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

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 facilitating 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 corresponds to the amount of food the birds kleptoparasitize from ant raids, and the heavier Pacific‐slope bird‐flocks could have greater negative kleptoparasitic impacts.     

Elevational and geographic variation in army ant swarm raid rates

Geographic and elevational variation in the local abundance of swarm-raiding army ants has implications for the population dynamics of their prey, as well as affecting the profitability of army-ant-following behavior for birds. Here, we analyze systematically collected data on E. burchellii and L. praedator raid rates from geographically and elevationally wide-ranging sites, from lowland to montane forests. We show that raids of each species, and of both species pooled, reach peak densities at intermediate (premontane) elevations. These patterns suggest that army ant swarm raids are relatively abundant in Neotropical montane forests. Therefore, a paucity of ant raids does not explain the absence of obligate ant-following bird species, particularly true antbirds (Thamnophilidae), from montane forests. As army ant raids are relatively common at middle elevations, opportunities exist for other montane bird taxa to exploit army ant raids as a food source.     

Ant‐following and the prevalence of blood parasites in birds of African rainforests

Blood parasites are widespread in birds, several are pathogenic and may affect the fitness of their hosts, and their evolution. By reanalyzing recently published data I show that parts of the variation in prevalences of parasites in the blood of African rainforest birds and the occurrence of similar or same parasite haplotypes in rather unrelated birds are well understood when considering the ecological aspects of foraging of some of these birds. Specialized ant‐following birds, which regularly follow the massive swarm raids of army ants and feed on insects flushed by the ants, have higher prevalences of nematode microfilariae (~10×), Trypanosoma (~10×), and Plasmodium parasites (~2×) and a much higher probability of infection with multiple parasites than other birds. Moreover, birds regularly attending army ant swarms share identical Trypanosoma haplotypes and show genetically similar microfilariae haplotypes. I conclude that ant‐following increases the probability of birds to get infected with blood parasites and may facilitate the switch of a parasite species from one host species to another. The costs of higher parasite intensities involved when specializing on following ant swarms may have influenced the evolution of foraging behaviour in birds of African rainforests and may help to explain the relatively low number of specialized ant‐following bird species on the African continent.     

Microclimatic factors associated with elevational changes in army ant density in tropical montane forest

Abstract.  1. The density (rate of encountering foraging raids) and species richness of army ants (Formicidae: Ecitoninae, and behaviourally convergent Ponerinae) was measured in montane tropical forest. Above-ground and subterranean army ant raids were sampled using standard protocols at four sites across an elevational gradient (1200–1650 m above mean sea level) in and near cloud forest in the area of Monteverde, Costa Rica.
2. Mean ambient temperature differed among sites, and decreased with elevation. For the above-ground foraging army ant species, raid rates also declined with elevation. Surface army ant raid rates, however, were not affected by day to day weather variation within sites (temperature, cloud cover, or precipitation).
3. For the underground foraging army ant species, raid rates did not vary directionally with elevation, and subterranean raid rates were not affected by day to day weather variation within sites.
4. Army ant species richness was not directionally related to elevation, and species sharing among sites was generally high.
5. Army ant community structure changes with elevation in Neotropical montane forest, and the results suggest that the strongest effects are of temperature regimes on the density of raids. These findings provide a baseline against which to detect changes in army ant communities that may accompany directional climate change in tropical cloud forests.     

Species and site differences in Neotropical army ant emigration behaviour

Abstract 1. Along with large wingless queens and group foraging raids, periodic colony movements or emigrations are a defining feature of army ant behaviour. Emigrations are important because they regulate spacing among colonies, and provide access to new foraging sites. 2. Raid and emigration activity of army ant communities was measured at four Neotropical sites using a standardised sampling protocol. Sampling of emigration activity was carried out throughout the diel cycle. 3. Both raid and emigration activity occurred throughout the day and night. Emigration activity was highest under cover of darkness, but sites and species differed in the diel timing of emigrations. These site and species differences have implications for the evolution of emigration behaviour, as well as for the community ecology of army ants.     

How much do army ants eat? On the prey intake of a neotropical top-predator

New World army ants (Ecitoninae) are nomadic group-predators that are widely thought to have a substantial impact on their prey. Nevertheless, quantitative data on prey intake by army ants is scarce and mostly limited to chance encounters. Here, I quantify the prey intake of the army ant Eciton hamatum at the contrasting scales of raid, colony (sum of simultaneous raids), and population. Like most army ants, E. hamatum conducts narrow ‘column raids’ and has a specialized diet of ant prey. I show that individual raids often had periods of no prey intake, and raid intake rates, calculated in g/min, differed significantly among colonies. Moreover, neither mean nor peak raid intake rates were correlated with colony size. Similarly, colony intake rates differed significantly among colonies, and mean colony intake rates were not correlated with colony size. However, mean colony intake rates were significantly higher than mean raid intake rates, and peak colony intake rate was correlated with colony size. Having multiple raids thus improves colony-level intake rates, and larger colonies can harvest more prey per unit time. Mean colony intake rate across colonies was 0.067 g/min dry weight and mean daily colony intake was calculated at 38.2 g. This intake is comparable to that of Eciton burchellii, which has a more generalized diet and conducts spectacular ‘swarm raids’ that are seen as having a greater impact on prey than column raids. Population size on Barro Colorado Island, Panama, was estimated to be 57 colonies, which extrapolates to a daily population intake of nearly 2 kg of prey dry weight, or 120 g/km². Broadly, these findings demonstrate that column raiding army ants experience considerable variation in prey intake for individual raids, but can still achieve notable impact at the larger scales of colony and population. Furthermore, they challenge the idea that swarm-raiding species necessarily have greater intake and thus impact on prey. Instead, I suggest that conducting multiple column raids may be a strategy that allows for comparable intake from a more specialized diet.     

Army ants in four forests: geographic variation in raid rates and species composition

1. The New World army ants are top predators in the litter of tropical forest, but no comprehensive studies exist on variation in assemblage-wide activity and species composition. We used standardized protocols to estimate foraging raid rates and species composition of army ant communities in four Neotropical forests. The study sites spanned approximately 10 degrees latitude, with two sites each in Central and South America. 2. We recorded a total of 22 species of army ants. The four sites varied in observed and estimated species richness. Species overlap was highest between the Central American sites, and lowest between the South American sites. 3. Raid activity varied significantly among sites. Raid activity per kilometre of trail walks was over four times higher at the most active site (Sta. Maria, Venezuela) than at the least active site (Barro Colorado Island, Panama). Furthermore, each site showed a different diel pattern of activity. For example, raid activity was higher during daylight hours in Costa Rica, and higher at night in Venezuela. Raid activity relationships with ambient temperature also varied significantly among sites. 4. The overall rate of army ant raids passing through 1 m(2) plots was 0.73 raids per day, but varied among sites, from 0 raids per day (Panama) to 1.2 raids per day (Venezuela). 5. Primarily subterranean species were significantly more abundant in Venezuela, and above-ground foragers that form large swarm fronts were least abundant in Panama. The site heterogeneity in species abundance and diel activity patterns has implications for army ant symbionts, including ant-following birds, and for the animals hunted by these top predators.     

Spatial Variation in Army Ant Swarm Raiding and its Potential Effect on Biodiversity

Invertebrate communities of the tropical rain forest floor are highly diverse, characterized by patchy species distribution patterns and high variation in species density. Spatial variation in the foraging activity of swarm raiding army ants, prime invertebrate predators in tropical rain forests, is discussed as a mechanism contributing to these patterns, but highly resolved long‐term data on army ant raiding on the local and landscape scale are hitherto lacking. In this study, 196 positions in 11 study sites in a tropical rain forest in western Kenya were continuously monitored over ~4 mo for the occurrence of swarm raids of army ants. Using population simulation analyses, the consequences of army ant raiding for prey communities were assessed. We found an unexpectedly high variation in raid rates at the study site and landscape scale. The weekly chance of communities to become raided by army ants was on average 0.11, but ranged from 0 to 0.50 among the 196 positions. Simulating population developments of two Lotka–Volterra species—showing slight trade‐offs between competitive strength and resistance to army ant raids—in the real raiding landscapes showed that the observed spatial variation in raid rates may produce high prey diversity at larger spatial scales (due to high β‐diversity) and strong variation in species density. Our results indicate that high spatial variation in army ant swarm raiding is a mechanism capable of generating patchy species distribution patterns and maintaining the high biodiversity of invertebrate communities of the tropical rain forest floor.     

The blind leading the blind in army ant raid patterns: Testing a model of self-organization (Hymenoptera: Formicidae)

We present field experiments and analyses that test both the assumptions and the predictions of a model that showed how the swarm raids of the army ant Eciton burchellimight be self-organizing, i.e., based on hundreds of thousands of interactions among the foraging workers rather than a central administration or hierarchical control. We use circular mill experiments to show that the running velocity of the ants is a sigmoidal function of the strength of their trail pheromones and provide evidence that the swarm raid is structured by the interaction between outbound and inbound forager traffic mediated by the pheromones produced by both of these sets of ants. Inbound traffic is also affected by the distribution of prey, and hence, sites of prey capture alter the geometry of the raid. By manipulating the prey distributions for E. burchelliswarms, we have made them raid in a form more typical of other army ant species. Such self-organization of raids based on an interaction between the ants and their environment has profound consequences for interpretations of the evolution of army ant species.     

Influence of driver ant swarm raids on earthworm prey densities in the Mount Kenya forest: implications for prey population dynamics and colony migrations

African driver ants are nomadic social mesopredators feeding on a highly diverse array of prey species at different trophic levels. Colonies of certain driver ant species have a biomass which can equal that of medium-sized mammalian carnivores and the ultimate cause of their nomadic life-style is thought to be local prey depletion. The impact of driver ant swarm raids is therefore expected to be strong but the degree to which they reduce prey populations has not been quantified and it is unknown whether these spectacular predators exert significant top-down effects. We examined the combined effect of driver ant (Dorylus molestus) and swarm-attending bird (Alethe poliocephala) predation on the population dynamics of earthworms, which constitute the ants’ main prey type in the montane forest of Mount Kenya. Pre-raid earthworm biomass densities in the soil layer down to a depth of 8 cm varied by a factor of 31. The immediate effect of swarm raids was a reduction in earthworm numbers in this layer, but 8 days later earthworm numbers had recovered to pre-raid levels. When earthworm biomass densities were compared, no significant effect of swarm raids was detected. The estimated proportion of earthworm prey biomass extracted from 0 to 8 cm layer by driver ants and birds together was about 2.2%. Although colony distribution was overdispersed as expected based on knowledge of D. molestus migratory behaviour, predation events were highly localized. Predation frequency was low (once every 62 days on average) and highly variable. These results indicate that earthworm prey is highly abundant but at the same time so difficult to harvest that swarm raids exert only a marginal influence on earthworm populations. Longer-term studies would be required to determine whether earthworm populations are limited by swarm raids. The small impacts of individual raids and rapid recovery of earthworm prey populations likely underlie the low frequency of migrations and short distances travelled by migrating colonies of D. molestus.     

Spatial movement optimization in Amazonian <Emphasis Type="Italic">Eciton burchellii</Emphasis> army ants

Foraging army ants face a problem general to many animals—how best to confront resource depletion and environmental heterogeneity. Army ants have presumably evolved a nomadic lifestyle as a way to minimize re-exploitation of previously foraged areas. However, this solution creates a challenge for an army ant colony: foraging by this colony and others creates a shifting landscape of food resources, where colonies should theoretically avoid their own previous foraging paths as well as those of other colonies. Here, we examine how colonies exploit this resource mosaic, using some of the optimality arguments first proposed and tested by Franks and Fletcher (1983), but with much larger data sets in a new location in SW Amazonia. Our data supported Franks and Fletcher’s (1983) model for systematic avoidance of raided areas during the statary phase, as well as a hypothesis of distance optimization between successive statary bivouacs. We also test and find significant evidence that foraging raids turn in opposite directions from the previous day’s directional angles more frequently than what would be expected if turning angles were distributed at random, which acts to move a colony away from recently exploited areas. This implies that colonies follow a straighter line path during the nomadic phase as opposed to a curved one, which acts to maximize distance between statary bivouacs. In addition to intra-colony movement optimization, we examine evidence for inter-colony avoidance from more than 330 colony emigrations and suggest that colony-specific pheromones are not necessarily repulsive to other colonies. Lastly, we compare our results with those of similar studies carried out at Barro Colorado Island (BCI), Panama. Despite a higher density of army ants in the SW Amazon region, colonies spend less time emigrating than their counterparts at BCI, which suggests a higher prey density in SW Amazonia.     

The Influence of Ants on the Foraging Behavior of Birds in an Agroforest1

Ants limit bird foraging success via interference or exploitative competition. We compared bird foraging (number and duration of visits, bird species visiting) on ant (Azteca instabilis)‐infested and ant‐free tropical trees (Inga micheliana and Alchornea latifolia). Ants did not affect the number of bird visits or the number of species visiting. Ant presence shortened visit duration (overall and for insectivores) only on A. latifolia where ant activity was higher. Ants may thus hinder bird foraging on some tropical trees potentially shaping how predators affect arthropod communities; yet ant effects depend on bird foraging guild and ant activity.     

Effect of trail pheromones and weather on the moving behaviour of the army ant <Emphasis Type="Italic">Eciton burchellii</Emphasis>

Most of what we know about the moving behaviour of the nomadic army ant Eciton burchellii comes from Barro Colorado Island (BCI) in Panama. Nomadic colonies raid roughly in straight line during the day and relocate their nests along this path in the evening. At BCI, nomadic colonies raid roughly in the same compass bearing of the previous day, presumably using their pheromone-marked raiding trails as cues to pick directions. Deviations from this direction occur when a nomadic colony fails to move, possibly due to environmental conditions. The generality of these results has been questioned. We studied nomadic colonies of E. burchellii at La Selva Biological Station, Costa Rica to evaluate the generality of the results obtained from BCI. We measured the angle between consecutive raids, manipulated the distribution of previous day’s raid pheromones around nests to evaluate the effect of raid pheromone on foraging direction, and evaluated the effect of rainfall on the probability of moving and on deviation from the previous day’s raid. Colonies did not follow the same compass bearing of the previous day and formed new raids on areas with previous day’s raid pheromones or without them. Rainfall can explain when nomadic colonies move, but did not explain deviation from the previous day’s raid direction. Our results suggest that caution should be taken when generalizing the insightful results obtained from the BCI population.     

Optimization, conflict, and nonoverlapping foraging ranges in ants

An organism's foraging range depends on the behavior of neighbors, the dynamics of resources, and the availability of information. We use a well-studied population of the red harvester ant Pogonomyrmex barbatus to develop and independently parameterize models that include these three factors. The models solve for an allocation of foraging ants in the area around the nest in response to other colonies. We compare formulations that optimize at the colony or individual level and those that do or do not include costs of conflict. Model predictions were compared with data collected on ant time budgets and ant density. The strategy that optimizes at the colony level but neglects costs of conflict predicts unrealistic levels of overlap. In contrast, the strategy that optimizes at the individual level predicts realistic foraging ranges with or without inclusion of conflict costs. Both the individual model and the colony model that includes conflict costs show good quantitative agreement with data. Thus, an optimal foraging response to a combination of exploitation and interference competition can largely explain how individual foraging behavior creates the foraging range of a colony. Deviations between model predictions and data indicate that colonies might allocate a larger than optimal number of foragers to areas near boundaries between foraging ranges.     

The foraging ecology of the army ant Eciton rapax: an ergonomic enigma?

Abstract. 1. The army ant Eciton rapax (F. Smith) produces longer raid systems than any other member of its genus and it is a specialist predator of forest floor and understory ants such as species of Camponotus, Odontomachus and Pachycondyla.
2. Allometrical analysis confirms that E. rapax is the only member of its genus without distinct physical castes among its workers: its foraging population is entirely monomorphic and there are no majors.
3. The workers of E. rapax are distributed over a considerable size range, and there are distinct divisions of labour within these colonies: small workers tend to stay in the nests and among the larger foraging workers those retrieving prey items are significantly bigger than the rest.
4. An analysis of foraging efficiency and worker performance in E. rapax suggests that transport costs, resulting from the great distances that workers travel during raids and emigrations, are one of the selection pressures that have favoured the evolution of large monomorphic workers in this species.     

Serial monodomy in ants: an antipredator strategy?

Abstract.  1. The term serial monodomy is used to describe a life-history phenomenon in social insects. Serially monodomous colonies maintain multiple nests for their exclusive use, but only occupy one nest at a time.
2. The hypothesis that colony odours mediate nest relocation decisions was tested in the serially monodomous species Aphaenogaster araneoides from Central America. Odour extracts of colony members were created using a non-polar solvent.
3. Colonies strongly avoided reoccupying nests treated with colony odour extracts, while control colonies often returned to nests subjected to solvent-only control. Behavioural observations indicated that A. araneoides colonies are capable of detecting army ant ( Eciton burchellii ) raids up to 1.4 m from the raiding front, with several seconds to evacuate nests.
4. It is proposed that the function of serial monodomy in A. araneoides is the reduction of nest odour to enhance detection of predaceous army ants. Serial monodomy may be a widespread but undocumented mode of nesting where army ants occur in tropical and subtropical climates.     

Combat between large derived societies: A subterranean army ant established as a predator of mature leaf-cutting ant colonies

Summary. Mature colonies of Atta leaf-cutting ants are dominant herbivores throughout the Neotropics. Although young colonies have natural enemies, mature colonies, which live in extensive nests containing millions of workers, currently have no recognised predators. New World army ants (Ecitoninae) are specialist social predators of other ants, and the army ant Nomamyrmex esenbeckii, a primarily subterranean species, is known to prey upon young Atta colonies. Here we present the results of the first long-term study of the predator-prey interaction between N. esenbeckii and Atta. Our study establishes the army ant N. esenbeckii as the only known predator capable of successfully attacking and killing mature as well as young colonies of Atta leaf-cutting ants. In natural raids, and experimental tests, Atta rapidly recruited their largest workers (majors) as a specific defensive response to N. esenbeckii raiders and both taxa used their largest individuals in the frontline of battles. The deployment and behaviour of these large workers demonstrates a size-related division of labour and agrees with the predictions of Lanchesters Linear Law of Combat. Both taxa also used cooperative combat teams to overwhelm large combatants from the other side. The success of N. esenbeckii raids varied greatly, such that they were prevented from entering Atta nests in the least successful raids, and completely overran Atta colonies in the most successful raids. The speed and magnitude of the defensive response of mature Atta colonies was key in determining the level of success of N. esenbeckii raids.Received 12 December 2003; revised 25 March 2004; accepted 1 April 2004.Work conducted at the Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Ancon, Republic of Panama     

An energetic correlate between colony size and foraging effort in seabirds, an example of the Adélie penguin Pygoscelis adeliae

Central-place foraging seabirds alter the availability of their prey around colonies, forming a "halo" of reduced prey access that ultimately constrains population size. This has been indicated indirectly by an inverse correlation between colony size and reproductive success, numbers of conspecifics at other colonies within foraging range, foraging effort (i.e. trip duration), diet quality and colony growth rate. Although ultimately mediated by density dependence relative to food through intraspecific exploitative or interference competition, the proximate mechanism involved has yet to be elucidated. Herein, we show that Adélie penguin Pygoscelis adeliae colony size positively correlates to foraging trip duration and metabolic rate, that the metabolic rate while foraging may be approaching an energetic ceiling for birds at the largest colonies, and that total energy expended increases with trip duration although uncompensated by increased mass gain. We propose that a competition-induced reduction in prey availability results in higher energy expenditure for birds foraging in the halo around large colonies, and that to escape the halo a bird must increase its foraging distance. Ultimately, the total energetic cost of a trip determines the maximum successful trip distance, as on longer trips food acquired is used more for self maintenance than for chick provisioning. When the net cost of foraging trips becomes too high, with chicks receiving insufficient food, chick survival suffers and subsequent colony growth is limited. Though the existence of energetic studies of the same species at multiple colonies is rare, because foraging metabolic rate increases with colony size in at least two other seabird species, we suggest that an energetic constraint to colony size may generally apply to other seabirds.     

Microsatellite analysis reveals strong but differential impact of a social parasite on its two host species

The speed and the dynamics of the co-evolutionary process strongly depend on the relative strengths of reciprocal selection pressures exerted by the interacting species. Here, we investigate the influence of an obligate social parasite, the slave-making ant Harpagoxenus sublaevis, on populations of the two main host species Leptothorax acervorum and Leptothorax muscorum from a German ant community. A combination of genetic and demographic data allowed us to analyse the consequences of raiding pressure on the hosts' life history and possible host preferences of the parasite. We can demonstrate that slave raids during which the social parasite pillages brood from neighbouring host colonies are both frequent and extremely destructive for both host species. Microsatellite analysis showed that, on average, a single slave-maker colony conducts more than three raids per year and that host colonies mostly perish in the aftermath of these parasite attacks. Only in few cases, surviving nests of previously raided host colonies were found in the surroundings of slave-maker colonies. As a consequence of the high prevalence of parasites and their recurrent and devastating slave raids on host colonies, the life expectancy of host colonies was severely reduced. Combining our results on host-specific parasitic colony founding and raiding frequencies with the post-raid survival rate, we can demonstrate an overall higher mortality rate for the smaller host species L. muscorum. This might be caused by a preference of H. sublaevis for this secondary host species as demographic data on host species usage indicate.     

Temporal and spatial patterns in the emigrations of the army ant Dorylus (Anomma) molestus in the montane forest of Mt Kenya

Abstract.  1. The emigration behaviour of the army ant Dorylus ( Anomma ) molestus was studied in the montane forest of Mt Kenya. This species forages by massive swarm raids (mean width 10.3 m ± 4.6 m SD), which are assumed to have a strong negative impact on the densities of prey populations.
2. For non-reproductive colonies the stay duration in a nest is highly variable (median 17, range 3–111 days). This suggests that the frequency of emigrations is not dictated by a brood cycle as an underlying endogenous pattern generator.
3. Colony density is high (mean nearest neighbour's distance 82.1 m ± 29.4 m SD) and mean foraging range is 75.0 m, so encounters with neighbouring colonies occur frequently.
4. The straight line emigration distance is on average 92.7 m (± 29.7 SD). The emigration direction is random with respect to absolute bearing and also relative to the direction of the previous emigration. However, the emigration direction is influenced by the location of the nearest neighbour. Colonies typically emigrate directly away from their nearest neighbour.
5. Local food depletion is likely to be the ultimate cause for emigrations in this species, because emigration distance is larger than foraging range and colonies move away from their nearest neighbour. A small percentage of emigrations may be triggered by pangolin attacks on nests.
6. Contrary to the prediction of a recently developed mathematical model for epigaeic swarm-raiding Dorylus ( Anomma ) species, D.  ( A .)  molestus colonies do not engage in intraspecific battles. Possible reasons for the absence of fights between colonies despite apparently fierce intraspecific competition are discussed.