanning and = Habitat and foraging behavior 10 s handling prey were included in foraging For each observation period, I recorded 10 periods. No bird was recorded around abun- variables including habitat type, height of dant food sources (e.g., army ants, insect bird, capture technique and substrate, dura- swarms), or in large canopy gaps, or in tion (s), number and length of moves, num- unusual situations, or when moving excep- ber of attacks, prey size and handling time. tionally fast or slowly. Every contact of a Three forest types were defined (see Table 1, same species was both in widely spaced areas and Thiollay 1994), as well as three levels of

51 THIOLLAY

TABLE 3. Foraging behavior of obligate flock members (occurrence in mixed flocks: 92-100%).

a b c d Group F2 Sample Habitat Foraging Speed Rufous-rumped Foliage-gleaner (Philydor erythro- 98 (71) A 3 Search-epiphytes Active 2 (12.7) cercus) Olive-backed Foliage-gleaner (Automolus infusca- 42 (27) A 3 Search-epiphytes Active 2 (11.3) tus) Plain Xenops (Xenops minutus) 28 (18) A 3 Search-twigs Active 3 (9.1) Chestnut-rumped Woodcreeper (Xiphorhynchus 46 (33) A 3 Search-bark Active 3 (23.7) pardalotus) Curve-billed Scythebill (Campyloramphus procur- 22 (13) A 3 Search-bark Active 3 (14.5) voides) Dusky-throated Antshrike (Thamnomanes ardesia- 68 (43) A 3 Strike-foliage Still 2 (0.8) cus) Cinereous Antshrike (Thamnomanes caesius) 119(74) A 3 Strike-foliage Still 2 (0.6) Brown-bellied Antshrike (Myrmotherula gutturalis) 66 (45) A 3 Search-dead leaves Active 2 (7.9) White-flanked Antwren (Myrmotherula axillaris) 53 (41) A 3 Glean-foliage Active 3 (9.9) Long-winged Antwren (Myrmotherula longipennis) 101(79) A 3 Glean-foliage Active 3 (8.9) Gray Antwren (Myrmotherula menetriesii) 85 (59) A 3 Glean-foliage Active 3 (12.3) Sulphur-rumped Flycatcher (Myiobius barbatus) 33 (20) A 3 Glean-foliage Active 2 (3.3) a–dsee Table 1. foraging height which separated species for- active-hunting were divided into low and high aging always low (< 2 m), at mid-level (2–10 speed classes according to the number of m) or usually higher (4–25 m). Two basic for- moves per min (Table 1). Prey attacks aging behaviors were defined according to included both unsuccessful attempts and cap- prey capture maneuvers and substrates (Table tures, divided into short (glean, snatch, peck) 1): still-hunting, i.e., sit-and-wait from a perch and long attacks (strike, sally, probe, chase, (strike, sally), and active-hunting, i.e., continu- hover), using an average duration of 1 and 2 s ous foraging with rapid movements and short respectively, including quick small insect swal- stops (glean, search). Gleaning implied mov- lowing. Only prey handling lasting 1–10 s ing constantly in vegetation and picking up were timed. Longer periods were excluded arthropods on foliage, bark or litter; it also from measured foraging bouts. Prey sizes included hanging, snatching, sweeping foli- were classified as small and large, i.e., shorter age or chasing disturbed insects. Searching and longer than bill length, a simple measure- included closely inspecting, probing, pecking ment better correlated with the bird’s han- or tearing wood, bark, epiphytes or dead dling ability than the absolute prey length. leaves. Striking implied perch to substrate pounce or hover-glean; it also included klep- Conspicuousness and vigilance toparasitism. Sallying involved aerial hawking Six summary variables, likely to affect the insects from a perch. Foraging moves, involv- conspicuousness and the vigilance of a foraging perch changes, were divided into hops (< ing bird, were computed for each individual 1 m), short flights (1–5 m) and long flights (> sample. 5 m). Their mean duration was estimated to be 0.3, 0.6 and 1.5 s respectively. Still- and Visibility. An index of visibility (VIS) assessed

52 VULNERABILITY IN MIXED-SPECIES FLOCKS the focal bird’s detectability for a potential handling, any substrate inspection or manipu- predator according to habitat density, vegeta- lation (e.g., probing, tearing, pecking) and tion structure and substrate type. Along six periods during which the bill was consistently perpendicular axes (four in a plane parallel to close to, or directed toward a substrate that the ground, one above and one below the was also blocking view in that direction. Such bird), I scored the average distance between restrictive criteria probably underestimated the bird and the first obstacle (vegetation actual searching time. In those species where item) likely to obscure it (0 = < 1 m; 1 = 1–5 searching was easier to identify and measure m; 2 = > 5 m). All six scores summed, the than scanning, it was used as the basis for the index ranged from 0 (fully hidden birds) to 12 proportion of time spent, together with (completely exposed individuals). This was an MOVE, and SCAN was then estimated as the indicator of concealment or accessibility: a complement to 100%. branch or foliage may hide a bird or impair the possibility for a predator to attack it from Percentage of time spent scanning or watching, sup- this side, while a trunk or the ground prevent posedly for predators (SCAN). For birds foraging detection and access on one side. So the bird actively, it was sometimes possible to count becomes vulnerable only from open sides, or the number of actual scans, when the bird it may be visible (e.g., through vine tangles), stopped, the bill pointed upward or away but difficult to reach, while still able to see from the nearest substrate. Such stops were approaching predators. divided into short (fixed average = 0.6 s) and long scans (> 1 s, then accurately timed). Velocity (VEL) or foraging speed. Was the num- However, it was usually impossible to differ- ber of moves (hops + flights) per minute. entiate between true vigilance (scanning for The detectability of a bird is expected to predators) and looking for prey, foraging increase with the frequency of its move- sites, next perches or surveillance of flock- ments., but, at the same time, its effective vig- mates. Therefore, unless intentional scans ilance may be reduced since flying precludes could be clearly identified and timed, scan- attentiveness. ning included all stops or sit-and-wait activi- ties that could allow some antipredator Foraging success (SUC) or attack rate. Was the vigilance, even if it was not their main pur- number of prey capture attempts per minute, pose. As a result, whereas SEARCH values in addition to other moves. Prey attacks are may be conservative, actual SCAN often noteworthy in the perspective of both the tended to be overestimated. In short, VIS feeding enhancement hypothesis of flocking, was a variable that referred only to conspicu- and its antipredator advantages because prey ousness, SEARCH decreased and SCAN attacks and manipulations may focus the increased the vigilance rate, whereas VEL, bird’s attention and reduce its vigilance even SUC and MOVE all affected both conspicu- more than other foraging movements. ousness and vigilance.

Percentage of time spent moving (MOVE). Hops + Data analysis flights only were summed after being multi- The descriptive habitat and foraging parame- plied by their respective fixed duration. ters characterized the foraging environment and behavior of species that were originally Percentage of time spent searching for prey placed in groups on the basis of their flocking (SEARCH). This included prey attacks and propensity alone. On the other hand, the six

53 THIOLLAY summary variables (VIS to SCAN) were confirmed through Kolmogorov-Smirnov intended to look for differences in the goodness-of-fit and Bartlett tests respectively assumed vulnerability to predators of the spe- (Sokal & Rohlf 1981). When successive cies in each group, using the implied degree univariate tests were conducted, I used a Bon- of conspicuousness and the likely loss of vigi- ferroni adjustment of the P value and a signif- lance as indicators of vulnerability. icance level of P < 0.01. Generalized linear I used species as independent statistical models were used with individual observa- units although this assumption may not be tions as random effects, flocking categories as true because some species within a group fixed effects (no pseudo-replications) and

(especially F2) were phylogenetically related Tukey’s test for post-hoc testing to explore (even congeners) and they tended to forage factors affecting vulnerability, as well as under quite similar conditions. Therefore Spearman’s correlation coefficients on their behavior may not be independent from untransformed data. Logistic regressions of a statistical point of view and this may pro- non-intercorrelated factors with flocking cat- duce a pseudo-replication effect. However, I egory as the dependent variable were used to have not statistically controlled for this assess the determinants of flocking propen- phylogenetic effect because the main bird sity. All tests were two-tailed, all means were families were represented in all three groups ± 1 SD, and minimum levels of significance (Thamnophilidae, Tyrannidae) or present were set at P < 0.05. in two of them (Dendrocolaptidae, Furnari- idae) and the relative importance of different RESULTS families within the subset of species studied was not different from that found in the Habitat use. Six of the 12 solitary foragers were whole insectivorous, arboreal, understory found in the most open of the three forest bird community of the study area (Thiollay understory types (high mature, Table 1), while 1994). the 6 other species were chiefly recorded in Variables used were an index (VIS), fre- stands of intermediate density. quencies (VEL, SUC) or proportions (percent The 13 species of occasional flock partici- of total time spent: MOVE, SEARCH, pants (Table 2) were distributed in all forest SCAN) to weight foraging bouts of different types and heights, but they included the only lengths equally. However, by that very fact, species (5) in our sample which were associ- VEL, MOVE, SEARCH and SCAN were ated with the densest forest (C). In contrast, intercorrelated. I did not attempt to reduce all the obligate flock members (Table 3) typi- the number of variables, e.g., to principal cally occurred at mid or upper level (class 3) component scores, because the main goal was of open understory, although they also used to investigate the relative importance of these occasionally denser forest types. So, the pro- factors individually. MOVE, SEARCH and portion of species using the most open forest SCAN were used as dependent variables in understory (A) and its highest level (3) univariate factorial ANOVAs, with VIS or increased with flocking propensity (8, 23 and

VEL as factors. In parametric tests, VEL and 100% from group F0 to F2). VIS were log transformed, SUC was log(x + Even stronger differences appeared 1) transformed because of zero scores and among groups in foraging substrates. Air and MOVE, SEARCH and SCAN were arc-sine litter were used only by solitary foragers or square root transformed. Normality and occasional flock members ( Tables 1 and 2), homosedasticity of transformed data were whereas almost all epiphyte, bark or twig

54 VULNERABILITY IN MIXED-SPECIES FLOCKS

searchers and most foliage gleaners were classes of log2 body masses (2 = 8–16 g, to 6 found among obligate flock members (Table = 128–256 g, Thiollay 1994) did not differ 3). among the three groups (Kruskall-Wallis ANOVA, df = 2, H = 0.254, P = 0.880). Foraging speed. The most active foragers (speed It was difficult to estimate the relative

2 and 3, Table 1) were few in group F0 (2/12 importance of the frequency of movements species), numerous in F1 (8/13) and included (VEL) vs the visibility index (VIS) on the all the F2 species (Table 3), except the Dusky- actual detectability (or conspicuousness) of a throated (Thamnomanes ardesiacus) and Cinere- bird to a visually searching predator. VEL, ous (Tcaesius ) Antshrikes. The latter, only that was directly related to the foraging perch-hunting foragers among obligate flock behavior, was much lower (F1,942= 286,6, members, were in fact kleptoparasites, mostly P < 0.001) for sit-and-wait foragers (strikers foraging on prey disturbed or caught by other = 2.9 ± 2.3 and sallyers = 2.5 ± 2.4 move- species. They had also to move very often to ments/min) than for active foragers (search- follow their flock mates. Conversely, still ers = 21.9 ± 11.8, gleaners = 17.5 ± 9.2). hunting, which involved infrequent perch From the way VIS was measured, it was changes (< 6/min on average), was found dependent upon habitat and substrate types. only among F0, and to a lesser extent, F1 spe- It decreased significantly (F = 91.3, P < cies (Tables 1 and 2). 0.001) from mature open understory (6.9 ± 1.3) to low dense forest (1.9 ± 0.5), but not Foraging behavior. Hunting techniques paral- with increasing height above ground, where leled the above trends. Catching prey by VIS ranged from 4.9 ± 1.6 to 6.0 ± 1.6 (P = strikes (on trees or litter) or aerial sallies was 0.435). Of course, significant differences (P < common in F0 species (7/12), rare in F1 (3/ 0.001) occurred among substrates used, 13) and restricted to the atypical Thamnomanes where mean VIS indices ranged from 2.1 ± in F2. Conversely, the proportion of species 1.0 in dense tangles to 7.5 ± 2.1 on the open using the most active techniques (gleaning perches of flycatchers. As a result, the mean and searching) was twice higher among the species velocity increased sharply from soli- 12 obligate flocking species (n = 10) than tary to obligate flock foragers (VEL = 7.0 ± among solitary foragers (n = 5). 6.7 to 17.5 ± 11.0 moves/min, F2,941 = 114.1, The hops/flights ratio, that was related to P = 0.001). The mean index of visibility (VIS) both foraging method, density of vegetation varied widely among solitary and opportunis- and the kind of substrate, was highly variable tic foragers, but it was consistently high between species in all three groups and no among obligate flock members (6.7 ± 1.6) trend emerged. The percentage of relatively and significantly higher than among occa- large prey in the set of observed captures was sional on non flocking taxa (F2,941= 120.2, P similar also between the three groups (25.5– < 0.001). 25.9 ± 16.2–22.7%) Vigilance ability and flocking behavior. When they Detectability and flocking propensity. The larger are foraging, birds may be able to look at the (100–250 g) and only brightly colored taxa in same time for predators (vigilance) provided our species set (Trogon, Momotus, Galbula) were they are neither moving, nor manipulating or solitary foragers, and they appeared very closely investigating a substrate. Thus, the quiet and inconspicuous in their natural set- proportion of time spent moving (MOVE) ting. The distribution of species among six and searching (SEARCH) is expected to be

55 THIOLLAY inversely correlated with vigilance. Scanning P < 0.005), whereas there was no significant (SCAN), a straightforward measure of vigi- differences between the success rates of spe- lance, was indeed negatively correlated with cies pouncing, flycatching or searching (P = SEARCH, VEL and MOVE (Pearson’s coef- 0.058 to 0.329). Species foraging on foliage ficient rs = - 0.72 to - 0.99, P < 0.01). There- (0.70 ± 0.58) and bark (0.62 ± 0.60) had a fore frequent foraging movements or higher SUC than those using any other sub- substrate searching may considerably lower strates (0.39 to 0.49) and significantly so (t- the rate of vigilance. tests, P = 0.0002 and 0.0132 respectively). All foraging behaviors pooled, mean Overall, the mean foraging success increased

SEARCH time increased significantly (F2,941 = from solitary foragers (0.44 ± 0.47) to flock

345.5, P < 0.001) from solitary foragers (4.1 ± members (0.67 ± 0.55, F2,941 = 15.7, P < 3.9%) to occasional (24.9 ± 26.4) and obligate 0.001) in parallel with the increasing propor- flock members (62.0 ± 34.8), as did MOVE tion of small foliage gleaners and bark search- (from 5.0 ± 3.6 to 11.1 ± 5.7, F = 88.4, P < ers. 0.001), whereas SCAN decreased (F = 332.0, P < 0.001) respectively from 90.8 ± 7.7 to Intraspecific differences between solitary and flock for- 65.5 ± 31.0 and 26.7 ± 38.2%. Results would aging. Only two species provided enough have been even more striking if species that observation samples in contrasting situations, have odd behaviors (Thamnomanes and Myio- i.e., when they were foraging either associated bius in species group F2, see Appendix 1) had with a multispecies flock or solitarily. The been excluded. This result is a consequence of Wedge-billed Woodcreeper (Glyphorhynchus the much higher proportion of both fast spirurus) occurred in most flocks but also reg- active gleaners and substrate searchers in ularly foraged independently, whereas the flocking than solitary foraging birds. Among White-flanked Antwren (Myrmotherula axil- gleaners alone, search time increased and laris) was an almost obligate flock member, scanning decreased from solitary foragers to rarely foraging in isolated pairs. flock members. Within each species separately, the mean value of each variable was compared between Foraging success and flocking behavior. According flock and solitary foraging bouts (ANOVAs, to the feeding enhancement hypothesis of Fig. 1). The woodcreeper exhibited no signifi- flocking, an increased foraging success (num- cant difference of its conspicuousness (VIS), ber of prey capture per min of active foraging foraging speed (VEL) and success rate (SUC) time, SUC), and/or a decrease in the variance when foraging alone compared to foraging in of feeding rate should be the main benefits flocks. Only its scan rate (SCAN) was signifi- and determinants of flocking. This rate, how- cantly lower in flocks (- 44%). For this spe- ever, was difficult to interpret and compare cies, joining opportunistically encountered between species because of its expected rela- flocks, social foraging apparently did not tionships with prey type, size, energy content result in a decisive improvement of its forag- and availability as well as predator body size ing conditions. Conversely, the Antwren and requirements. seemed to benefit more strongly from its Foraging success was inversely correlated association with flocks where it foraged faster with body size (r = - 0.123, t = - 4.325, P < (VEL = + 41%), in significantly more 0.001). Gleaners had a significantly higher exposed sites (VIS = + 66%), and where it mean SUC (0.67 ± 0.57) than any other type was less vigilant (SCAN = - 21%) than when of foragers (0.41 ± 0.38 to 0.54 ± 0.52, t-tests, foraging alone (Fig. 1).

56 VULNERABILITY IN MIXED-SPECIES FLOCKS

FIG 1. Intraspecific differences of the visibility index, foraging velocity, success rate, and scanning frequency of the Wedge-billed Woodcreeper (Glyphorhynchus spirurus) and the White-flanked Antwren (Myr- motherula axillaris) foraging either solitarily or in mixed flocks. Mean values ± 1 SD. VEL, VIS and SUC are log-transformed. P values of the differences between solitary and flock foraging (ANOVAs) are given. NS = P > 0.05.

General correlates of flocking propensity. Using lower F value than SEARCH or SCAN (88 vs flocking category as the independent variable 336–351). All interactions between any of the in a generalized linear model and pooling all VIS, VEL, SUC, SEARCH and SCAN fac- species within groups, each of the six factors tors were also highly significant (F = 70–112, measured differed significantly between obli- df = 6–10, P < 0.001, Wilks Lambda = 0.42– gate, facultative and non flock members 0.67). (ANOVA, P < 0.001). Foraging success In a multiple logistic regression of VIS, (SUC), however, had a lower F ratio that VIS VEL and SUC on flocking category, the over- or VEL (15 vs 113–164), and MOVE had a all coefficient of determination (R2) was

57 THIOLLAY

0.280, but only VIS and VEL were significant Costs and benefits of flocking. Potential benefits in (c2 = 250–340, P < 0.001) and not SUC (c2 = terms of feeding success were not the topic of 0.104). Separately, MOVE, SEARCH and this study. Any bird feeding in group may be SCAN were also highly significant (c2 = 199– expected to look at flock mates and thus may 518), but R2 was lower for MOVE (0.106) get information, may improve its foraging than for SEARCH and SCAN (0.263–0.276). technique and feeding rates, or merely may be In summary, the syndrome of at least obli- stimulated by movements of other birds. In gate flocking is the conjunction of a more Madagascar rain forest, for instance, several active foraging behavior than non flocking species increased their feeding rates and mod- species (frequency of movements and/or sub- ified their foraging techniques in heterospe- strate searching), in more exposed situations cific flocks through mutualism and (density of the surrounding vegetation) and a commensalism (Hino 1998). However, that at lower vigilance (scanning rate). least some birds may improve their fitness by following more experienced foragers may be a DISCUSSION mere opportunistic consequence of such associations and not the primary determinant There are many forms of flocking even in of flocking. tropical forests alone (Thiollay & Jullien Interspecific differences are difficult to 1998), each of them with possibly different interpret. Obligate flock members should causes and consequences. Our results and derive the most critical benefit from their interpretations here only refer to mixed-spe- association with other birds. A less decisive cies flocks of insectivores in the understory of advantage is expected in facultative flocking. lowland Neotropical forests, one of the most Only two such species could be compared in permanent and highly evolved type of flock- contrasting situations. The Wedge-billed ing. Woodcreeper was on average neither in more For the flocking behavior to evolve, bene- exposed sites, nor moving faster, nor more fits must outweigh costs. This study could successful when foraging in flocks. It proba- not, and no other study has yet measured and bly did not derive from this association a ben- combined all the possible benefits and costs efit decisive enough to consistently outweigh of flocking. Some benefits (e.g., feeding the costs incurred. Conversely, the White- enhancement) may be more immediate and flanked Antwren, a nearly obligate flock easily measurable than others (e.g., antipreda- member, showed an obvious advantage in tor protection), though the former are joining flocks where it used more exposed not necessarily more determinant than the sites, moved faster, had a higher success and latter. Benefits also can be either root causes lower vigilance. The two antshrikes were a or mere consequences of feeding associations. particular case: they obtained a large part of The sit-and-wait or slow foraging behavior, their food from insects flushed by flock mates or the semi-terrestrial habits, or the use or from kleptoparasitism. This may be a of dense vegetation, or a small territory size, strong incentive for them to join flocks. typical of non-flocking species, may be either Because of their slower foraging speed, high simply not compatible with the speed and vigilance and loud calls, they could act as effi- range of foraging flocks., or they may be cient sentinels and they were mainly responsi- sufficient antipredator defenses to make ble for the cohesion of the flocks (Jullien & flocking unnecessary or unprofitable Thiollay 1998), from which they may also get (incurred costs). protection (the “many eyes” and “safety in

58 VULNERABILITY IN MIXED-SPECIES FLOCKS number” hypotheses). Other flock members tance from any hide from where a predator suffered (moderately) from their parasitism, could launch a surprise attack.. Therefore, but this may have been far outweighed by the both very open (high detection radius) or protection gained from these sentinels. very dense (protective) vegetation may co- Obligate flock species, in our study area, infer the lowest predation risk. The semi- had a higher survival rate than solitary and open understory of primary forest is interme- even facultative flock members (Jullien & diate, and thus expected to be the most risky Clobert 2000). During > 1000 h spent watch- habitat. It may provide some protection if ing mixed flocks (Jullien & Thiollay 1998, and nearby refuges are available, but foraging unpubl.), in this forest with a rich predator birds remain visible and stalking predators are community (Thiollay 1989), raptor attacks often concealed by trunks and dim light. were very rare (7 observed) and actual cap- Frequent movements or substrate prob- tures even rarer (2 records). So, there was no ing preclude, or at least reduce, vigilance, evidence that an increased detectability of unless the bird stops to scan (loss of foraging flocks resulted in increased predation rate. time). On the contrary, perch hunting allows Within flocks, suggestions of serious intra some antipredator vigilance while looking for on interspecific competition were almost prey. So, when velocity or searching increase, absent (only brief and occasional cases of overt vigilance can only be accomplished at aggressive interference). Most flocks included the expense of feeding (Lima & Bednekoff a single pair of each species (Jullien & Thiol- 1999). Birds are known to change their forag- lay 1998), and birds followed independent ing behavior and habitat use and increase paths, using their specific foraging behaviors, their vigilance rate under increasing predation substrates and prey types. Even the average risk (Lima 1982, Lendrem 1983, Lima & Dill risk of kleptoparasitism by antshrikes was 1990, Suhonen 1993, Barbosa 1997). low. Therefore, the real cost of flocking was Flocking has well known antipredator likely to be minimal, unless some scramble advantages, such as high collective vigilance competition occurred. and efficient escape flights or freezing behaviors (Morse 1970, Pulliam 1973, Powell 1985, Vulnerabilty and vigilance. Foraging behavior Elgar 1989, Master et al.. 1993). Permanent may be related to antipredator defense in two tropical forest flocks have highly vigilant ways: 1) the degree of conspicuousness of a leaders and interspecific responsiveness to foraging bird, and 2) the level of vigilance it their mutual alarm calls (Jullien & Thiollay can maintain while looking for prey. Addi- 1998). Observations of encounters between tionally, habitat structure may influence both these mixed flocks and forest raptors (e.g., foraging behavior, conspicuousness and vigi- forest falcons, Micrastur spp.) also strongly lance requirements. Morphology, especially suggested that flocks had a deterrent effect body size, may also affect conspicuousness on predators which rarely tried to attack and even foraging behavior. them, as already documented in an African The conspicuousness, or detectability, has rain forest (Thiollay 1984). two components: active (frequency of movements, i.e., velocity) and passive (density of Behavioral correlates of flocking propensity. The vegetation, i.e., visibility). A bird may be presence, or fear of predators may constrain either concealed by vegetation and substrate foraging behavior and/or foraging sites, and and inaccessible to a predator (e.g., in vine increase the tendency of birds to flock (Curio tangles) or it may be in the open at a safe dis- 1976, Morse 1977, Schneider 1984, Elgar

59 THIOLLAY

1989, Lima & Dill 1990, Suhonen 1993). This threat from diversified predators (snakes, relationship was documented in temperate birds, mammals), or the fear they may inspire ecosystems but not yet in tropical forests, are difficult to quantify. So, the predation risk, where the diversity, if not the density, of pred- behaviors roused by fear, or antipredator ben- ators may be higher (Greene 1988). efits, are difficult to assess and the related It seems that the most regular mixed-spe- hypotheses are uneasy to test directly. Any cies flock of insectivorous birds in tropical feeding enhancement, from information forest understories may share a unique set of transfer to increasing foraging success, can be foraging behaviors, substrates and/or micro- a cause as well as a consequence of flocking. habitats that make them more conspicuous or Hypotheses are only testable on facultative exposed and less vigilant than ecologically flock members whose behaviors should be similar, but solitary foragers. This possibly compared in and out of flocks in similar envi- higher susceptibility to predation could ronmental conditions. But how to deal with explain their strong association with mixed species that are always solitary foragers or flocks because of the antipredator protection obligate flock members? The contrasting afforded by such flocks, and especially their behavioral syndromes of solitary and flocking sentinels. The hypothesis was supported by foraging birds suggest a complementary the consistent correlation between flocking explanation that may be called the vulnerabil- propensity and expected determinants of vul- ity hypothesis, stated as follows. nerability or predation risk. Facultative flocking species would join The results suggest that, from solitary for- flocks to benefit from the collective vigilance, agers to occasional and obligate flock mem- and/or experience of flock mates. In doing bers, the overall conspicuousness of birds so, they may reduce the time lost scanning, increased significantly (decreasing conceal- increase their feeding rate, and/or decrease ment by surrounding vegetation, increasing their predation risk. Additionally, when forag- habitat openness and frequency of move- ing in flocks, they could adopt more vulnera- ments), while their potential vigilance ble, but more successful behaviors, or they decreased (increasing proportion of foraging could use more dangerous microhabitats or time spent moving and/or searching). On the prey types, while keeping below a safety contrary, species foraging always or regularly threshold. When reversing to solitary forag- alone were either still or slow-moving hunters ing, they may tend to use more inconspicuous in open understory, or faster and frequently tactics and less exposed sites, reminiscent of moving species in dense vegetation or low antipredator adaptations. Permanent (obli- over the ground. In fact, most birds foraging gate) flock members should stay in groups out of flocks were almost always in pairs, an because their conspicuous and little vigilant intermediate behavior between flocking and foraging behavior and semi-open habitat true solitariness. This is typical of many soli- would put them too much at risk, if they were tary species in tropical forests (pers. observ.) foraging alone. I hypothesize that this forag- and is likely to provide an increased safety ing syndrome is fixed and not a mere conse- through shared vigilance and experience. quence of being in the safety of a flock. For Additionally, most of them had surprisingly these obligate flock members, it would be the secretive and inconspicuous behaviors. best, if not only alternative, to compensate for their unsafe foraging behaviors if they are A general theory. Predation events are very actually unable to use different foraging strat- rarely observed in the field and the actual egies to do without protective sentinels.

60 VULNERABILITY IN MIXED-SPECIES FLOCKS

Moreover, flocking would also allow them to Cimprich, D. A., & T. C. Grubb, Jr. 1994. Conse- use resources (microhabitats, substrates or quences for Carolina Chickadees of foraging prey types) not safely accessible to solitary with Tufted Titmice in winter. Ecology 75: foragers. This could give them a competitive 1615–1625. advantage decisive enough to maintain their Cressvell, W. 1994. Flocking is an effective anti- predation strategy in Redshanks, Tringa totanus. flocking behavior on an evolutionary time Anim. Behav. 47: 611–617. scale. Curio, E. 1976. The ethology of predation. Springer Verlag, New York, New York. ACKNOWLEDGMENTS Diamond, J. 1987. Flocks of brown and black New Guinean birds: a bicolored mixed species for- This work was a by-product of a wider study aging association. Emu 87: 201–211. funded by a grant from the French Ministry Elgar, M. A. 1989. Predator vigilance and group of Environment (SRAE). It was conducted as size in mammals and birds: a critical review of an addition to the Ph.D. of Mathilde Jullien empirical evidence. Biol. Rev. Camb. Philos. on the ecology of mixed-species flocks, and I Soc. 64: 13–35. thank her for sharing ideas on this topic, as Ekman, J. 1979. Coherence, composition and terri- tories of winter social groups of the Willow well as Douglas Stotz for comments on an Tit, Parus montanus, and the Crested Tit, Parus earlier version. cristatus. Ornis Scand. 10: 656–68. Ekman, J. 1987 Exposure and time use in Willow REFERENCES Tit flocks: the cost of subordination. Anim. Behav. 35: 445–452. Altmann, J. 1974. Observational study of behavior: Ekman, J., & M. Hake. 1988. Avian flocking sampling methods. Behaviour 49: 227–267. reduces starvation risk: an experimental dem- Barbosa, A. 1997. The effects of predation risk on onstration. Behav. Ecol. Sociobiol. 22: 91–94. scanning and flocking behavior in Dunlin. J. Erard, C. 1987. Ecologie et comportement des Field Ornithol. 68: 607–612. Gobemouches (Aves: Muscicapinae, Platys- Barnard, C. J. 1983. Animal behaviour. Wiley Inter- teirinae, Monarchinae) du Nord-Est du Science, New York, New York. Gabon. I. Morphologie des espèces et organi- Barnard, C. J., & H. Stephens. 1983. Costs and sation du peuplement. Mem. Mus. Natl. Hist. benefits of single and mixed species flocking in Nat. Zool. 138: 1–256 . Fieldfares (Turdus pilaris) and Redwings (T. ilia- Faaborg, J. 1988. Ornithology. An ecological cus). Behaviour 84: 91–123. approach. Prentice Hall, Englewood Cliffs, Bertram, B. C. R. 1978. Living in groups: predators New Jersey. and prey. Pp. 64–96 in Krebs, J.R., & N. B. Fanshawe, J. H. 1995. Effects of selective logging Davies (eds.). Behavioural ecology. Blackwell, on the bird community of Arabuko-Sokoke Oxford, UK. forest, Kenya. Ph.D. diss., Univ. of Oxford, Brosset, A. 1969. La vie sociale des oiseaux dans Oxford, UK. une forêt équatoriale du Gabon. Biol. Gabon- Giraldeau, L. A., C. Soos, & G. Beauchamp. 1994. ica 5: 29–69. A test of the producer-scrounger foraging Buskirk, W. H. 1976. Social systems in a tropical game in captive flocks of Spice Finches, Lon- forest avifauna. Am. Nat. 110: 293–310. chura punctulata. Behav. Ecol. Sociobiol. 34: Buskirk, W. H., G. V. Powell, J. F. Wittenberger, R. 251–256. E. Buskirk, & T. V. Powell. 1972. Interspecific Graves, G. R., & N. S. Gotelli. 1993. Assembly of bird flocks in tropical highland Panama. Auk avian mixed-species flocks in Amazonia. Proc. 89: 612–624. Natl. Acad. Sci. USA 90: 1388–1391. Caraco, T. 1979. Time budgeting and group size: a Greene, H. W. 1988. Species richness in tropical therory. Ecology 60: 611–617. predators. Pp. 259–280 in Almeda, F., & C. M.

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63 THIOLLAY etection d Scan 4.6 ± 2.0 97.6 ± 2.0 97.6 ± 0.6 98.7 ± 1.9 96.9 ± 0.5 98.7 ± 3.2 91.1 ± 4.4 82.6 ± 1.7 88.5 ± 3.3 90.9 ± 4.1 93.6 ± 1.1 97.4 ± 2.8 93.5 ± 3.0 84.1 ± 2.8 96.3 ± 5.8 73.5 ± 7.4 75.6 ± 4.3 78.9 ± 6.0 74.6 ± 4.1 72.9 ± 7.1 74.7 ± 1.9 94.4 ± 2.8 91.4 ± 5.4 18.4 ± 4.3 77.7 , as in Tables in , as 2 to F arching (observingarching 0 e /min; success = number success /min; Search s roup F 0.6 ± 0.7 0.6 ± 0.4 0.2 ± 1.0 1.3 ± 0.4 0.3 ± 2.0 4.9 ± 3.8 8.7 ± 1.8 5.9 ± 2.0 3.4 ± 3.6 3.8 ± 0.5 0.4 ± 1.1 2.1 ± 1.7 4.1 ± 2.4 1.9 ± 0.4 0.9 ± 1.2 1.6 ± g 19.6 ± 4.6 19.6 ± 8.8 73.9 ± 6.6 18.6 ± 3.5 13.9 ± 4.8 15.7 ± 4.3 14.4 ± 5.6 17.4 ± 4.7 70.5 ± 4.4 10.1 ± Move 1.8 ± 1.6 1.1 ± 0.5 1.8 ± 1.0 1.0 ± 0.0 4.0 ± 2.0 8.7 ± 2.3 5.6 ± 1.2 5.7 ± 1.5 2.5 ± 1.0 2.2 ± 1.1 4.5 ± 1.9 1.8 ± 0.9 6.9 ± 3.2 5.9 ± 1.8 7.1 ± 1.8 9.7 ± 2.8 7.9 ± 2.7 4.7 ± 1.8 7.0 ± 2.7 11.8 ± 2.4 11.8 ± 8.5 21.5 ± 3.5 12.7 ± 3.5 11.1 ± 3.2 12.2 Success 0.3 ± 0.5 0.3 ± 0.2 0.6 ± 0.5 0.6 ± 0.1 0.1 ± 0.3 0.3 ± 0.6 0.7 ± 0.2 0.2 ± 0.3 0.5 ± 0.3 0.4 ± 0.2 0.2 ± 0.3 0.6 ± 0.3 0.5 ± 0.2 0.3 ± 0.4 0.5 ± 0.7 0.9 ± 0.3 0.2 ± 0.2 0.2 ± 0.6 0.7 ± 0.4 0.8 ± 0.6 0.5 ± 0.2 0.5 ± 0.4 0.5 ± 0.3 0.5 ± 0.3 0.4 ± Velocity 0.7 ± 0.5 0.7 ± 0.5 0.6 ± 0.2 0.3 ± 0.2 0.3 ± 3.5 5.5 ± 2.3 8.0 ± 2.7 7.1 ± 1.3 2.2 ± 1.2 2.5 ± 2.3 4.2 ± 0.3 0.5 ± 3.6 9.8 ± 2.0 4.4 ± 3.0 6.0 13.9 ± 4.0 20.7 ± 4.8 13.4 ± 7.4 12.3 ± 3.9 14.9 ± 4.8 20.7 ± 6.2 13.9 ± 5.5 20.1 ± 7.0 23.5 ± 5.3 38.0 ± 17.2 Visibility 6.9 ± 1.0 8.4 ± 1.4 9.3 ± 1.0 9.1 ± 1.0 4.1 ± 1.4 4.3 ± 1.4 4.5 ± 0.5 6.1 ± 1.0 6.6 ± 1.1 7.2 ± 1.2 5.1 ± 0.8 2.8 ± 0.7 9.1 ± 1.6 2.5 ± 0.7 4.9 ± 1.4 1.4 ± 0.5 2.4 ± 0.5 4.9 ± 1.4 2.0 ± 1.0 2.3 ± 0.8 7.4 ± 2.2 4.6 ± 1.1 1.2 ± 1.1 3.2 ± 0.9 scanning(stopped and looking around). Species are listed from ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) ) Glyphorhynchus spirurusGlyphorhynchus Platyrinchus coronatus ) Thamnophilus murinus Thamnophilus Myrmotherula guttata Terenotriccus erythrurusTerenotriccus Malacoptila fusca Malacoptila Mionectes macconnelli Mionectes Momotus momota Ramphocaenus melanurus Automolus rubiginosus Thamnophilus amazonicusThamnophilus Galbula albirostrisGalbula Microrhopias quixensis Hylophylax poecilonota Hylophylax Percnostola leucostigma Percnostola Hylophylax naevia Trogon viridis Cymbilaimus lineatus Cymbilaimus Microbates collaris Hypocnemis cantator Hypocnemis Rhynchocyclus olivaceus Rhynchocyclus Monasa atra Cercomacra cinerascens Thryothorus coraya Indices of conspicuousness Means and vigilance ± SD fromobservation all in Visibility foraging birds. = cumulative periods. . White-tailed ( Trogon Motmot ( Blue-crowned ( Jacamar Yellow-billed White-chested Puffbird( ( Mouse-colored Antshrike Antbird ( Warbling Spot-winged Antbird ( Antbird ( Spot-backed ( Antbird Scale-backed Spadebill ( Golden-crowned ( Flycatcher Ruddy-tailed Collared Gnatwren( ( Nunbird Black ( Foliage-gleaner Ruddy ( Woodcreeper Wedge-billed ( Antshrike Fasciated Amazonian Antshrike ( Antwren( Rufous-bellied Dot-winged ( Antwren ( Antbird Gray McConnell's Flycatcher ( Flatbill ( Olivaceus ( Wren Coraya Long-billed Gnatwren( SOLITARY FORAGERS SOLITARY MEMBERS OCCASIONAL FLOCK APPENDIX 1 distancesalong of foragingindividuals six orthogonal directions(range = 0–12, seehopsflightof methods); + number = velocity move attempts/min; capture of searchflights+ (hops attempts); + capture moving spent time = % foraging total of = s spent % time or manipulating substrate + handling prey); scan = % time spent 1–3.

64 VULNERABILITY IN MIXED-SPECIES FLOCKS 3.4 ± 1.3 7.2 ± 2.8 6.8 ± 1.7 4.2 ± 1.6 4.4 ± 1.3 3.8 ± 1.6 4.7 ± 1.7 3.6 ± 1.0 3.5 ± 0.6 91.0 ± 4.2 91.0 ± 3.5 92.0 ± 3.4 94.1 ± 6.7 73.2 5.9 ± 2.8 5.9 ± 2.6 2.8 ± 2.0 2.0 ± 85.2 ± 4.0 85.2 ± 3.4 84.5 ± 3.3 81.2 ± 5.1 79.0 ± 5.9 80.0 ± 4.2 85.7 ± 4.3 80.9 ± 4.0 82.4 ± 5.8 17.0 ± 79.3 ± 11.5 79.3 ± 3.1 ± 1.6 8.4 ± 2.4 5.2 ± 2.1 3.9 ± 1.8 9.8 ± 4.5 11.4 ± 3.8 11.4 ± 3.5 12.0 ± 4.8 16.8 ± 5.0 15.6 ± 4.3 10.5 ± 4.6 13.0 ± 4.6 15.5 ± 4.1 14.1 0.2 ± 0.3 0.2 ± 0.4 0.5 ± 0.4 0.4 ± 0.4 0.5 ± 0.5 0.5 ± 0.4 0.4 ± 0.5 0.6 ± 0.5 0.5 ± 0.4 0.5 ± 0.5 0.8 ± 0.6 0.9 ± 0.6 1.0 ± 0.5 0.7 ± 4.0 ± 1.8 4.0 ± 2.7 4.6 ± 1.4 3.0 18.9 ± 7.9 13.6 ± 4.9 20.1 ± 7.0 30.1 ± 9.2 27.2 ± 8.9 16.7 ± 7.6 21.1 ± 9.1 25.4 ± 7.8 22.5 ± 7.7 14.1 ± 8.2 Visibility Velocity Success Move Search Scan 7.6 ± 1.6 6.2 ± 1.4 5.8 ± 1.1 5.7 ± 0.9 5.5 ± 1.4 5.4 ± 1.1 7.5 ± 1.5 7.2 ± 1.4 6.2 ± 1.4 5.4 ± 2.0 7.0 ± 1.2 7.6 ± 1.2 8.0 ± 1.7 ) ) ) ) ) ) ) ) ) ) ) ) Xiphorhynchus pardalotus Xiphorhynchus Philydor erythrocercus Automolus infuscatus ) Myiobius barbatus Myiobius Thamnomanes ardesiacus Thamnomanes Tachyphonus surinamus Tachyphonus Myrmotherula gutturalis Myrmotherula axillaris Myrmotherula longipennis Campyloramphus procurvoidesCampyloramphus Thamnomanes caesius Thamnomanes Myrmotherula menetriesii Xenops minutus Fulvous-crested Tanager ( Tanager Fulvous-crested Curve-billed Scythebill ( ( Brown-bellied Antshrike ( Antwren Gray Plain Xenops( ( Chestnut-rumped Woodcreeper Dusky-throated Antshrike ( Cinereous Antshrike ( ( Flycatcher Sulphur-rumped White-flanked( Antwren Long-winged Antwren ( Long-winged Antwren Rufous-rumped Foliage-gleaner( Olive-backed Foliage-gleaner ( Foliage-gleaner Olive-backed OBLIGATE FLOCK MEMBERS OBLIGATE APPENDIX 1. 1. Continuation. APPENDIX