Resource partitioning in army communities

Maria S. Calvi ’00, Megan K. Jennings ’00, Michael D. Foote ’01 and Laura R. Nagy G

Abstract Community theory predicts that resources should be partitioned to minimize interspecific competi- tion. We tested for niche partitioning in the community of that forage in association with the continually moving swarms of foraging army . These birds follow the swarming front of army ants and feed on the fleeing that are flushed out as they try to escape the swarm. Ant bird species were non-randomly distributed in their horizontal perching positions relative to the ant swarm. Foraging height and foraging substrate were also significantly different among species. The number of successful foraging bouts averaged about 1.6 prey items • bird– 1 • 15 min– 1 for all species, indicating all species in the community accrue comparable benefits from their association with army ants. Other communities that also depend on mobile resources (e.g., bird communities of frugivorous altitudinal migrants that track seasonally fruiting trees) rely on niche partitioning to solve similar challenges in spite of the dynamic spatial structure of their resource base.

INTRODUCTION single ant swarm are potentially competing for the same resources. Community theory there- Species often compete for space and fore predicts that this resource base should be parti- resources in natural communities. To minimize com- tioned. Coates-Estrada (1989) suggested that the bird petition, coexisting species that utilize similar species associated with army ants tend to partition resources may partition these resources in space or space with respect to the position of the moving front time to reduce niche overlap. This partitioned of the foraging ant swarm. We hypothesized that the resource base tends to be relatively fixed in space. bird community associated with army ants has parti- However, birds that follow army ant swarms are an tioned the resource base by utilizing different hori- exception. These birds exploit the chaos induced by zontal and vertical foraging positions relative to the army ant foraging to feed upon fleeing . moving swarm of army ants. If ant bird assemblages Army ants, which are primarily carnivorous, use their are structured communities rather than random aggre- large numbers and thorough scouring of an area to gations, it also follows that the bird species most often overtake prey which may be larger than the individ- found with ant swarms would tend to have the high- ual ants. They are reported to have an extremely fast est foraging success and occupy the best foraging recruiting system, making it even easier for them to positions within the community. swamp prey as they are found (Rettenmeyer, 1983). Because the location of the foraging ants constantly METHODS changes, the related bird community must also move if they are to maintain an organized spatial structure. We located a colony of the army ant The multiple bird species that forage over a burchelli that was foraging between the Ollas and Espaveles trails at the La Sirena biological station in Corcovado, Costa Rica. An assemblage of birds was following the army ants. We studied this aggregation of birds on 4, 6, and 7 February 2000 from 15:20 to 16:00, 10:00 to 11:20 and 12:30 to 17:20, and 08:30 to 11:20, respectively. At 15 min intervals during our observations, we mapped the horizontal and vertical perching positions of every bird relative to the ant swarm. Birds were assigned to a horizontal perching position category of front, center, or periphery (Figure 1). We also esti- mated the height above ground of each bird at the time of our visual scan. The 15 min interval was cho- sen because it allowed enough time for the birds to relocate in order to retain the same position relative to the ants. Thus, this interval was sufficiently long to to test for differences among species in foraging sub- strate, number of successful foraging attempts per individual, and aggressive interactions between species. A one-way analysis of variance was used to test for differences among species in perching and foraging height.

RESULTS

On 6 February 2000, we located the bivouac of the ant swarm by following a narrow column (≈ 3 cm wide) of ants returning to the temporary shelter. The bivouac was within the hollow spaces of a decom- posing log. When the entire colony was present, we visually estimated that it filled ≈ 31 dm3. Ants were The barred , , is one of the species of birds which is frequently found removing pupal cases on the morning of 7 February, in the community of ant birds which occur in associa- indicating that this colony was nearing the end of a tion with army ant swarms. statatory reproductive phase, which is reported to last treat the scans as independent observations. 17 – 22 d for this species. On 7 February, the day on We also monitored the front and center of the which most of our data were collected, the first for- flock continuously for foraging events and agonistic aging column left the bivouac at 08:30. By 09:00, the interactions among birds, such as fights over prey ants had organized themselves into a foraging swarm items. For each successful foraging event, we record- that headed in a westerly direction from the bivouac. ed the species of bird, the height from which the for- By 09:45, the area occupied by foraging ants (Figure aging maneuver was initiated, the height and sub- 1) was ≈ 10 x 15 m, which remained relatively con- strate where the prey item was caught, and, if seen, stant (range = 7 x 15 m to 12 x 20 m) until we ceased the length of the prey item (relative to bill length). For observations at 11:15. The foraging swarm moved ≈ each agonistic behavior, we recorded the bird species 57 m from the bivouac site over 2:45 h. The rate of that were participating and where those interactions movement ranged from 1 - 7 m / 15 min. took place relative to the ant swarm in an attempt to We observed five species of ant birds forag- determine if one species held a more coveted posi- ing in association with the ant swarm. Of these, the tion over the swarm based on attacks on its position only species that is reported to be an obligate associ- or defense of its position. ate of army ants was the bicolored This ant colony utilized two distinct foraging (Gymnopithys leucaspis), which was also the most strategies. Primarily, ants foraged in a single swarm abundant species (up to 9 individuals). Other species ranging in size from 50 to 240 m2. However, on 6 – 7 were gray-headed tanagers (Eucometis penicillata; up February 2000 we also observed small groups of ants to 3 individuals), tawny-winged foraging in multiple, narrow columns rather than one ( anabatina; up to 2 individuals) and unified front. Analyses of foraging behavior used barred woodcreepers (Dendrocolaptes certhia; up to observations taken during both types of ant activity, 1 individual; Figure 2). On the morning of 7 February, but analyses of the mapped spatial positions of the the bicolored antbird was the first species to join the birds were restricted to the more common situation swarm. The tawny-winged woodcreeper, a banded where there was a single, foraging ant swarm (n = 23 individual that had been observed on previous days position maps collected on 4, 6, 7 February). with the same ant swarm arrived as the swarm began We used chi-square goodness-of-fit statistics to move in a unified front and was followed shortly Bicolored antbirdGray-headed tanagerTawny-winged woodcreeper Barred woodcreeper Front 25 (27.4) 10 (9.0) 7 (4.9) 2 (2.7) Center 29 (34.9) 11 (11.4) 9 (6.2) 7 (3.5) Periphery 47 (38.7) 12 (12.6) 2 (6.9) 1 (3.8)

Table 1. The number of bird observations at three horizontal positions in the ant swarm (based on the sum from 23 maps recorded at 15 min intervals). Parenthetical values indicate the expected frequen- cies if birds were randomly distributed with respect to species.

27 Bicolored antbirdsGray-headed tanagerTawny-winged woodcreeper Barred woodcreeper Ground 73 34 29 5 Other 12 00 Trunk 1 3 10 7 Sum 75 39 39 12 Bird observation units a 54 21 16 9 Expected b 89.1 34.65 26.4 14.85 Table 2. The number of successful foraging bouts by substrate (ground, trunk or other) for four bird species associated with an army ant swarm. a Average number of individual birds in front or center of swarm (see Fig. 1), which was the focal area for foraging events, multiplied by the number of 15 min observation periods (23). b Based on the null hypothesis that bird species did not differ in their foraging success (i.e., foraging events • bird-1 • 15 min-1 was the same) by the barred woodcreeper. Gray-headed tanagers tended to pass in and out of the swarm throughout the morning of 7 February, but were foraging contin- ually with the swarm for at least 1.5 h during the pre- vious afternoon. All four of these bird species were foraging on the invertebrates under attack by the army ants. One individual of the chestnut-backed antbird (Myrmeciza exsul), another species reported to regularly forage with army ants, was associated with our ant swarm for ≈ 15 min during our observa- tions. The chestnut-backed antbird, was not included in the analyses that follow as it was only present for one of the mapping intervals out of the 23 total. Eciton burchelli army ants fill this hollowed-out log Bird species were non-randomly distributed where they have temporarily created a bivouac during in their horizontal perching positions relative to the a reproductive period. ant swarm (Table 1; G = 15.82, P = 0.02). Bicolored higher than for the other species, especially bicolored were over-represented in the periphery of antbirds which engaged in far fewer aggressive inter- the swarm while tawny-winged and barred wood- actions than expected based on their abundance creepers were under-represented in the periphery. (Table 3; χ2 = 24.62, df = 1, p < 0.0001). All aggressive Tawny-winged woodcreepers tended to position interactions of the barred woodcreepers were with themselves in the front and center of the swarm while tawny-winged woodcreepers, but data were not the barred woodcreeper was usually in the center. included in the chi-square test because there was only Bicolored antbirds perched significantly lower to the one barred woodcreeper and three interactions. ground than tawny-winged and barred woodcreepers (Fig. 3; F3, 124 = 7.07, P = 0.0002). Direction of Foraging height and foraging substrate both swarm movement differed among species (F3, 168 = 189.84, P < 0.0001; G = 27.8, df = 3, P < 0.0001, respectively). Eighty-four Front percent of all foraging attempts were initiated from foraging heights < 0.5 m high. The barred wood- creeper foraged from a significantly higher starting Center point than the other three species (Fig. 4). Eighty- seven percent of all prey captures occurred on the Periphery ground. However, tawny-winged and barred wood- creepers were often foraging on trunks (Table 2). The number of successful foraging bouts averaged about Narrow trail (≈ 5 - 20 cm wide) 1.6 prey items • bird – 1 • 15 min – 1 and was not sig- connecting foraging swarm with bivouac site nificantly different among species (χ2 = 9.34, df = 6, p = 0.16). Aggressive interactions involving tawny- Figure 1. Possible bird locations relative to army ant swarms. winged woodcreepers averaged about 0.6 interac- Every 15 min during observation periods, we recorded which of tions • bird– 1 • 15 min– 1, which was significantly these three positions was occupied by each bird. Birds foraging in association with the ant swarm were assigned map locations. Bicolored antbirdGray-headed tanagerTawny-winged woodcreeper Barred woodcreeper Bicolored antbird 20 60 Gray-headed tanager 02 40 Tawny-winged woodcreeper 10 03 Sum 3 2 10 3 Expected a 8.1 3.15 2.4 1.35 Table 3. The number of observations of aggressive interactions among four bird species asso- ciated with an army ant swarm. Columns indicate one participant and rows indicate the other. a Based on the null hypothesis that species did not differ in their propensity for aggressive interactions (i.e., interactions • bird-1 • 15min-1 was the same). Bird observation units same as in Table 2. DISCUSSION length of the bird, so bird species that differ in bill size apparently differ in prey size selection. These results Various species within an ant bird communi- suggest that the birds have partitioned the resources ty appear to occupy different niches as defined by provided by army ants through differences in both their horizontal and vertical positions relative to the spatial distribution and prey selection. ant swarm. The central position of the swarm may be Although the position of the resources the most rewarding foraging location because the change rapidly with the movement of the army ant high density of ants in the center seems to flush out swarm, ant bird community structure is maintained. many insects, which are then exposed to the foraging Because all species are comparable competitors, we birds (Coates-Estrada, 1989). The tawny-winged and would predict that larger swarms would support a the barred woodcreepers most frequently occupied greater number of individuals in the same relative this preferred position. These two relatively large proportions. species may be actively excluding other individuals Resource bases that move in space are not from the center of the swarm; 74 % of conflicts unique to army ant communities. Other bird commu- involved woodcreepers interacting with bicolored antbirds and gray-headed tanagers (Table 3). Species 7 also partition space vertically through their use of dif- ferent perching heights (Figure 3). For example, bicol- 6 ored antbirds were primarily perched close to the ground while the woodcreepers perched higher in 5 the canopy. 4 Despite the vertical structuring of foraging height, all birds except the barred woodcreeper tend- 3 ed to capture prey items close to the ground. Because prey were usually located on or in the leaf litter, for- 2 aging on the ground may maximize the view of insects fleeing from the army ants and decrease the 1 traveling distance to capture prey. This strategy may be more energy efficient and effective in competing 0 with the ants and other birds for the same food resource. In contrast, barred woodcreepers apparent- ly prefer to forage from higher substrates. They utilize their climbing ability to capture prey that have moved up tree trunks, where they would be inacces- sible to bicolored antbirds and gray-headed tanagers. Although tawny-winged woodcreepers foraged on trunks as well, barred woodcreepers dominated the higher vertical positions, perhaps excluding the tawny-winged woodcreepers from these heights by virtue of their greater body size. Bird Species The similarity of prey capture rates for all Figure 2. Mean abundance (± SD) of four bir species suggests that direct competition does not limit species within a swarm of foraging ants at Corcovado National Park, Costa Rica. Data are foraging success in this community. The majority of based on 23 scans (15 min apart) conducted prey captures were approximately equal to the bill on 4, 6 - 7 Feb 2000.

29 nities, such as frugivorous altitudinal migrants, are If these communities resemble that of the antbirds, also challenged to continually readjust their position then they retain their structure of niche partitioning in response to the changing spatial patterns of fruiting even as they and their resources move. This parti- trees. Similarly, mobile resources are also common in tioning presumably allows them to harvest their other systems, such as piscivores feeding on mobile resource base more completely and efficiently than if schooling fish and large terrestrial predators that fol- the organization of the community were continually low migrating ungulate communities across savannas. disrupted by the movement of resources.

3 REFERENCES 2.5 Coates-Estrada, R. & Estrada, A. (1989). Avian attendance and for- 2 aging of army ant swarms in the tropical rain forest of Los Tuxtlas, Veracruz, Mexico. Journal of Tropical Ecology, 5, 281–292. 1.5 Rettenmeyer, C. W. (1983). Eciton burchelli and Other Army Ants. In D. H. Janzen (Ed.), Costa Rican natural history (pp. 716 – 1 718). Chicago, IL: University of Chicago Press.

0.5 ABOUT THE AUTHORS 0 Megan Jennings ’00 is an Environmental and Evolutionary Biology major, modified with Environmental Studies. She is from suburban Maryland and has enjoyed several opportuni- ties to travel over her four years at Dartmouth. She spent time doing field work in the tropics with the Nature Conservancy Figure 3. Perching height (± SE) of four bird on Maui, HI and on the Biology FSP in Costa species foraging within an army ant swarm Rica and Jamaica. Megan is pursuing a career (based on the average result from up to 23 in conservation biology and wildlife manage- scans, each of which was an average of all ment. birds present at the time). Mike Foote ’01 is a Biochemistry major. He is 4 from Chicago. He spent his fall off term on 3.5 Guegeegue, Marshall Islands teaching high 3 school, and went on the Costa Rica Bio FSP this winter. He works with a mentoring pro- 2.5 gram called DREAM and loves the outdoors. 2 Laura Nagy is a graduate student in Ecology 1.5 and Evolution working in the lab of Richard 1 Holmes. She was a biology major at Oberlin College and did her masters work at the 0.5 University of Arkansas. She left the U.S. Fish 0 and Wildlife Service to continue her educa- tion at Dartmouth.

Maria Calvi ’00 is an Ecology and Evolutionary Biology Major with a minor in Native American Studies. This is her second article in the DUJS. Figure 4. Average foraging height (± SE) of four bird species associated with an army ant swarm. Data describe the height of a bird directly before the maneuver that led to a successful prey capture (n = 12 - 79 observation / species).