Thermoregulation in army ant bivouacs

ABSTRACT. The temporary nests (bivouacs), of Eciton burchelli (Westwood) thermoregulate with considerable precision. Temperatures at the core of the bivouac are maintained at 28.5±1C even though ambient temperatures in their tropical rainforest home change during the day over a range of 7C. Temperatures just under the mantle of the bivouac vary much more than at the core. Calculations suggest that the basal metabolic rate of the army ants in bivouac will generate all the heat that they need to keep warm when ambient temperatures drop. The army ants probably regulate heat loss by opening up ventilation channels within the nest.     

Birds and army ants in a fragment of the Atlantic Forest of Brazil

ABSTRACT Little is known about the birds associated with army‐ant swarms in the Brazilian Atlantic forest. Our objectives were to locate and monitor army‐ant swarms in the Atlantic rainforest of Brazil and to identify the species of birds that attended the swarms and exhibited bivouac‐checking behavior. From July 2004 to August 2005, we located 49 swarms of army ants, including 28 Eciton burchelli, 19 Labidus praedator, and 2 Eciton vagans swarms. No birds were present at 17 (35%) swarms. At 32 swarms where birds were present, 22 (69%) were E. burchelli swarms and 10 (31%) were L. praedator swarms. No birds were observed at the two E. vagans swarms. We identified 66 species of birds attending the swarms, but only 43 species were observed foraging on prey flushed by the ants. Eighteen of these species had not been previously reported to forage in association with army‐ant swarms. Most birds observed during our study attended army‐ant swarms opportunistically, with White‐shouldered Fire‐eyes (Pyriglena leucoptera) the only obligate ant follower. Our observations suggest that the arthropods and other organisms flushed by army ants represent an important food resource for several species of birds in the Atlantic forest ecosystem.     

The evolution of multiple mating in army ants

The evolution of mating systems in eusocial Hymenoptera is constrained because females mate only during a brief period early in life, whereas inseminated queens and their stored sperm may live for decades. Considerable research effort during recent years has firmly established that obligate multiple mating has evolved only a few times: in Apis honeybees, Vespula wasps, Pogonomyrmex harvester ants, Atta and Acromyrmex leaf-cutting ants, the ant Cataglyphis cursor, and in at least some army ants. Here we provide estimates of queen-mating frequency for New World Neivamyrmex and Old World Aenictus species, which, compared to other army ants, have relatively small colonies and little size polymorphism among workers. To provide the first overall comparative analysis of the evolution of army ant mating systems, we combine these new results with previous estimates for African Dorylus and New World Eciton army ants, which have very large colonies and considerable worker polymorphism. We show that queens of Neivamyrmex and Aenictus mate with the same high numbers of males (usually ca. 10-20) as do queens of army ant species with very large colony sizes. We infer that multiple queen mating is ancestral in army ants and has evolved over 100 million years ago as part of the army ant adaptive syndrome. A comparison of army ants and honeybees suggests that mating systems in these two distantly related groups may have been convergently shaped by strikingly similar selective pressures.     

Eight highly polymorphic microsatellite markers for the army ant Eciton burchellii

The army ant Eciton burchellii is a nomadic predator in the rain forests of Central and South America. Detailed work has documented many aspects of this species’ ecology, behaviour and life history. However, a detailed investigation into within colony relatedness structure requires the development of genetic tools. Here we present eight microsatellite markers with between nine and 25 alleles. For each loci there is close agreement between observed and expected heterozygosity.     

Six weeks in the life of a reproducing army ant colony: male parentage and colony behaviour

The army ant Eciton burchellii is one of the most conspicuous ant species in New World tropical forests, but studies of colony life histories have been hampered by the nomadic lifestyle of these ants, which alternate between a nomadic phase when the colony relocates frequently, and a statary phase when the colony remains at a fixed site. Here we report on a colony from Venezuela that we studied continuously for six weeks, from the time that the queen produced a reproductive brood until the adult reproductives emerged and the colony entered the next cycle. Our findings support the contention that reproductive larvae develop faster than worker larvae, and that the nomadic phases of colonies with reproductive broods are significantly shorter than those of colonies with worker broods. This strongly suggests that the onset of pupation is linked to the onset of the statary phase. We used microsatellite genotyping to accurately identify male and queen larvae and we describe how they can be distinguished morphologically. Using the same genetic markers, we determined the parentage of 81 males produced by this colony. Only one of the males had a genotype that could not be directly derived from the observed queen genotype, but this mismatch is most probably due to a single mutation at one of the microsatellite loci, rather than this male being a worker son. We therefore conclude that this colony provides no evidence that workers lay eggs that develop into adult males in the presence of the queen, confirming the results of an earlier study on male parentage in an Old World army ant. Received 16 November 2006; revised 15 January 2007; accepted 16 January 2007.     

Specializations of birds that attend army ant raids: An ecological approach to cognitive and behavioral studies

Tropical birds forage at army ant raids on several continents. Obligate foraging at army ant raids evolved several times in the Neotropical true antbird family (Thamnophilidae), and recent evidence suggests a diversity of bird species from other families specialize to varying degrees on army ant exploitation. Army ant raids offer access to high prey densities, but the ant colonies are mobile and widely spaced. Successful army ant exploitation requires solving a complex foraging problem because army ant raids are unpredictable in space and time. Birds can counteract the challenges posed by the ants by using strategies that raise their chances of detecting army ant raids, and birds can use additional strategies to track army ant colonies they have located. Some features of army ant biology, such as their conspicuous swarms and columns, above-ground activity, and regular cycles of behavior, provide opportunities for birds to increase their effectiveness at exploiting raids. Changes in sensory, cognitive and behavioral systems may all contribute to specialized army ant exploitation in a bird population. The combination of specializations that are employed may vary independently among bird species and populations. The degree of army ant exploitation by birds varies geographically with latitude and elevation, and with historical patterns such as centers of distribution of obligate thamnophilid antbirds. We predict the set of specializations a given bird population exhibits will depend on local ecology, as well as phylogenetic history. Comparative approaches that focus on these patterns may indicate ecological and evolutionary factors that have shaped the costs and benefits of this foraging strategy. The development of army ant exploitation in individual birds is poorly understood, and individual expression of these specializations may depend on a combination of genetic adaptation with cognitive plasticity, possibly including social and experiential learning. Future studies that measure developmental changes and quantify individual differences in army ant exploitation are needed to establish the mechanisms underlying this behavior.     

Early and dynamic colonization of Central America drives speciation in Neotropical army ants

The emergence of the Isthmus of Panama is one of the most important events in recent geological history, yet its timing and role in fundamental evolutionary processes remain controversial. While the formation of the isthmus was complete around 3 million years ago (Ma), recent studies have suggested prior intercontinental biotic exchange. In particular, the possibility of early intermittent land bridges facilitating colonization constitutes a potential mechanism for speciation and colonization before full closure of the isthmus. To test this hypothesis, we employed genomic methods to study the biogeography of the army ant genus Eciton, a group of keystone arthropod predators in Neotropical rainforests. Army ant colonies are unable to disperse across water and are therefore ideally suited to study the biogeographic impact of land bridge formation. Using a reduced representation genome sequencing approach, we show that all strictly Central American lineages of Eciton diverged from their respective South American sister lineage between 4 and 7 Ma, significantly prior to the complete closure of the isthmus. Furthermore, three of the lineage pairs form extensive and coincident secondary contact zones in Costa Rica and Nicaragua, with no evidence of gene flow. Such a discrete and repeated biogeographic pattern indicates at least two waves of army ant dispersal into Central America that were separated by significant genetic divergence times. Thus, by integrating phylogenomic, population genomic and geographic evidence, we show that early colonization of Central America across the emerging Isthmus of Panamá drove parallel speciation in Eciton army ants.     

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.     

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.     

Raiding and emigration dynamics in the ponerine army ant Leptogenys distinguenda (Hymenoptera, Formicidae)

Summary: Field and laboratory observations demonstrate that Leptogenys distinguenda is characterized by typical army ant behavior. Like in the "classical" army ants from the subfamilies Ecitoninae, Dorylinae and Aenictinae, raiding and emigration behavior are closely linked. The direction of raids can be altered in field experiments to a wide extent by offering ample food, suggesting it is highly influenced by the patchiness of prey. The sum of recruitments coming from one direction and the recruitment overrun are primarily responsible for the spatial development and the extension of raids. Emigration frequency can be suppressed by overfeeding a colony in the field. This result is interpreted as a secondary effect of reduced swarming activity, which gets suppressed as well in the same experiment. The discovery of a suitable nest site is considered the proximate stimulus for emigration, and the best explored areas are those that have been most thoroughly raided. As a result, emigrations are likely to lead into areas with high prey densities.     

Characterization of 12 new microsatellite loci in Aenictus and Neivamyrmex army ants

Here we describe 12 polymorphic microsatellite loci that were cloned and characterized for three species of army ants: the North American Neivamyrmex nigrescens, and the Asian Aenictus laeviceps and Aenictus dentatus. Observed and expected heterozygosities ranged from 0.37 to 0.97 (mean 0.70), and from 0.48 to 0.95 (mean 0.72), respectively. We observed 2–30 (mean 12) alleles per locus. These new genetic markers will be useful for studies of overall population structure and the complex pedigrees in colonies of army ants.     

Complex Nesting Behavior by Two Neotropical Species of the Ant Genus Stenamma (Hymenoptera: Formicidae)1

Two Neotropical ant species, Stenamma expolitum Smith and S. alas new species (described here), exhibit three unusual nesting behaviors: (1) they build architecturally sophisticated nest entrances that elevate the nest opening away from the surface; (2) they maintain multiple identical nests but occupy only one of them; and (3) they keep a round “door pebble” at the nest entrance, with which they plug the opening in response to army ants. Adaptive hypotheses for these behaviors are discussed, including the possibility that there are multiple lines of defense against army ant predation.     

Species‐level predation network uncovers high prey specificity in a Neotropical army ant community

Army ants are among the top arthropod predators and considered keystone species in tropical ecosystems. During daily mass raids with many thousand workers, army ants hunt live prey, likely exerting strong top‐down control on prey species. Many tropical sites exhibit a high army ant species diversity (>20 species), suggesting that sympatric species partition the available prey niches. However, whether and to what extent this is achieved has not been intensively studied yet. We therefore conducted a large‐scale diet survey of a community of surface‐raiding army ants at La Selva Biological Station in Costa Rica. We systematically collected 3,262 prey items from eleven army ant species (genera Eciton, Nomamyrmex and Neivamyrmex). Prey items were classified as ant prey or non‐ant prey. The prey nearly exclusively consisted of other ants (98%), and most booty was ant brood (87%). Using morphological characters and DNA barcoding, we identified a total of 1,103 ant prey specimens to the species level. One hundred twenty‐nine ant species were detected among the army ant prey, representing about 30% of the known local ant diversity. Using weighted bipartite network analyses, we show that prey specialization in army ants is unexpectedly high and prey niche overlap very small. Besides food niche differentiation, we uncovered a spatiotemporal niche differentiation in army ant raid activity. We discuss competition‐driven multidimensional niche differentiation and predator–prey arms races as possible mechanisms underlying prey specialization in army ants. By combining systematic prey sampling with species‐level prey identification and network analyses, our integrative approach can guide future research by portraying how predator–prey interactions in complex communities can be reliably studied, even in cases where morphological prey identification is infeasible.     

The structured diversity of specialized gut symbionts of the New World army ants

Symbiotic bacteria play important roles in the biology of their arthropod hosts. Yet the microbiota of many diverse and influential groups remain understudied, resulting in a paucity of information on the fidelities and histories of these associations. Motivated by prior findings from a smaller scale, 16S rRNA‐based study, we conducted a broad phylogenetic and geographic survey of microbial communities in the ecologically dominant New World army ants (Formicidae: Dorylinae). Amplicon sequencing of the 16S rRNA gene across 28 species spanning the five New World genera showed that the microbial communities of army ants consist of very few common and abundant bacterial species. The two most abundant microbes, referred to as Unclassified Firmicutes and Unclassified Entomoplasmatales, appear to be specialized army ant associates that dominate microbial communities in the gut lumen of three host genera, Eciton, Labidus and Nomamyrmex. Both are present in other army ant genera, including those from the Old World, suggesting that army ant symbioses date back to the Cretaceous. Extensive sequencing of bacterial protein‐coding genes revealed multiple strains of these symbionts coexisting within colonies, but seldom within the same individual ant. Bacterial strains formed multiple host species‐specific lineages on phylogenies, which often grouped strains from distant geographic locations. These patterns deviate from those seen in other social insects and raise intriguing questions about the influence of army ant colony swarm‐founding and within‐colony genetic diversity on strain coexistence, and the effects of hosting a diverse suite of symbiont strains on colony ecology.     

Differences in oxygen consumption and diel activity as adaptations related to microhabitat in Neotropical freshwater decapods (Crustacea)

This study evaluated oxygen consumption (MO₂) and diel activity in Aegla longirostri, Trichodactylus panoplus and Parastacus brasiliensis (three species of freshwater decapods that occur in sympatry), under two different conditions of O₂ availability, limited and constant; and searched for the existence of a relationship between these two variables. The Kruskal–Wallis test showed that in all the species, MO₂ was higher under constant O₂ availability; T. panoplus and P. brasiliensis showed an oxygen-dependent pattern, while A. longirostri showed higher MO₂ values and less variation in the values between the treatments, indicating a higher and more oxygen-independent metabolism. P. brasiliensis was more active in constant O₂. A. longirostri was more active in limited O₂ and did not show a clear diel activity in any case, showing behavioral changes when in unfavorable conditions. The Spearman's rank correlation analysis did not indicate any relationship between MO₂ and activity. These results indicate a higher metabolism in A. longirostri. The less demanding metabolisms of P. brasiliensis and T. panoplus allow these species to occupy environments that are unavailable to A. longirostri due to differences in dissolved-oxygen concentrations.     

Choice of nest site protects army ant colonies from environmental extremes in tropical montane forest

Unlike most social insects, Eciton burchellii army ants cannot thermoregulate through nest construction. Instead, army ants thermoregulate behaviorally by creating a living nest (bivouac), shifting its position and structure, and potentially through nest site selection. We hypothesized that bivouac site selection is critical to E. burchellii colony survival. We predicted elevation above sea level, with associated variation in local abiotic environments, would affect bivouac site selection by E. burchellii colonies. We also expected nest sites to buffer against ambient variation in abiotic conditions. We recorded bivouac site choice by E. burchellii colonies at sites ranging from lowland wet forests to montane forests and reviewed previously published data. We measured microclimatic variables associated with nest sites in high-elevation montane forests: temperature, relative humidity, and light levels. Bivouac site selection varied with elevation: as elevation increased, fewer bivouac sites were exposed, more were underground, and fewer were elevated (in trees). High-elevation bivouac sites moderated diurnal temperature variation and had higher relative humidity levels and lower light levels than ambient conditions. The buffering of ambient temperature and humidity decreased with elevation in montane forests, suggesting that abiotic extremes in bivouac sites at the highest elevations may contribute to the upper elevational range limits of E. burchellii.     

Dynamics of colony emigration in the ant Aphaenogaster senilis

In many social insect species, colonies frequently emigrate to a new nest. This requires the coordination of many individuals, and it puts the queen at risks of being lost or predated. We experimentally studied colony emigration in the ant Aphaenogaster senilis, who emigrates frequently and obligatorily reproduces by colony fission. As in other species, colony emigration was characterised by a synchronised relocation of workers. Foragers found the new nest site and triggered the relocation of the “inside” workers, which built up following a sigmoid curve. Unlike in Temnothorax, where workers are transported to the new nest, most individuals relocated by walking. The brood was transported around the middle of colony relocation, mostly by “inside” workers because they represent most of the workforce. The queen walked to the new nest at the middle of colony relocation, when the flow of ants to the new nest was maximal. Overall, this temporal dynamic of colony emigration is similar to that observed in other species. However, we argue that species-specific traits, such as whether workers are transported to the new nest or relocate by themselves, may affect parts of the process of colony emigration.