Diel Emigration and Foraging Behaviors of the Army Ant Eciton hamatum (Subfamily Ecitoninae)
As predators of many social insects and larger arthropods, army ants are a key component of tropical forest ecosystems. Specifically, their foraging behaviors and food preferences can affect forest invertebrate abundance and composition. To better understand army ant behavior, we observed foraging and movement patterns of Eciton hamatum for a continuous 20 hour period. We measured movement rates in and out of the bivouac and mapped changes in foraging column and bivouac locations. We also characterized substrate use by foraging columns. The number of columns and movement rates varied with foraging status (e.g. active foraging or zero foraging). E. hamatum moved only in dense columns (~4 ants wide), showing no swarm foraging behavior. E. hamatum workers foraged during the morning hours and only on larvae of social insects, including wasps, ants, and termites. From the evening into the night, the ants spent seven hours (1600-2300) emigrating from their old bivouac to their new bivouac approximately 90 meters away (column distance). Army ants were more commonly found traveling on branches than on leaves or bare soil. E. hamatum may have considerable effects on the reproductive success and colony structures of their primary prey sources (social insects).
Introduction
In many tropical and subtropical forests, army ants are important predators of social insects, large arthropods, and small vertebrates (1,2). They can influence tropical biodiversity by two mechanisms: (1) migrating army ant colonies can alter arthropod community composition and abundance, and (2) army ants can create niches for approximately 200 obligate and facultative associate species, including 50 neotropical bird species, phorid flies, parasitic beetles, and mites (3,4).
Recent genetic and fossil evidence suggest that the 298 ant species with ‘army ant adaptive syndrome’ (i.e. obligate social foraging, nomadism, and dichthadiigyne queens (blind queens with large gasters and ovaries)) evolved from a common subterranean ancestor in the subfamily Dorylinae (1,5). Only true army ants display all three characteristics of army ant adaptive syndrome, although some non-army ant species display two of the three. Many army ant genera have remained partially or completely subterranean, but some exhibit derived epigaeic (above-ground) foraging behaviors. Foraging strategies differ among lineages, ranging from swarm feeding to the specialized raiding of termite, ant, or wasp colonies in columns (6,7,8). Many species also exhibit diel and/or seasonal variation in prey selection, raid formations, and emigration cycles (9).
We studied the foraging and emigration behavior of Eciton hamatum (Subfamily Ecitoninae), a species of epigaeically and arboreally foraging army ant in the tropical moist forests of Corcovado, Costa Rica. We aimed to better understand the ecological roles of E. hamatum as arthropod predators by measuring the ant’s diel foraging behavior, movement patterns, and interactions with other species. We hypothesized that the colony would have periods of maximum biotic interaction (e.g. intense foraging) and minimum biotic interactions (e.g. retraction of all ant columns to the bivouac). Based on previous field observations of Eciton burchelli emigration at Corcovado on 3 February 2007, we predicted that maximum foraging would occur during daylight while bivouac emigration and rest would occur at night.
Methods
One army ant colony was observed continuously from 1045 on 4 February to 0630 on 5 February in Corcovado National Park, on the Osa Peninsula of Costa Rica. As soon as the colony was located on 4 February, the rates of movement of ants both in and out of the bivouac were recorded, and all columns leaving the bivouac were mapped. Natural history data (personal observations and notes about the surroundings and ant activity) were collected throughout the day and night.
Every half hour, five categories of ant movement rates (number of ants per minute in and out of the bivouac) were recorded. During periods of highly fluctuating movement (e.g. during bivouac dismantling and relocation), movement rates were recorded continuously. When the bivouac contained more than one column, the rates were recorded for each column. Ant movement rates were estimated by counting the number of ants crossing a designated point on the substrate in a ten second interval. Specifically, for each 10-second count, the number of ants moving into the bivouac, moving out of the bivouac, carrying larvae, and carrying larval prey were recorded. In all cases but those in which ant activity was changing at an interval of 10 seconds or less (high activity fluctuation), movement rates for each of the four movement types were recorded for five replicate 10-second sampling intervals per half-hour time period. In times of high activity fluctuation, rate samples were not replicated because ant movement changed rapidly between replicates. The only prey items the ants were observed to carry were larvae of other social insects (i.e. wasps, termites, and ants), which could be differentiated from their own larvae based on size and direction of movement (i.e. ants moved prey into the bivouac, while they only moved their own larvae out of the bivouac).
Bivouac emigration occurred from 1600-2300 on 4 February 2007. The columns of the colony were mapped every 2.5 hours during the study, except during bivouac dormancy from 2215 on 4 February to 0345 on 5 February. The lengths of all ant columns (main foraging columns plus side branches) were measured. For each distinct column segment, four items were recorded: the substrate type (i.e. sticks/twigs, bare soil, or leaves), the total number of ants carrying food sources, the number of ant body-bridges, and the length of the column segment. For each of the six replicate mapping periods, the proportion of each substrate type used was measured, summing across all columns and column branches sampled. A bridge was noted any time one or more ants served as a connector between two objects on the path; army ants link together to form these bridges, which expedite movement by other individuals in the colony.
To characterize the diel patterns of ant movements into and out of the bivouacs, average movement rates (with and without larvae, in and out of the nest) were plotted over the entire 20-hour period (averages of five replicate 10-second counts per movement type in each 30-minute time interval and single rates from periods of rapid change in movement rates). To calculate the rate of ants moving into the new bivouac, data from the ants moving out of the old bivouac were shifted forward three hours, the lag time between departure from old bivouac and arrival at new bivouac. Here it was assumed that all ant velocities were equal to the velocities of the final departing ants (used for lag time calculations). The mean percent of total column length of different substrate types used by the ants was compared with a one-way ANOVA (n = 6 mappings of the entire colony).
Results
Diel Patterns
During the 20-hour observation period, the army ants were observed both foraging and moving their bivouac. When we found the army ant colony at 1045 on 4 February 2007, they had an established bivouac and three foraging columns. At 1300, the ants from the foraging columns began to return to the nest, and at 1600, activity of one column greatly increased (Fig. 1): at this point, the ants began to carry their larvae towards the new bivouac along this column (Fig. 2). A new bivouac was discovered at the end of this column, and, as the movement of larvae towards the new bivouac increased, the number of foraging ants returning with prey items to the old bivouac decreased (Fig. 2). All other columns disappeared by the time activity in the column moving towards the new bivouac increased greatly (Fig. 3). There was a time lag of approximately three hours between complete desertion of the old bivouac (1937 hours) and arrival of the entire column of ants at the new bivouac (2216 hours; see Fig. 1). After the new bivouac was established, activity ended for approximately 5.5 hours until 0345 on 5 February, when the ants established three new foraging columns (Fig. 1).
Foraging Columns
Throughout the six replicate mapping periods, a total of 1159 meters of ant columns on three different substrates were surveyed. The ants did not use substrate types equally (ANOVA, F(2,15) = 17.00, P =0.0001, Fig. 4). Throughout the entire 20-hour sampling period, branches and twigs comprised 65% of total column length, leaf litter comprised 32%, and bare soil comprised 3% (mean values).
Early morning ant foraging activity was much lower than ant activity during bivouac emigration (Fig. 1). The maximum number of columns (13) was recorded when foraging recommenced at the new bivouac (Fig. 2). These columns extended as far as 200 meters away from the bivouac and typically ended with raids of arboreal insect nests (Fig. 3).
Calculations showed that the longest foraging columns would require a three-hour round trip from the bivouac to their prey location (0.0025 hour/m x 400 meters of column). Finally, it was observed that E. hamatum would not consume live or dead adult arthropods placed in their foraging columns, and the ants would notice and collect prey larvae only if larvae were placed within seven centimeters or less of the foraging column.
Bivouac movement
Bivouac emigration took place over seven hours, followed by a 5.5 hour dormancy period after the entire colony had reached their final destination (Fig. 1). The ants moved their bivouac to a fallen log, 90 meters along a foraging column from the original bivouac location (71 meters absolute distance). Prior to bivouac emigration, this column had reached a length of 140 meters; it then retracted in the early afternoon before bivouac emigration. After soldier ants near the bivouac were observed to be erasing foraging paths using anally-transmitted pheromones, only a single column remained from the old bivouac to the new bivouac site (Fig. 2). Flanked by soldiers on the sides of the column, ants transported larvae in a narrow (3-4 cm wide) column through the forest floor at sunset. During the seven-hour emigration period (including preparation time), no foraging activity was observed. In total, the E. hamatum colony did not prey upon any insects in the trees or in the leaf litter for almost 12 hours, from 1600 on 4 February to 0345 on 5 February.
Discussion
Army ant foraging strategies and their subsequent ecological effects can vary both by species and by season (8). While approximately seven-week-long cycles of either bivouac dormancy or nomadism have been recorded in many army ant species (3), we found evidence for shorter diel behavioral cycles in E. hamatum. As predicted, peak foraging occurred in the early morning while bivouac movement occurred in the evening and early night. These diel foraging and movement patterns may reduce parasitism rates by diurnal phorid flies, the primary parasites of many army ant species. In addition to their direct lethal effects (i.e. fatal oviposition into head, thorax, or abdomen), some phorid flies elicit alarm pheromones from both sedentary and nomadic ants, which greatly decrease foraging and movement efficiency (10). Because E. hamatum bivouac emigration occurs in a single column, alarm pheromone release could devastate emigration. Additionally, larvae and the queen—the individuals directly linked to colony fitness—would be exposed to parasitism if the bivouac emigration occurred during the day. Experimental manipulations of phorid fly density during different foraging and emigration stages would help to isolate the effects of phorid flies on E. hamatum diel behavior patterns.
Foraging Columns
Army ants are obligate social foragers, requiring pheromones to maintain colony-scale efficiency. Without pheromone trails, ants that were experimentally displaced rarely found their way back to foraging columns, and often did not even return to the bivouac. Pheromones may also be necessary to recruit enough ants to overcome adult prey arthropods that defend their own colony’s larvae.
Army ants are also selective foragers, in contrast to more generalized swarming army ant species (e.g. Eciton burchellii), which entirely clear leaf litter of adult arthropods and even small lizards (2). The distinct foraging columns observed are likely to affect the terrestrial invertebrate community differently than mass foraging swarms characteristic of some other army ant species, such as the well-studied E. burchellii. Columnar foraging is extremely selective, as foragers ignore nearby food sources to raid large larval caches farther away. Therefore, instead of creating large changes in invertebrate community composition and abundance, E. hamatum reduces reproductive success of a few social invertebrate species.
Even though the forest floor we studied consisted mostly of leafy material (personal observations), E. hamatum foraging columns primarily moved on woody substrates (Fig. 4). Therefore, they are spatially removed from most of the terrestrial invertebrates that live only in the leaf litter, such as the prey harvested by swarming army ant species. Because E. hamatum forages in columns on woody substrates without flushing out leaf-litter arthropods, they do not create niches for ant-following birds which feed on flushed-out arthropods (3).
Bivouac Movement
Foraging and bivouac emigration periods occurred at different times of day, and the transition between the two was documented. Because foraging occurred in columns, retraction of the day’s raid was rapid, at a rate of up to two meters per minute. Immediately before the colony moved their bivouac, workers formed bridges with their bodies to span gaps in the leaf litter. In foraging columns, bridging behavior was only observed when movement rates were high. The occurrence of bridges in high-traffic columns suggests that bridging is important for efficiently transporting large numbers of ants across broken terrain. The army ant body-bridges observed were composed of as many as 90 bodies per bridge, and bridges sometimes occurred in densities greater than 10 per meter of column. All bivouac emigration was concentrated in a single four-centimeter-wide column with many ant body bridges. Therefore, larger colonies may spend a greater proportion of their time transporting their bivouac, which could cut into overall foraging time. Single column emigration may limit E. hamatum colony size. Further research should investigate emigration patterns of different colony sizes and how this relates to the colony energy budget.
Ecological Impacts
Army ants can influence tropical forest biological diversity through two mechanisms: predation leading to changes in arthropod community composition and abundance (3,11) and facilitation of obligate and facultative associates (4). In addition, the selective larval predation exhibited by E. hamatum may impact life history strategies in their arboreal social insect prey. When an E. hamatum worker successfully communicates the location of a potential food source to the rest of the colony, forager recruits proceed to remove larvae from that source until it is depleted. Therefore, column army ant predation may select small, well-hidden colonies as its prey (e.g. wasps), while having little effect on litter-dwelling arthropods. Thus, column-foraging species of army ants may have concentrated, species-specific effects on invertebrate communities. In contrast, a mass swarming foraging strategy might create changes in invertebrate communities that affect more invertebrate individuals and species, which can subsequently influence invertebrate competition and diversity in tropical ecosystems (3).
Compared to swarming foragers such as E. burchelli, the intensity of E. hamatum foraging is mitigated by both its propensity for selective foraging as well as the time required for bivouac emigration in columns. However, the effects of E. hamatum on its individual prey species are still likely very strong, removing all or the majority of larvae from a given nest (personal observation). Social insects, such as those targeted by E. hamatum, are ecologically important species that make up a large portion of forest biomass and perform essential ecosystem functions (12). By decimating colonies of these ecologically important insects, E. hamatum fits the similar characterization of E. burchelli as a keystone species.
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All authors contributed equally to this manuscript.