Evidence for Facilitation Among Avian Army‐Ant Attendants: Specialization and Species Associations Across Elevations

Home , Army ant, Lesser greenlet, Ochraceous wren, Olivaceous woodcreeper, Plain antvireo, Ruddy treerunner

BIOTROPICA 49(5): 665–674 2017 10.1111/btp.12452

Evidence for facilitation among avian army-ant attendants: specialization and species associations across elevations

Sean O’Donnell Department of Biodiversity Earth and Environmental Science, Drexel University, Philadelphia, PA 19104, USA

ABSTRACT Mixed-species assemblages can involve positive and negative interactions, but uncertainty about high-value patchy resources can increase the value of information sharing among heterospecific co-foragers. I sampled species composition of bird-flocks attending army-ant raids in three adjacent elevation zones in Costa Rica, across multiple years, to test for positive and negative associations among raid- attending bird species. My goal was to test whether the most frequent and specialized raid-attending species showed evidence of facilitat- ing or excluding other bird species. I quantified elevational variation in avian community composition at raids, then asked whether species composition was associated with variation in flock characteristics (flock size and species richness). I identified the most frequent raid-attending species (those that attended raids most frequently relative to their mist-net capture rates), and bird species that performed specialized army ant-following behavior (bivouac-checking, which allows birds to memorize and track mobile army-ant colonies). There was significant turnover of bird species among zones (including the frequent and specialized attendants); patterns of species overlap suggested a gradual transition from a Pacific-slope to an Atlantic-slope raid-attending bird fauna. Raid-attendance frequency was positively correlated with bivouac-checking behavior. With few exceptions, the most frequent raid-attending bird species, and the bivouac-checking species, also participated in the most species-rich flocks. High species-gregariousness suggests many of the frequently attending and/or bivouac-checking species functioned as core flock members. However, some bird species pairs were significantly negatively associated at raids. Despite species turnover, per-flock numbers of birds at raids did not differ among geographic zones, but flocks on the Pacific- slope were heavier because larger bodied bird species attended raids. Previous studies showed that the size (biomass) of bird-flocks cor- responds to the amount of food the birds kleptoparasitize from ant raids, and the heavier Pacific-slope bird-flocks could have greater negative kleptoparasitic impacts.

Abstract in Spanish is available with online material.

Key words: bivouac-checking; Costa Rica; elevational gradient; multi-species associations; montane forest; social network analysis.

MIXED-SPECIES ASSEMBLAGES CAN INVOLVE COMPLEX COMBINATIONS advancing ant swarms, and raid-attending birds kleptoparasitize of positive and negative interactions (Hancock & Milner-Gulland the ants by reducing army-ants’ prey capture rates (Willis & Oniki 2006, Odadi et al. 2011, Cortes-Avizanda et al. 2012). There is an 1978, Wrege et al. 2005). Swarm-raiding army-ant colonies occur inherent tension between competition and facilitation (e.g., recruit- at low densities, and colonies frequently emigrate to new nest ment to resource patches; shared vigilance) when multiple animal sites (Vidal-Riggs & Chaves-Campos 2008, O’Donnell et al. species exploit the same resource (Seppanen et al. 2007, Sridhar 2009). Because army-ant colonies are widely spaced and mobile, et al. 2012), but uncertainty about the occurrence and location of army-ant raids represent an unpredictable but high-value resource high-value patchy resources can increase the relative value of to insectivorous birds. Multiple sympatric species exploit this sin- information sharing among foragers (Hancock & Milner-Gulland gle shared resource, and bird-flocks at ant raids present an excel- 2006). lent opportunity to assess the roles of positive and negative Multi-species foraging flocks are characteristic of tropical interspecific interactions in governing foraging guild structure. forest avian communities; these flocks are important subjects for I asked whether interspecific facilitation was important to analyzing the ecology of mixed-species assemblages (Powell 1979, structuring flocks at army-ant raids. Flocks at raids typically com- Peron & Crochet 2009, Cordeiro et al. 2015, Goodale et al. 2015, prise multiple bird species, but sympatric bird species vary in Styring et al. 2016). In the Neotropics and Afro-tropics, mixed- their reliance on army-ant raids as a food source. Both positive species flocks of birds often forage at army-ant swarm raids and negative effects among bird species are possible at army-ant (Willis & Oniki 1978, Peters et al. 2008). Army-ant raid fronts raids. Some bird species, particularly specialized ant-following are mobile, advancing at approximately 15 m/h, and are often 3– birds in the family Thamnophilidae, are notably aggressive at 10 m wide (Swartz 1997). Birds feed on prey driven out by raids; antbird competition may exclude other birds from raids (Willis & Oniki 1978, Willson 2004, Brumfield et al. 2007, Touch- Received 30 November 2016; revision accepted 22 March 2017. ton & Smith 2011). However, playback studies of the calls of Corresponding author; e-mail: [email protected] obligate antbirds suggest other bird species can be recruited to ª 2017 The Association for Tropical Biology and Conservation 665 666 O’Donnell

raids by antbird vocalizations (Willis 1972, Chaves-Campos Harvey 2000). All data were collected in intact forest within or 2003). Unrelated groups of Ocellated Antbirds (Phaenostictus contiguous with large forest reserves (Children’s Eternal Rain mcleannani) travel through the forest, with informed birds leading Forest, Monteverde Cloud Forest Reserve, and adjacent private na€ıve birds to new army-ant colonies (Chaves-Campos 2011). forested properties). Life zone ecology, forest characteristics, and Observations near Monteverde, Costa Rica (January 2012) sug- avian communities of the sample area are discussed in several gested similar interactions occurred between species: groups of reference works (Hodridge 1966, Guindon 1997, Young et al. four bird species (P. mcleannani, Myrmeciza zeledoni, Gymnopithys leu- 1998, Haber 2000). I observed birds at N = 74 army-ant swarm capsis, and Catharus fuscater) departed and arrived at three raids raids. Data were collected during nine separate observation peri- simultaneously, travelling single-file through the forest (pers. obs.). ods that collectively spanned much of the year: 11 January–4 The challenges to birds of locating ant colonies and monopoliz- March 2005, 2 July–11 December 2005, 19 December 2007–1 ing raid fronts may reduce the costs of associating at raids, favor- January 2008, 7–10 April 2008, 7–19 January 2012, 20–27 July ing interspecific facilitation (Peiman 2010). 2012, 8–21 April 2013, 18 July to 5 August 2014, 22–24 March I used geographic variation in raid-attending bird-flock spe- 2015, and 11–29 July 2016. I grouped raid observations into cies composition to test whether facilitation was evident when three geographically adjacent elevation zones for analysis. From different sets of bird species were in attendance. Neotropical bird southwest to northeast across the continental divide, the zones I communities exhibit strong species turnover across elevation gra- sampled were: Pacific (28 raids observed, 1140 to 1450 masl, dients (Diamond 1973, Terborgh & Weske 1975, Blake & Loiselle roughly corresponding to the Premontane Wet Forest life zone), 2000, Jankowski et al. 2010). The available pool of insectivorous high elevation (25 raids observed, 1500–1680 masl, including birds in a given area should affect what birds attend raids in a Lower Montane Wet Forest and Lower Montane Rain Forest life given location (O’Donnell et al. 2012). zones), and Atlantic (21 raids observed, 910–1350 m asl, roughly Surface-swarming (bird accessible) army ants span a wide corresponding to the Premontane Rain Forest life zone). Linear elevation range in Costa Rica (O’Donnell et al. 2011), and birds dimensions of the study area were approximately 9.75 km N-S attend raids throughout the known range of surface-swarming by 10.25 km E-W. army ants (Vallely 2001, Kumar & O’Donnell 2007, O’Donnell et al. 2010, 2014). I tested whether the structure of flocks at raids SAMPLING FLOCK COMPOSITION AND BIRD BEHAVIOR AT ARMY-ANT changed with bird species identity by sampling in three adjacent RAIDS.—Army-ant foraging raids were detected by walking trails elevation zones in Costa Rican montane forests. I first quantified and encountering army-ant raid fronts or foraging columns, or by the degree of turnover of raid-attending bird species among ele- observing birds foraging near ground level. One or both of two vations. I used two methods to categorize the bird species that experienced observers (S.O’D. and A. Kumar: Kumar & O’Don- participated most strongly in foraging at raids. First, the relatively nell 2007, O’Donnell et al. 2010, 2014) participated in data collec- high frequency attendants were species that appeared at raids at tion (either alone or with other observers) at 95% of the raids. the highest rates, after accounting for local variation in mist-net Observers walked toward the swarm fronts and positioned them- capture rates. Second, specialized raid-attending bird species were selves 5–10 m from the edge of the ant swarm at a location with those that performed bivouac-checking, a specialized behavior an unobstructed view of the raid front. Observers waited 5 min which allows bird to localize and track army-ant colonies (Swartz for birds to resume foraging activity before collecting data. 2001, Logan et al. 2011). I used the observed patterns of species Observation sessions lasted for 1 h except when raid activity co-occurrence at army-ant raids within elevation zones to assess ceased, when heavy rainfall began, or when the ants traversed whether interspecific interactions played a strong role in shaping impassable terrain. All observations were during daylight hours flock composition; if high frequency or specialized attendants with observation start times from 0900–1600 local time. A maxi- were negatively associated with other species at raids, this would mum of three raids was observed per day (raids observed on the suggest interference or resource competition drives flock species same day were from different army-ant colonies). To avoid assembly (Bruno et al. 2003). Alternatively, if high frequency or resampling the same army-ant colony, I alternated sampling dates specialized attendants were positively associated with other spe- among geographic zones whenever possible. If I observed more cies at raids, these species could function as core flock members than one raid for a colony, I only analyzed data collected on the that facilitate attendance by other species (Srinivasan et al. 2010). first raid observed; when I was uncertain of colony identity Finally, I asked whether geographic variation in flock species within a zone, I only analyzed data from raids that were more composition was associated with differences in flock size and than 300 m linear distance from each other on the same day or flock species richness. I discuss the possible implications of bird- raids that were separated in time by at least 7 days. flock characteristics for army-ant foraging success. I collected data at the army-ant swarms following the methods of Coates-Estrada and Estrada (1989), recording the geo- METHODS graphic location (GPS coordinates) of the raid to the nearest 10 m, and the number and species identities of raid-attending STUDY SITES AND SAMPLING DATES.—I collected data in forests in birds. I identified birds to species based on plumage, behavior, the vicinity of Monteverde, Puntarenas Province, Costa Rica relative body size, geographic range, and vocalizations (Stiles & (Tilaran mountain range, N10180, W84480; Guindon 1997, Skutch 1989, Garrigues & Dean 2007). Bird nomenclature Facilitation in Ant-attending Birds 667

follows IOC World Bird List v. 7.1 (http://www.worldbirdnames. mist-net capture rate (birds/1000 net meter hours from Young org/; accessed 10 March 2017). et al. 1998) as a predictor covariate in the statistical model. Only birds seen pursuing or consuming prey fleeing from For each geographic zone, I developed an index to categorize the ants were counted as raid attendants. I used the maximum a set of relatively high frequency raid attendants, following the number of individuals seen at the same time as a conservative method developed by Peters et al. (2008, O’Donnell et al. 2010). estimate of the number of birds from each species at the raid. I Within each zone, I regressed the number of individuals seen at used species’ mean weight in grams taken from Stiles and Skutch raids against the local mist-net capture frequency of each bird spe- (1989) as an index of body size for each bird; for all analyses of cies (Young et al. 1998), calculating the 95% CI of the regression bird body weights I used metabolic biomass (g0.75) (Touchton & line. Bird species with attendance rates above the 95% CI of the Smith 2011). Unless otherwise noted, all statistical analyses were regression line were categorized as high frequency attendants. Mist- performed using SPSS v. 24 software (IBM corporation 2016). net capture rates may give biased estimates of species’ relative abundances (Remsen & Good 1996). The mist-net data were collected OBSERVATIONS OF BIRDS AT ARMY-ANT BIVOUACS.—I conducted prior to my observations, and changes in species composition bivouac-checking observations in the Pacific zone in June-July among elevations are likely to have occurred (Pounds et al. 1999). 2009, July 2012, May 2013, and July 2014, and in the Atlantic Therefore, I used performance of bivouac-checking behavior as an zone in January 2012. No High elevation zone bivouac-checking alternative method of identifying specialized raid-attending species. data were collected. I collected bird bivouac-checking data at I calculated the mean number of birds per bivouac for each species N = 34 Pacific bivouacs and N = 6 Atlantic bivouacs. Bivouac seen at raids in the Pacific and Atlantic zones. I used Pearson corre- observations were conducted in the morning or afternoon and lations to test the relationship between bivouac-checking rate lasted 120 min unless heavy rain fell or if the colony began raid- (birds/bivouac) and raid-attendance rate (birds/raid). ing. Behavioral data were collected following O’Donnell et al. (2010). A bird was classified as bivouac-checking when it flew ANALYSIS OF SPECIES CO-OCCURRENCE IN FLOCKS.—I analyzed spe- toward the bivouac site, perched within 5 m of the bivouac cies-association data and social network structure for flocks using (10 m distance limit for birds perching on tree trunks) in any SOCPROG v. 2.7 (for MATLAB 8.5.0, release 2015a, Whitehead direction, and oriented toward the ant mass or the entrance to 2009). I used species occurrence data (presence/absence) in each the bivouac site. Observers sat obscured by vegetation or camou- flock as the unit of replication within geographic zones. There- flage-cloth blinds approximately 10 m from the bivouac entrance fore, the analyses tested for the effects of a species presence in a in a location from which the bivouac entrance was clearly visible. flock (regardless of the number of individual birds) on presence Most birds were identified only to species because most birds of other species in the flock. I used bootstrapping procedures were not banded and many of the observed species have sexually implemented in SOCPROG to test for evidence of subdivision monomorphic plumage. I conservatively used the maximum of bird species into preferred assemblages within zones, correct- number of conspecifics seen simultaneously as the number of ing for each species’ relative frequency of raid attendance (Bejder bivouac-checking birds, unless the birds were sexually dimorphic et al. 1998, Whitehead 2008). Flock species composition was per- or were color banded for individual identification. mutated semi-randomly by shuffling species among flocks while holding species abundance constant (permute all groups in SOC- BIRD SPECIES DIFFERENCES IN RAID ATTENDANCE AND BIVOUAC- PROG). I present the results of Whitehead’s (2008) recom- CHECKING.—EstimateS v. 9.1 software (Colwell 2013) was used to mended test for overall species associations, the proportion of calculate species rarefaction curves with confidence intervals for non-zero elements in the association matrix. each geographic zone and raid-attending species overlap among I then tested for evidence of pairwise species avoidances. I geographic zones. I used overlap of 95% CI of species accumula- calculated all pairwise species associations with a two-tailed criti- tion curves to test for significant differences in overall species cal P-value cutoff of 0.05, selecting species pairs that were richness of raid-attending birds among geographic zones (Colwell significantly negatively associated at P < 0.025. Bootstrapping et al. 2012). To quantify raid-attending species turnover among permutation methods for analyzing pairwise associations can be geographic zones, the degree of species overlap among each pair- conservative and sensitive to the number of permutations exe- wise combination of geographic zones was calculated using the cuted (Whitehead 2009). I present results from 10,000 permuta- Chao-Jaccard estimated statistic with standard errors; this statistic tions with 500 randomization trials/permutation for each computes the probability a species randomly drawn from one geographic zone; in all cases, I also ran the analyses at 1000 per- geographic zone would be shared with the other geographic zone mutations and the bootstrapped P-values changed by <10% (Colwell 2013). I calculated the 95%CI value of the Chao-Jaccard between the 1000 and 10,000 permutation runs, suggesting the estimated statistic and used non-overlapping 95% CI to indicate 10,000 permutation effort was sufficient to yield reliable P-values significantly different levels of species sharing. (Manly 1995, Bejder et al. 1998). I used a generalized linear model (GLM) to test whether Finally, I used SOCPROG social network analyses to calcu- species’ raid-attendance frequency (birds/raid) corresponded to late the mean 95% CI association strength (number of species variation in mist-net capture rates among geographic zones. I associates) for all species in each zone, as well as the zone overall included bird species and geographic zone as fixed factors and mean association strength (Barrat et al. 2004). I plotted 668 O’Donnell

association strength against a measure of the frequency of raid in each geographic zone, five to six species were identified as attendance [Pr(raids attended)] for all species in each zone. Com- high frequency raid attendants in each zone (Fig. 2). Two high mon species with high association strengths may function as frequency attending species were shared between the high eleva- nuclear species and interspecific facilitators of flock participation; tion and Atlantic zones (Zeledon’s Antbird and Slaty-backed common species with low association strengths show evidence of Nightingale Thrush); all other high frequency attendants were interspecific avoidance and/or exclusion. unique to a single zone. I observed nine Pacific zone species and a non-overlapping FLOCK COMPOSITION DIFFERENCES AMONG GEOGRAPHIC ZONES AND set of six Atlantic zone bird species checking bivouacs (Table 1). ESTIMATED KLEPTOPARASITIC PRESSURE ON ARMY ANTS.—I tested Most of the frequent raid-attending species also checked bivouacs geographic zone differences in measures of flock composition (Table 1: Pacific zone: 6/6; Atlantic zone: 4/5). Bivouac-checking (number of birds, metabolic biomass of birds, and number of rates were significantly positively correlated with raid-attendance species) using GLMs, with geographic zone as a predictor vari- rates in both zones (Pacific zone: r = 0.59, P < 0.001, N = 39; able. Assumptions of normality and equality of variance were not Atlantic zone: r = 0.96, P < 0.001). However, a few species significantly violated. checked bivouacs but were not categorized as frequent attendants (Table 1: Pacific zone three species; Atlantic zone two species). RESULTS SOCIAL NETWORK ANALYSES OF SPECIES CO-OCCURRENCE.—There GEOGRAPHIC VARIATION IN BIRD SPECIES COMPOSITION.—I observed was no evidence that particular pairs of raid-attending bird spe- 685 birds from 79 species at raids (Table 1). Birds were observed cies were associated more often than expected: (Pr(non-zero at raids of three army-ant species: Eciton burchellii parvispinum, associations)- Pacific observed 0.42, bootstrapped 0.40, P = 0.89; Labidus praedator, and L. spinninodis. Eciton b. parvispinum was the high elevation observed 0.28, bootstrapped 0.27, P = 0.70; Pacific most abundant army ant in all zones, accounting for 93% of the observed 0.34, bootstrapped 0.34, P = 0.36). However, some N = 74 raids where army-ant species was recorded, and army- species pairs showed evidence of significant avoidance, co-occur- ant species did not differ in relative frequency among zones ring in flocks less often than expected based on their overall (v2 = 2.40, df = 4, P = 0.66). attendance frequencies (Table 2). In the Pacific zone, two rela- There was no evidence for geographic zone differences in tively large-bodied and common species (Blue-throated Toucanet total species richness of the raid-attending bird guilds: species and Brown Jay) were never seen together at raids; two common accumulation curves showed no significant differences among ground-foraging species (migrant Wood Thrush and resident geographic zones in species observed versus sampling effort White-eared Ground Sparrow) co-occurred rarely. In both high (Fig. 1; 95% confidence intervals of expected species richness elevation and Atlantic zones, Slaty-backed Nightingale Thrush overlapped among all geographic zones). Within bird species, was a high frequency species that was negatively associated with geographic variation in mist-net capture rates corresponded with three other species: Black-headed Nightingale Thrush and two zone differences in raid-attendance frequency: after accounting antbird (Thamnophilidae) species. for species and zone effects, species mist-net capture rates Most of the high frequency attending species and the bivouac- (birds/1000 net meter hours) were highly significantly correlated checking species in each zone had relatively high mean species- = with species raid-attendance rates (birds/raid: F1,155 21.2, association strengths, at or above the overall mean association P < 0.001; R2 = 0.51). strength (Fig. 3). The only exception was the relatively low associa- There was a gradual shift from a Pacific-slope raid-attend- tion strength of Zeledon’s Antbird in the high elevation zone. ing bird fauna to a distinct Atlantic-slope fauna: estimated probabilities of species sharing among habitats were lowest FLOCK STRUCTURE DIFFERENCES AMONG GEOGRAPHIC ZONES.— between the Pacific and Atlantic geographic zones while the There were no significant differences among the geographic fl = = high elevation zone showed moderate and statistically similar zones in the number of birds per ock (F2,70 0.33, P 0.72) fl fl = rates of species sharing with both anking geographic zones nor in the number of bird species per ock (F2,70 1.98, (Fig. 1; Chao-Jaccard estimated probabilities of species shar- P = 0.15). The weight of birds at raids (total metabolic biomass) ing 95% CI: Pacific with high elevation 0.5 0.15; high differed significantly among the geographic zones (Fig. 4; fi = = elevation with Atlantic 0.64 0.10; Paci c with Atlantic F2,70 4.31, P 0.02). Post-hoc analyses suggested the mean 0.16 0.06). metabolic biomass of Pacific flocks (189.4 g0.75/raid) was higher than high elevation flocks (100.5 g0.75/raid); Atlantic flocks had BIRD SPECIES DIFFERENCES IN RAID ATTENDANCE AND BIVOUAC- intermediate biomass and did not differ from the other zones 0.75 CHECKING WITHIN ZONES.—Bird species mist-net capture frequen- (125.5 g /raid) (Fig. 4). cies were weakly positively correlated with raid-attendance frequencies in two zones (Fig. 2; Pacific: R2 = 0.14, P = 0.008; DISCUSSION High: R2 = 0.12, P = 0.01); there was no significant relationship in the Atlantic zone (Fig. 2; R2 = 0.001, P = 0.82). After correct- The species richness of bird communities at army-ant raids did ing for the relationship of raid attendance with mist-net captures not differ significantly among the geographic zones sampled in Facilitation in Ant-attending Birds 669

TABLE 1. Frequencies of observing bird species at army-ant raids and army-ant bivouacs in three geographic zones in Costa Rican montane forests. Four-letter common name abbreviations are given for species named in the ﬁgures or other tables. Metabolic biomass (g 0.75; Stiles & Skutch 1989) is given for each species. Species identiﬁed as frequent raid attendants are indicated by shading; species observed checking bivouacs are indicated in bold text. Bird nomenclature follows IOC World Bird List v. 7.1 (http://www.worldbirdnames.org/; accessed 10 March 2017).

High Pacific elev Atlantic Atlantic Metab. Pacific Birds/ Birds/ Birds/ Birds/ Bird species common name Abbr. Bird species scientific name Biomass Birds/ Raid Bivouac Raid Raid Bivouac

Orange-billed Nightingale Thrush OBNT Catharus aurantiirostris 11.8 1.39 0.41 0.16 Brown Jay BRJA Psilorhinus morio 60.0 1.25 0.15 0.08 White-eared Ground Sparrow WEGS Melzone leucotis 16.8 1.00 0.26 0.12 Ruddy Woodcreeper RUWO Dendrocincla homochroa 17.1 0.71 1.12 0.08 0.10 Blue-diademed Motmot BDMO Momotus coeruliceps 36.3 0.79 0.12 0.04 Rufous-capped Warbler RCWA Basileuterus rufifrons 6.2 0.43 0.12 Three-striped Warbler TSWA Basileuterus tristriatus 6.4 0.18 0.60 0.10 Black-headed Nightingale Thrush BHNT Catharus mexicanus 12.8 0.48 0.19 Ruddy-capped Nightingale Thrush RCNT Catharus frantzii 12.2 0.07 0.36 White-throated Thrush WTTH Turdus assimilis 24.7 0.25 0.28 0.24 Slaty-backed Nightingale Thrush SBNT Catharus fuscater 14.4 2.36 1.38 0.83 Zeledon’s Antbird ZEAN Myrmeciza zeledoni 15.9 0.68 3.24 1.67 Ocellated Antbird OCAN Phaenostictus mcleannani 20.2 0.71 0.33 Spotted Antbird SPAN Hylophylax naevioides 8.7 0.57 Golden-crowned Warbler GCWA Basileuterus culicivorus 5.8 0.11 0.16 0.48 0.33 Gray-breasted Wood Wren Henicorhina leucophrys 8.7 0.04 0.44 0.29 Chestnut-capped Brush Finch CCBF Arremon brunneinucha 16.5 0.04 0.36 0.19 0.33 Plain Antvireo Dysithamnus mentalis 7.4 0.12 0.33 Rufous-and-white Wren RWWR Thryophilus rufalbus 11.2 0.39 0.21 0.04 Yellowish Flycatcher Empidonax ﬂavescens 6.4 0.11 0.24 0.05 Azure-hooded Jay Cyanolyca cucullata 28.7 0.20 0.19 Slate-throated Whitestart Myioborus miniatus 5.6 0.07 0.16 0.14 Bicolored Antbird BIAN Gymnopithys bicolor 12.8 0.33 0.33 Wood Thrush WOTH Hylocichla mustelina 18.2 0.18 0.08 0.05 Clay-colored Thrush Turdus grayi 25.7 0.16 0.14 Kentucky Warbler Geothlypis formosa 6.8 0.18 0.04 0.05 Northern Barred Woodcreeper NBWO Dendrocolaptes sanctithomae 25.0 0.14 0.24 0.04 0.05 Blue-throated Toucanet BTTO Aulacorhynchus caeruleogularis 49.1 0.21 0.09 White-throated Spadebill Platyrinchus mystaceus 6.0 0.04 0.08 0.10 Spotted Barbtail Premnoplex brunnescens 8.4 0.16 0.05 Black-faced Solitaire Myadestes melanops 13.8 0.20 Long-tailed Woodcreeper Deconychura longicauda 10.8 0.19 Wedge-billed Woodcreeper Glyphorynchus spirurus 8.2 0.19 Cabanis’s Wren Cantorchilus modestus 8.7 0.14 0.04 Swainson’s Thrush Catharus ustulatus 8.4 0.18 Wilson’s Warbler Cardellina pusilla 4.3 0.18 White-breasted Wood Wren Henicorhina leucosticta 8.0 0.04 0.14 Common Chlorospingus Chlorospingus ﬂavopectus 9.5 0.12 0.05 Black-throated Wren Pheugopedius atrogularis 10.8 0.14 Song Wren Cyphorhinus phaeocephalus 11.2 0.14 Ochraceous Wren Troglodytes ochraceus 5.4 0.12 Black-and-white Warbler Mniotilta varia 6.0 0.07 0.05 Dusky-capped Flycatcher Myiarchus tuberculifer 9.5 0.11

(continued) 670 O’Donnell

TABLE 1 (continued).

High Pacific elev Atlantic Atlantic Metab. Pacific Birds/ Birds/ Birds/ Birds/ Bird species common name Abbr. Bird species scientific name Biomass Birds/ Raid Bivouac Raid Raid Bivouac

Buff-rumped Warbler Myiothlypis fulvicauda 7.4 0.10 Northern Tufted Flycatcher Mitrephanes phaeocercus 5.0 0.10 Stripe-breasted Wren Cantorchilus thoracicus 12.2 0.10 Barred Forest Falcon Micrastur ruficollis 46.0 0.08 Silvery-fronted Tapaculo Scytalopus argentifrons 8.4 0.08 Streak-breasted Treehunter Thripadectes rufobrunneus 19.9 0.08 Olivaceous Woodcreeper Sittasomus griseicapillus 7.2 0.04 0.04 Chestnut-sided Warbler Setophaga pensylvanica 5.2 0.07 Lesser Greenlet Pachysylvia decurtata 5.2 0.07 Streak-headed Woodcreeper Lepidocolaptes souleyetii 19.9 0.07 Black-crowned Antshrike Thamnophilus atrinucha 10.8 0.05 Black-headed Antthrush Formicarius nigricapillus 24.2 0.05 Buff-throated Foliage Gleaner Automolus ochrolaemus 16.5 0.05 Chestnut-backed Antbird Myrmeciza exsul 12.2 0.05 Crimson-collared Tanager Ramphocelus sanguinolentus 15.9 0.05 Dull-mantled Antbird Myrmeciza laemosticta 11.2 0.05 Golden-crowned Spadebill Platyrinchus coronatus 5.2 0.05 Long-billed Gnatwren Ramphocaenus melanurus 5.6 0.05 Red-faced Spinetail Cranioleuca erythrops 8.0 0.05 Ruddy Treerunner Margarornis rubiginosus 8.7 0.05 Rufous-breasted Antthrush Formicarius rufipectus 25.5 0.05 Bay Wren Cantorchilus nigricapillus 11.8 0.04 Olive-striped Flycatcher Mionectes olivaceus 7.4 0.04 Slaty Antwren Myrmotherula schisticolor 5.4 0.04 Spot-crowned Woodcreeper Lepidocolaptes affinis 14.4 0.04 Spotted Woodcreeper Xiphorhynchus erythropygius 18.8 0.04 Tawny-throated Leaftosser Sclerurus mexicanus 12.2 0.04 Black-throated-green Warbler Setophaga virens 5.2 0.04 Canada Warbler Cardellina canadensis 5.8 0.04 Golden-winged Warbler Vermivora chrysoptera 5.0 0.04 Gray-headed Tanager Eucometis penicillata 13.1 0.04 House Wren Troglodytes aedon 6.4 0.04 Ovenbird Seiurus aurocapilla 8.7 0.04 Philadelphia Vireo Vireo philadelphicus 6.2 0.04 Squirrel Cuckoo Piaya cayana 32.8 0.04 Yellow-throated Brush Finch Atlapetes albinucha 13.8 0.04 this study, but the species composition of flocks at army-ant raids abundance at different elevations likely play a strong role in deter- varied geographically. There was significant turnover of raid- mining the local pool from which raid-attending birds are drawn. attending bird species across the elevation gradient I sampled. However, within all zones, species’ relative mist-net capture Although some species spanned the entire elevation range, overall rates were poor predictors of raid-attendance frequency. Several patterns of species sharing among zones were consistent with a species in each zone attended raids at relatively high rates and transition from a Pacific-slope to an Atlantic-slope raid-attending more frequently than expected based on their local mist-net cap- bird fauna. Species’ relative mist-net capture rates among zones ture rates. The identity of the most frequent raid-attending bird corresponded to their zone-specific raid-attendance frequencies, species varied among geographic zones, with no overlap of fre- suggesting zone differences in species raid attendance were quent attendants between the Pacific zone and the other zones. strongly affected by elevational differences in their relative abun- Thamnophilid antbirds were among the high frequency attending dance. Ecological or historical factors that affect bird species birds in the High and Atlantic zones. Resident Catharus thrushes Facilitation in Ant-attending Birds 671

FIGURE 1. A: Species accumulation curves generated by rarefaction, showing numbers of bird species observed plus/minus 95% confidence intervals FIGURE 2. Relationships of raid-attendance rates (number of birds/raid) versus sampling effort, for bird-flocks observed at army-ant raids in three with mist-net capture rates (from Young et al. 1998) for bird species observed geographically adjacent elevation zones in Costa Rican montane forest. B: at army-ant raids in three elevation zones. Best fit linear regressions (solid Venn diagram showing numbers of bird species and overlap of bird species lines) and 95% CI of the regression (dashed lines) are indicated. Bird species attending army raids in the three elevation zones. that attended raids at rates higher than the regression 95% CI are indicated by black symbols with four-letter common name abbreviations. Bivouac- (nightingale thrushes) and Basileuterus warblers were high fre- checking species are indicated by star symbols (Pacific and Atlantic zones quency attendants in all zones. In both genera, there was appar- only); high frequency species are indicated by black symbols, other bivouac- ent elevational segregation of species at raids, as suggested for checking species are indicated by gray symbols. See Table 1 for common and their overall local abundances by mist-net surveys (Young et al. scientific names of abbreviated species designations. 1998). Bivouac-checking was strongly, but imperfectly, associated with frequent raid attendance. Bivouac-checking species were species richness by many of the frequently attending and special- non-overlapping between the Pacific and Atlantic zones (no data ized species suggests ecological facilitation. These species may for high elevation zone). function as core flock members in their zones of highest raid- Nightingale thrushes and Basileuterus warblers of different attendance frequency. The bivouac-checking species are likely to species checked bivouacs in both the Pacific and Atlantic zones, initiate foraging at raids because they can track ant colonies and suggesting these genera converged on the army-ant tracking consequently are present when raids begin. Other bird species behavior of some Thamnophilid antbirds (O’Donnell et al. 2014). may be attracted to foraging flocks, possibly via vocal recruitment (Willis 1972, Chaves-Campos 2003). SPECIES ASSOCIATIONS AT RAIDS.—Most of the frequent raid-attend- Why do mixed-species flocks form and persist around the ing and bivouac-checking species in all zones participated in specialized raid attendants? Interspecific avian facilitation at ant flocks with at least average expected species richness, and many raids may persist because it involves low costs to the core species. of them participated in flocks with higher than average numbers The wide and mobile army-ant raid fronts may be difficult for of species. Attendance of flocks with higher than expected birds to monopolize while they are searching for flushed insect 672 O’Donnell

TABLE 2. Species pairs that associated in ﬂocks at lower than expected frequencies in each of three elevation zones near Monteverde, Costa Rica (critical P- value = 0.025).

Overlap Species 1 Species 2 index P-value

Paciﬁc Blue-throated Toucanet Brown Jay 0.00 0.023 Wood Thrush White-eared Ground 0.05 0.017 Sparrow High elevation Slaty-backed Nightingale Thrush Black-headed 0.05 0.013 Nightingale Thrush Atlantic Slaty-backed Nightingale Thrush Bicolored Antbird 0.11 0.002 Slaty-backed Nightingale Thrush Spotted Antbird 0.11 0.001 Slaty-backed Nightingale Thrush White-breasted 0.06 0.014 Wood Wren

prey, and division of prey items by size, and of prey type by foraging substrate, may also reduce the costs of foraging in the com- pany of other species at raid fronts (O’Donnell et al. 2014, but see Chesser 1995). Advantages of group foraging, such as selfish- herd predator dilution and shared vigilance, may favor mixed-species flock formation and maintenance at raids (Creel et al. 2014, Schmitt et al. 2014, Sridhar & Shanker 2014). The bird species in each zone did not show evidence of subdivision into exclusive assemblages. However, several species pairs fi showed evidence of avoidance or exclusion at raids. In the Paci c FIGURE 3. Relationships of mean + 95% CI network association strength zone, non-overlap between Blue-throated Toucanet and Brown Jay (species partners per flock) with raid attendance (proportion of raids attended) fi may be associated with intense interspeci c aggression related to for bird species in three elevation zones. Species identified as high frequency ’ nest predation (Williams & Hale 2006, S. O D. pers. obs.). Other raid attendants in each zone are indicated by shaded symbols; bivouac-check- cases may involve mutual avoidance or exclusion between species ing species are indicated by star symbols. The zone mean association strength that overlap in body size and foraging substrate (e.g., Wood Thrush is indicated by the dashed line. See Table 1 for common and scientific names and White-eared Ground Sparrow; Slaty-backed Nightingale of abbreviated species designations. Thrush and Black-headed Nightingale Thrush: Jankowski et al. 2010). Significant avoidance between two species of thamnophilid antbirds and Slaty-backed NightingaleThrush in the Atlantic zone set upper limits on the number of birds (and species) that can is of particular interest as all were frequent raid attendants. accumulate at a raid front, but my data suggest these factors do Geographically matched species co-occurrence data at a not involve species exclusion by strong competitors. Despite geo- shared resource can indicate positive or negative species associa- graphic variation in species composition, the mean number of tions, but these data represent outcomes and do not indicate birds per raid did not vary significantly among geographic zones. what mechanisms drive the patterns. For example, bird species The size of bird-flocks may be constrained by ant-raid travel rate, showing low species-level gregariousness by attending relatively total food availability, and/or physical space at raid fronts inde- species-poor flocks (e.g., Zeledon’s Antbird in the high elevation pendently of interspecific interactions (Willis 1966, 1985, Swartz zone) may either avoid joining speciose flocks, or drive other 1997, O’Donnell et al. 2014). birds from the flocks they join. Detailed data on interspecific Bird-flocks were heaviest (though they included similar num- interactions at raids, and data on birds’ time budgets among dif- bers of birds) in the Pacific zone. Birds kleptoparasitize the army ferent raids and away from raids, are needed to determine how ants they attend by consuming large, high-value prey items the interspecific positive and negative associations arise. ants would otherwise capture. Birds potentially impose negative effects on army-ant foraging success, and field experiments sug- GEOGRAPHIC VARIATION IN FLOCK STRUCTURE AND IMPLICATIONS FOR gested the total weight of birds in a flock explained more of the ARMY-ANT FORAGING SUCCESS.—Presumably, there are factors that variation in costs to the ants than the number of birds (Wrege Facilitation in Ant-attending Birds 673

with data collection in the ﬁeld. Thanks to Frank Joyce and Katy Van Dusen for logistical support in Monteverde, and to residents of the Monteverde area who allowed access to private properties for data collection. The Tropical Science Center, San Luis Eco- lodge/University of Georgia, the Monteverde Conservation Lea- gue, and the Monteverde Institute extended support and access to land for data collection. Susan Bulova and Nicole Arcilla made valuable comments on the manuscript. This project was supported by a National Geographic/Waitt Foundation grant and Drexel University start-up funds. Research was conducted under permits from the Ministry of the Environment and Energy, Republic of Costa Rica (Scientiﬁc Passport numbers 0387 and 01667), and in accordance with the laws of the Republic of Costa Rica. Thanks to the Organization for Tropical Studies (OTS) for research support, including assistance in obtaining permits. Research followed Drexel University IACUC protocol 20046.

DATA AVAILABILITY

Data deposited in the Dryad Repository: https://doi.org/10. 5061/dryad.bb67v (O’Donnell 2017).

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