Army Ant Eciton Burchellii Research Articles

Microbial symbionts are shared between ants and their associated beetles.

The transmission of microbial symbionts across animal species could strongly affect their biology and evolution, but our understanding of transmission patterns and dynamics is limited. Army ants (Formicidae: Dorylinae) and their hundreds of closely associated insect guest species (myrmecophiles) can provide unique insights into interspecific microbial symbiont sharing. Here, we compared the microbiota of workers and larvae of the army ant Eciton burchellii with those of 13 myrmecophile beetle species using 16S rRNA amplicon sequencing. We found that the previously characterized specialized bacterial symbionts of army ant workers were largely absent from ant larvae and myrmecophiles, whose microbial communities were usually dominated by Rickettsia, Wolbachia, Rickettsiella and/or Weissella. Strikingly, different species of myrmecophiles and ant larvae often shared identical 16S rRNA genotypes of these common bacteria. Protein-coding gene sequences confirmed the close relationship of Weissella strains colonizing army ant larvae, some workers and several myrmecophile species. Unexpectedly, these strains were also similar to strains infecting dissimilar animals inhabiting very different habitats: trout and whales. Together, our data show that closely interacting species can share much of their microbiota, and some versatile microbial species can inhabit and possibly transmit across a diverse range of hosts and environments.

One ant's trash is another ant's treasure: Army ant middens provide resources for diverse ant assemblages

AbstractThe army ant Eciton burchellii boasts more animal associates than any other animal species yet described, but the relationship between army ants and other ant species has only been studied in the context of predation. The waste deposits (middens) of army ant colonies are nitrogen‐rich, a potentially high‐value nutrient source for leaflitter arthropods. We explored this bottom‐up role of army ant middens in the context of tropical ant communities. Our three main questions were the followings: (1) Which ant species forage on army‐ant middens? (2) How does the bi‐phasic life cycle of army ant colonies (affecting midden size, persistence, and abundance) affect which and how many ant species a midden boasts? (3) How do the ants that forage on army ant middens differ across elevations? Across 39 bivouacs, we found 36 species of ants foraging on army ant middens. These included highly predatory ants, nitrogen‐limited arboreal ants, and fungus‐farming ants. Per‐midden richness was significantly lower for the usually smaller middens deposited during the nomadic phase and was higher for the typically larger middens deposited during the statary phase. Per‐midden richness was not significantly different across elevations, but there was far greater species turnover across elevations than across phases within the same elevational site. Our results suggest that army ant middens are an important resource for a wide variety of tropical ants, informing a better understanding of the complex network of associations revolving around this keystone species.Abstract in Spanish is available with online material

The genomic basis of army ant chemosensory adaptations.

The evolution of mass raiding has allowed army ants to become dominant arthropod predators in the tropics. Although a century of research has led to many discoveries about behavioural, morphological and physiological adaptations in army ants, almost nothing is known about the molecular basis of army ant biology. Here we report the genome of the iconic New World army ant Eciton burchellii, and show that it is unusually compact, with a reduced gene complement relative to other ants. In contrast to this overall reduction, a particular gene subfamily (9‐exon ORs) expressed predominantly in female antennae is expanded. This subfamily has previously been linked to the recognition of hydrocarbons, key olfactory cues used in insect communication and prey discrimination. Confocal microscopy of the brain showed a corresponding expansion in a putative hydrocarbon response centre within the antennal lobe, while scanning electron microscopy of the antenna revealed a particularly high density of hydrocarbon‐sensitive sensory hairs. E. burchellii shares these features with its predatory and more cryptic relative, the clonal raider ant. By integrating genomic, transcriptomic and anatomical analyses in a comparative context, our work thus provides evidence that army ants and their relatives possess a suite of modifications in the chemosensory system that may be involved in behavioural coordination and prey selection during social predation. It also lays the groundwork for future studies of army ant biology at the molecular level.

Multi-year genetic sampling indicates maternal gene flow via colony emigrations in the army ant Eciton burchellii parvispinum

Sex-biased dispersal occurs when one sex disperses more frequently or farther than the opposite sex. In ants, dispersal is often male biased and males typically contribute more strongly to gene flow within and among ant populations. However, army ants may offer an exceptional case of female-biased dispersal, because army ant colonies (particularly species in the Neotropical genus Eciton) routinely emigrate among nest sites. We hypothesized that maternal mobility via successive colony emigrations would reduce the relative male bias in dispersal, and that emigrations would contribute to gene flow within an Eciton population. We genotyped workers (highly variable DNA microsatellite loci) from Eciton burchellii parvispinum colonies collected over a 10 × 10 km area in Monteverde, Costa Rica. Samples were spaced approximately 3 years apart (in 2006 and 2009), the typical time between colony reproductive bouts. We used worker genotypes to reconstruct the genotypes of their mother queens and of a subset of the males that sired the workers. We then analyzed the population genetic structure of the queen and male genotypes by comparing individual-based relatedness estimates for each sex across geographic distance and over time. There was no significant difference in spatial genetic structure between the sexes, either within or between the 2006 and 2009 samples. There was some evidence against genetic philopatry: 2009 queens were significantly unrelated to 2006 queens collected nearby (within 0.5 km). The patterns suggest maternal dispersal via emigrations contributes to gene flow, reducing or eliminating male biases in dispersal. From two populations, we estimated average queen dispersal distance to be 0.63–1.04 km, a greater distance than many winged ant queens disperse. Because emigrations over the lifetime of army ant queens may contribute to gene flow across the landscape, habitat connectivity should be maintained to permit colony emigrations and support genetic diversity in populations of this keystone species.

Complex body size differences in thermal tolerance among army ant workers (Eciton burchellii parvispinum)

In social insects, group members can differ in thermal physiology, and these differences may affect colony function. Upper thermal tolerance limits (CTmax) generally increase with body size among and within ant species, but size effects on lower thermal tolerances (CTmin) are poorly known. To test whether CTmin co-variation with body size matched patterns for CTmax, we measured CTmax and CTmin in workers of four size-based worker subcastes in the army ant Eciton burchellii parvispinum. CTmax increased with worker body size as expected. CTmin showed a more complex relationship with size: the two intermediate-size subcastes (media and porters) tolerated lower temperatures than the smallest (minims) and the largest (soldiers) worker subcastes. Body-size effects on CTmax were not predictive of body-size effects on CTmin. These patterns held for colonies collected across elevations that spanned approximately 8 °C in mean annual temperature, even though high-elevation colonies had significantly lower CTmin overall. We predict Eciton army ant subcastes will be differentially affected by directional changes in high and low temperature extremes. Worker subcastes perform distinct but complementary roles in colony function, and differential temperature effects among subcastes could impair colony performance and negatively impact colony fitness.

Heterospecific eavesdropping in ant-following birds of the Neotropics is a learned behaviour.

Animals eavesdrop on other species to obtain information about their environments. Heterospecific eavesdropping can yield tangible fitness benefits by providing valuable information about food resources and predator presence. The ability to eavesdrop may therefore be under strong selection, although extensive research on alarm-calling in avian mixed-species flocks has found only limited evidence that close association with another species could select for innate signal recognition. Nevertheless, very little is known about the evolution of eavesdropping behaviour and the mechanism of heterospecific signal recognition, particularly in other ecological contexts, such as foraging. To understand whether heterospecific eavesdropping was an innate or learned behaviour in a foraging context, we studied heterospecific signal recognition in ant-following birds of the Neotropics, which eavesdrop on vocalizations of obligate ant-following species to locate and recruit to swarms of the army ant Eciton burchellii, a profitable food resource. We used a playback experiment to compare recruitment of ant-following birds to vocalizations of two obligate species at a mainland site (where both species are present) and a nearby island site (where one species remains whereas the other went extinct approx. 40 years ago). We found that ant-following birds recruited strongly to playbacks of the obligate species present at both island and mainland sites, but the island birds did not recruit to playbacks of the absent obligate species. Our results strongly suggest that (i) ant-following birds learn to recognize heterospecific vocalizations from ecological experience and (ii) island birds no longer recognize the locally extinct obligate species after eight generations of absence from the island. Although learning appears to be the mechanism of heterospecific signal recognition in ant-following birds, more experimental tests are needed to fully understand the evolution of eavesdropping behaviour.

Novel approach to heritability detection suggests robustness to paternal genotype in a complex morphological trait.

Heritable variation is essential for evolution by natural selection. In Neotropical army ants, the ecological role of a given species is linked intimately to the morphological variation within the sterile worker caste. Furthermore, the army ant Eciton burchellii is highly polyandrous, presenting a unique opportunity to explore heritability of morphological traits among related workers sharing the same colonial environment. In order to exploit the features of this organismal system, we generated a large genetic and morphological dataset and applied our new method that employs geometric morphometrics (GM) to detect the heritability of complex morphological traits. After validating our approach with an existing dataset of known heritability, we simulated our ability to detect heritable variation given our sampled genotypes, demonstrating the method can robustly recover heritable variation of small effect size. Using this method, we tested for genetic caste determination and heritable morphological variation using genetic and morphological data on 216 individuals of E. burchellii. Results reveal this ant lineage (1) has the highest mating frequency known in ants, (2) demonstrates no paternal genetic caste determination, and (3) suggests a lack of heritable morphological variation in this complex trait associated with paternal genotype. We recommend this method for leveraging the increased resolution of GM data to explore and understand heritable morphological variation in nonmodel organisms.

"Latitudinal Gradients in Species Diversity": Reflections on Pianka's 1966 Article and a Look Forward.

"Latitudinal Gradients in Species Diversity": Reflections on Pianka's 1966 Article and a Look Forward.

Nymphister kronaueri von Beeren & Tishechkin sp. nov., an army ant-associated beetle species (Coleoptera: Histeridae: Haeteriinae) with an exceptional mechanism of phoresy

BackgroundFor more than a century we have known that a high diversity of arthropod species lives in close relationship with army ant colonies. For instance, several hundred guest species have been described to be associated with the Neotropical army ant Eciton burchellii Westwood, 1842. Despite ongoing efforts to survey army ant guest diversity, it is evident that many more species await scientific discovery.ResultsWe conducted a large-scale community survey of Eciton-associated symbionts, combined with extensive DNA barcoding, which led to the discovery of numerous new species, among them a highly specialized histerid beetle, which is formally described here. Analyses of genitalic morphology with support of molecular characters revealed that the new species is a member of the genus Nymphister. We provide a literature review of host records and host-following mechanisms of Eciton-associated Haeteriinae demonstrating that the new species uses an unusual way of phoretic transport to track the nomadic habit of host ants. Using its long mandibles as gripping pliers, the beetle attaches between the ants’ petiole and postpetiole. The beetles specifically attach to medium-sized ant workers, thus participating as hitchhikers in the regular colony emigrations of the single host species Eciton mexicanum Roger, 1863.ConclusionBy providing tools for reliable species identification via morphology and DNA barcodes for hitherto unknown army ant guest species, we set the baseline for studies targeting the ecological and evolutionary dynamics in these species-rich host-symbiont communities.

Landscape genetics of a top neotropical predator

Habitat loss and fragmentation as a consequence of human activities is a worldwide phenomenon and one of the major threats to global biodiversity. Habitat loss and fragmentation is particularly a concern in the biodiverse tropics, where deforestation is occurring at unprecedented rates. Although insects are one of the most diverse and functionally important groups in tropical ecosystems, the quantitative effect of landscape features on their gene flow remains unknown. Here, we used a robust landscape genetics approach to quantify the effect of ten landscape features (deforestation, mature forests, other forest types, the River Chagres, streams, stream banks, roads, sea, lakes and swamps) and interactions between them, on the gene flow of a neotropical forest keystone species, the army ant Eciton burchellii. The influence of landscape on E.burchellii's gene flow reflected the different dispersal capability of its sexes; aerial for males and pedestrian for females, and the different depths of population history inferred from microsatellites and mitochondrial DNA. In contrast to the gene flow-facilitating effect of mature forests, deforested areas were found to be strong barriers for E.burchellii's gene flow. Other forest types were found to be gene flow facilitators but only when interacting with mature secondary forests, therefore indicating the importance of mature forests for the survival of E.burchelii and its associate species. The River Chagres was identified as a major historical gene flow barrier for E.burchellii, suggesting that an important loss of connectivity may occur because of large artificial waterways such as the Panama Canal.

Effect of trail pheromones and weather on the moving behaviour of the army ant Eciton burchellii

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.

The largest animal association centered on one species: the army ant Eciton burchellii and its more than 300 associates

As possibly two of the last true naturalists, Carl Rettenmeyer and his wife Marian dedicated their lives to the study of army ants and their associates. Over the course of 55 years, the Rettenmeyers went on numerous field trips mainly to the Central American tropics and analyzed hundreds of self-collected samples and those sent by a multitude of other scientists, who were inspired by Carl’s enthusiasm. It comes as no surprise that Carl Rettenmeyer became the world’s leading expert on army ant associates. This paper, which the Rettenmeyers nearly completed before Carl’s death in 2009, gives the first comprehensive list of animals known to be found in the company of a single army ant species: Eciton burchellii. The 557 recorded associates range from birds to insects and mites and comprise the largest described animal association centering around one particular species. Although some of these associates may be opportunistic encounters, we are confident that approximately 300 of the recorded species depend on the ants, at least in part, for their existence. The extinction of E. burchellii from any habitat over its vast area of distribution is likely to cause the extinction of numerous associated animals at that site. This overview will hopefully inspire researchers throughout the world to follow in the Rettenmeyers’ footsteps and continue the investigation of army ants and their associates.

Gene flow is maintained by polyandry and male dispersal in the army antEciton burchellii

AbstractThe combination of haplodiploidy, complementary sex determination and eusociality constrains the effective population size (Ne) of social Hymenoptera far more than in any other insect group. Additional limitations onNeoccur in army ants since they have wingless queens and colony fission, both of which are factors causing restricted maternal gene flow and high population viscosity. Therefore, winged army ant males gain a particular significance to ensure dispersal, facilitate gene flow and avoid inbreeding. Based on population genetic analyses with microsatellite markers, we studied a population of the Neotropical army antEciton burchellii, finding a high level of heterozygosity, weak population differentiation and no evidence for inbreeding. Moreover, by using sibship reconstruction analyses, we quantified the actual number of male contributing colonies represented in a queen's mate sample, demonstrating that, through extreme multiple mating, the queens are able to sample the genes of males from up to ten different colonies, usually located within an approximate radius of 1 km. We finally correlated the individual mating success of each male contributing colony with the relative siring success of individual males and found a significant colony‐dependent male fitness component. Our results imply that the dispersal and mating system of these army ants seem to enhance gene flow and minimise the deleterious effects associated with small effective population size.

Dispersal and population structure of a New World predator, the army ant Eciton burchellii

The army ant Eciton burchellii is probably the most important arthropod predator in the Neotropics, and many animal species depend upon it. Sex-biased dispersal with winged males and permanently wingless queens may render this species especially sensitive to habitat fragmentation and natural barriers, which might have severe impacts on population structure and lead to population decline. Using nuclear microsatellite markers and mitochondrial sequences, we investigated genetic differentiation in a fragmented population in the Panama Canal area. While nuclear markers showed little differentiation between subpopulations (F(ST) = 0.017), mitochondrial differentiation was maximal in some cases (Phi(ST) = 1). This suggests that, while females are not capable of crossing barriers such as large rivers, flying males are able to promote nuclear gene flow between the studied forest patches. Consistent with this interpretation, we did not find any evidence for inbreeding or genetic deterioration on Barro Colorado Island over the last 90 years since its formation.

Method Review: Estimation of Colony Densities of the Army Ant Eciton burchellii in Costa Rica

ABSTRACTWe evaluated the performance of a method developed to estimate colony densities of the army ant Eciton burchellii, a keystone species, based on raid crossings on trails, in Costa Rica. The method was compared with a census obtained by tracking ant‐following birds, and the effect of walking distance and rainfall was evaluated. We found that the method performs well when at least 60 km of trail have been walked (replicated walks are permissible), and when rainfall is avoided.

How a few help all: living pothole plugs speed prey delivery in the army ant Eciton burchellii

We investigated an extreme behavioural specialization in the army ant Eciton burchellii . The spectacular group raids of these ants, which can contain up to 200 000 workers, always remain connected to the nest by a ‘principal trail’ of forager traffic. Remarkably, some workers use their bodies to plug potholes in the natural surfaces that the principal trail travels over, to provide a partly living surface for their nestmates to use. We found that this highly specialized behaviour results in a clear net benefit to the colony. Our experiments show that foragers do not discriminate against surfaces that force all individuals to run as slowly as the smallest workers, but that this prompts some ants to plug neighbouring low-quality surfaces. Individuals size-match to the hole they plug and cooperate to plug larger holes. The resulting modified surface allows prey-laden foragers to attain maximum speed. Overall, this results in a strong positive relationship between ant size and speed and an increase in the mean speed of prey-laden traffic. Moreover, calculations suggest that under a range of realistic scenarios, plugging behaviour results in a clear increase in daily prey intake. Broadly, our study provides rare quantitative evidence that extreme specialization by a minority can significantly improve the performance of a majority, and benefit the group as a whole. It also suggests, however, that these benefits are a consequence of the unusual and derived foraging strategy of E. burchellii . This highlights the importance of considering ecology and evolutionary history in the study of social organization in animal societies.

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.

DOES THE AFROTROPICAL ARMY ANT DORYLUS (ANOMMA) MOLESTUS GO EXTINCT IN FRAGMENTED FORESTS?

Swarm-raiding army ants are extremely polyphagous nomadic predators inhabiting tropical forests. They are considered keystone species because their raids can regulate the population dynamics of their prey and because a plethora of both invertebrate and vertebrate species are obligatorily or facultatively associated with them. Field observations and mathematical modelling suggest that deforestation and accompanying forest fragmentation cause local extinctions of the neotropical swarm-raiding army ant Eciton burchellii which in turn have negative effects on its associated fauna. The aim of this study was to examine whether afrotropical army ants are affected by forest fragmentation in the same way. Surveys of Dorylus (Anomma) molestus colonies were carried out in forest fragments of different sizes and in the matrix habitat at two sites in Eastern Kenya, along the Lower Tana River and in the Taita Hills. There was no significant relationship between the presence of D. molestus, forest patch size and distance to the nearest neighbouring patch at either of the sites. Colonies were often found outside the forest and can survive long enough in dry scrubland areas to reach new forest patches as far as 2 km away. We conclude that populations of this army ant species are less vulnerable to fragmentation than those of the neotropical E. burchellii, and that D. molestus can survive better in matrix habitat between forests because of several key differences in the foraging and nesting behaviour of the two species. Finally, we present a simple scenario describing the complex D. molestus population dynamics along the Lower Tana River and discuss the implications of our findings for conservation-oriented management of the two forest systems.

Bare-necked Umbrellabird (Cephalopterus glabricollis) Foraging at an Unusually Large Assemblage of Army Ant-following Birds

I observed a juvenile male Bare-necked Umbrellabird (Cephalopterus glabricollis) forage on arthropods flushed by a large swarm of the army ant Eciton burchellii in the Caribbean foothills of Costa Rica. Apparently, this is the first report of this species attending an army ant swarm. At least 60 birds of eight different species were foraging at that swarm, the largest assemblage of army ant-following birds reported in the Neotropics.

Caste evolution and ecology: a special worker for novel prey

Individual specialization underpins the division of labour within ant societies, but only in a small minority do morphological specialists, or physical castes, exist in the workforce. The genetic conditions that allow such castes to evolve are well understood, but the ecological pressures that select for them are not. We provide compelling evidence that the task of transporting novel prey selected for an exaggerated transport caste, or 'submajor', in the army ant Eciton burchellii. This species is the only Eciton that preys upon large arthropods as well as ants, the ancestral prey type, and by comparing load-transport among Eciton species and within E. burchellii, we show that this mixed diet significantly constrains transport efficiency. Crucially, however, we also show that E. burchellii submajors are highly specialized on transporting non-ant prey, and we demonstrate experientially that it is specifically this prey type that constrains prey-transport efficiency. Our study also suggests that phylogenetic constraints associated with the Eciton lifestyle intensified selection for the exaggerated submajor of E. burchellii. Thus, we propose that a novel task may only select for a special caste when phylogenetic constraints preclude the evolution of alternative solutions. This identifies a new and potentially general scenario for the evolution of physical castes.