The response of grass-cutting ants to natural and synthetic versions of their alarm pheromone

The responses of the grass‐cutting ants Atta bisphaerica (Forel) and Atta capiguara (Gonçalves) to the main components of their alarm pheromones were examined in simple field bioassays. Both species react most strongly to 4‐methyl‐3‐heptanone, which causes the full range of alarm behaviour and a large increase in the number of individuals near the sources. In later experiments with A. capiguara, this increase was found to be due primarily to attraction, with some arrestment also occurring. The ant response to 4‐methyl‐3‐heptanone was compared with that to crushed heads and to that with whole ants with crushed heads. The pheromone 4‐methyl‐3‐heptanone by itself stimulates the same level of attraction as crushed heads, but results in far less alarm behaviour and arrests fewer ants. Whole ants with crushed heads attract a greater number of ants than the other sources and also cause more alarm behaviour. Bodies alone attract ants, but do not result in alarm behaviour. The main component in both species is the same, supporting the view that alarm pheromones lack species specificity. However, it appears that other components may also be important either as synergists of the main compound, or by stimulating behaviours that would not be observed in its absence.     

Genetic evidence for landscape effects on dispersal in the army ant Eciton burchellii

Inhibited dispersal, leading to reduced gene flow, threatens populations with inbreeding depression and local extinction. Fragmentation may be especially detrimental to social insects because inhibited gene flow has important consequences for cooperation and competition within and among colonies. Army ants have winged males and permanently wingless queens; these traits imply male‐biased dispersal. However, army ant colonies are obligately nomadic and have the potential to traverse landscapes. Eciton burchellii, the most regularly nomadic army ant, is a forest interior species: colony raiding activities are limited in the absence of forest cover. To examine whether nomadism and landscape (forest clearing and elevation) affect population genetic structure in a montane E. burchellii population, we reconstructed queen and male genotypes from 25 colonies at seven polymorphic microsatellite loci. Pairwise genetic distances among individuals were compared to pairwise geographical and resistance distances using regressions with permutations, partial Mantel tests and random forests analyses. Although there was no significant spatial genetic structure in queens or males in montane forest, dispersal may be male‐biased. We found significant isolation by landscape resistance for queens based on land cover (forest clearing), but not on elevation. Summed colony emigrations over the lifetime of the queen may contribute to gene flow in this species and forest clearing impedes these movements and subsequent gene dispersal. Further forest cover removal may increasingly inhibit Eciton burchellii colony dispersal. We recommend maintaining habitat connectivity in tropical forests to promote population persistence for this keystone species.     

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.     

Multiple functions of fire ant Solenopsis invicta mandibular gland products

Alarm pheromones of social insects are best known for their role in the defence and maintenance of colony integrity. Previous studies with the fire ant Solenopsis invicta Buren (Hymenoptera: Formicidae) demonstrate that the mandibular glands of workers (sterile females) and male and female sexuals produce an alarm pheromone, 2‐ethyl‐3,6‐dimethylpyrazine. The function of alarm pheromones in worker ants is well understood and divergent from the function of these compounds in the winged sexual forms. The present study quantifies the amount of pyrazine in the mandibular glands from male and female alate sexuals, as well as queens. Pyrazine production in female alates starts in the late pupal stage and increases until they reach mating flight‐ready maturity; however, after mating flight participation, the pyrazine level declines by >50%. Interestingly, mature male alates lose >85% of their mandibular gland pyrazine during mating flight activity. The results of the present study indicate that male and female sexuals use mandibular gland secretions for mating flight initiation and during mating flights. Furthermore, the ontogeny of mandibular gland products (pyrazine as the marker) from newly‐mated queens to mature colony queens shows a more than two‐fold increase in the amount of pyrazine by 6 months after mating. However, this is followed by a decline to trace amounts in mature colony queens (>2 years old), suggesting a function for mandibular gland products during colony development. Multifunctional use of social insect pheromones is well documented and data are reported in the present study suggesting new roles for mandibular gland products in fire ants.     

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.     

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.     

The largest animal association centered on one species: the army ant <Emphasis Type="Italic">Eciton burchellii</Emphasis> 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.     

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.     

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.     

Symbionts of societies that fission: mites as guests or parasites of army ants

• 1 Recently, Hughes et al. (Trends in Ecology & Evolution, 23 , 672–677, 2008) have theorised that symbionts of large, long‐lived, homeostatic, and well defended social insect colonies should mostly be of low virulence. If the symbionts are rare, i.e. few workers are co‐infected, competition between symbionts should be minimal and they should be selected to avoid over‐exploiting their hosts.
• 2 Here we analyse the mites that occur on Eciton burchellii army ant workers and note that our findings are consistent with the predictions from evolutionary theory.
• 3 The mites were species diverse but rare; only 5% of the 3146 workers we examined from 20 army ant colonies had mites. Only one worker was co‐infected by mites of different species and the one relatively common parasitic mite (Rettenmeyerius carli) was limited to only two individuals per ant.
• 4 We also showed that certain mites are more common on workers in nomadic rather than statary army ant colonies and that different worker castes differed in their infestation patterns.
• 5 We suggest that the three traits E. burchellii and honey bees (Apis mellifera) have in common (queens with very high mating frequencies, propagation by colony fission, and low number of parasites among the mite species they host) are associated with one another. Colonies that fission are likely to inherit symbionts and multiple mating will promote genetic diversity within colonies, which may help to limit the abundance of deleterious mites.
• 6 We conclude that most of the symbiotic mites found on workers of the army ant E. burchellii are probably relatively harmless guests, exploiting their hosts for phoresis or, for example, to use their waste deposits.

     

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.     

Source of alate excitant pheromones in the red imported fire antSolenopsis invicta (Hymenoptera: Formicidae)

At the onset of mating flights inSolenopsis invicta, workers swarm excitedly over the mound as alates prepare to fly. Previous studies demonstrated that this excitement is stimulated by the male and female alates. We investigated the glandular source(s) of pheromones produced by the alates that cause excitement. The only common female and male alate body part that elicited excitement when crushed was the head. Within the head, excised mandibular glands were found to be responsible for worker excitement. Fire ant workers are very sensitive to external stimuli and some excitement was elicited by crushed female gasters and male thoraces, but the response was never as significant as with crushed heads. Tests with summer and winter alates revealed similar results, except that gasters of winter female alates had a greater excitant effect than did gasters of summer female alates. This may be due to the production of attractant pheromones by the poison glands of overwintering female alates. We conclude that the mandibular gland is the source of alate excitant pheromones.     

Do army ant queens re-mate later in life?

Queens of eusocial Hymenoptera are inseminated only during a brief period before they start to lay eggs. This has probably been kin-selected because repeated insemination of old queens would normally be against the inclusive fitness interest of their daughter workers. Army ants have been considered to be the only possible exception to this rule due to their idiosyncratic life-history. We studied two distantly related species of army ants, the African Dorylus (Anomma) molestus and the Neotropical Eciton burchellii and present data from microsatellite genotyping, behavioural observations and sperm counts.We also describe the copulation behaviour of African army ants for the first time. Our results strongly suggest that, contradictory to earlier contentions, army ant queens do not mate repeatedly throughout their life and thus do not constitute an exception among the eusocial Hymenoptera in this respect. Sperm counts for males and queens of both species show that army ant queens have to mate with several males to become fully inseminated. However, sperm limitation by queens is unlikely to have been the prime reason for the evolution of high queen-mating frequencies in this group. Received 5 July 2006; revised 26 September 2006; accepted 11 October 2006.     

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.     

An ambiguous function of an alarm pheromone in the collective displays of the Australian meat ant,Iridomyrmex purpureus

Alarm pheromones, which have been documented in many species of ants, are thought to elicit responses related to aggressive or defensive behaviour. The volatile odour 6-methyl-5-hepten-2-one is described as an alarm pheromone in several species of ants, including the Australian meat ant, Iridomyrmex purpureus. The alarm pheromone is released by displaying workers that aggregate in the characteristic collective display grounds, located mid-way between colonies or near contested food trees. Workers are typically more aggressive at the latter location, and the alarm pheromone may regulate the collective level of aggression. We investigated this possibility by exposing displaying workers to synthesised alarm pheromone 6-methyl-5-hepten-2-one in a field experiment, and measuring their aggressive behaviour. We found no evidence that exposure to synthesised alarm pheromone caused changes in the aggressive level of workers. Subsequent field experiments revealed that the pheromone functions as an attractant, thereby increasing the density of displaying workers. More densely populated workers also display more aggressively, indicating that the interaction rate of displaying workers may determine the level of aggression in collective displays. This underlying mechanism can explain why displaying ants are more aggressive at the more densely populated food-tree locations than those displaying at locations midway between two neighbouring colony nest sites.     

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.     

A sophisticated,modular communication contributes to ecological dominance in the invasive ant <Emphasis Type="Italic">Anoplolepis gracilipes</Emphasis>

The ecological success of ants is founded on cooperative behaviour and a well functioning communication. Particularly invasive ants are able to act highly cooperatively, out-compete other species, and become ecologically dominant. Since ant communication is to a large extent chemical, we investigated the pheromone functions involved in foraging and alarm behaviour of the invasive tropical formicine Anoplolepis gracilipes. Our results suggest that long-lasting orientation cues are located in hindguts, while Dufour glands contain short-term attractants that trigger an effective recruitment. Poison gland effects were intermediate between hindgut and Dufour gland in terms of orientation, attraction and longevity. In contrast to the other pheromone sources, mandibular glands have a repellent effect and are most likely involved in alarm behaviour. Taken together, the pheromone glands of A. gracilipes contain functionally distinct signals with considerable differences in persistence. In this respect, its communication is exceptional in formicine ants. A strikingly similar communication system was previously detected in Paratrechina longicornis, another opportunistic and invasive formicine ant. Based on these similarities and the differences compared to non-invasive formicine ants, we discuss the role of chemical signals for the coordination of efficient foraging. We conclude that a sophisticated communication system can contribute significantly to ecological dominance and invasive success, in concert with other well known traits.     

Social Insect Pheromones: Their Chemistry and Function

Exocrine secretions of social insects are often characterizedby extraordinarily complex mixtures of natural products. Thus,chemical communication in social insects must be interpretedin terms of signals generated by multicomponent systems, theindividual constituents of which can affect the informationalcontent of the message. Alarm pheromones have been identified chiefly in three subfamiliesof ants and their distribution appears to be chemosystematicallysignificant. Myrmicine genera emphasize 3-alkanones as alarmreleasers, whereas methyl ketones, primarily of terpenoidalorigin, are widely utilized as alarm pheromones in the subfamilyDolichoderinae. Formicine species may employ formic acidas analarm pheromone in addition to the compounds produced in themandibular and Dufour's glands. The mandibular gland pheromonesare chiefly acyclic monoterpene aldehydes (e.g., citronellal)which are relatively low boiling compounds. Higher boiling n-alkanesare produced in the Dufour's glands and may serve as more persistentreleasers of alarm behavior. Alarm pheromones as well as thecaste-specific pheromones of male bees and ants, probably alsoserve as defensive products. In many cases it is likely thatpheromones were originally utilized as defensive compounds andtheir communicative function is a secondary development.     

Behaviour of the army ant Eciton burchelli westwood (Hymenoptera: Formicidae) in the Belém region. I. Nomadic-statary cycles

This paper is the first of a series on the behaviour of Eciton burchelli Westwood. Some observations on Eciton hamatum Fabricius are added. The study took 2 years and was carried out in a forest reserve at the Instituto de Pesquisa e Experimentação Agropecuárias dp Norte (IPEAN), Belém, State of Pará, Brazil. All the movements of E. burchelli and E. hamatum colonies were mapped. Colonies were observed in different seasons and in different types of forest. For six E. burchelli colonies 34 Nomadic-Statary cycle (NSC) durations were recorded giving the lengths of the Nomadic Phase (NP) and Statary Phase (SP). Five NSC, NP and SP durations of one E. hamatum colony were recorded. The data confirm the existence of endogenous cycles of activity in these ants and suggest that they have a basically uniform periodicity over a very wide area (Panama to Belém).     

Ants Do Not Traverse the Silk of Adult Female <Emphasis Type="Italic">Nephila clavipes</Emphasis> (Linnaeus) Webs

Many organisms use chemicals to deter enemies. Some spiders can modify the composition of their silk to deter predators from climbing onto their webs. The Malaysian golden orb-weaver Nephila antipodiana (Walckenaer) produces silk containing an alkaloid (2-pyrrolidinone) that functions as a defense against ant invasion—ants avoid silk containing this chemical. In the present study, we test the generality of ants’ silk avoidance behavior in the field. We introduced three ant species to the orb webs of Nephila clavipes (Linnaeus) in the tropical rainforest of La Selva, Costa Rica. We found that predatory army ants (Eciton burchellii Westwood) as well as non-predatory leaf-cutting ants (Atta cephalotes Linnaeus and Acromyrmex volcanus Wheeler) avoided adult N. clavipes silk, suggesting that an additional species within genus Nephila may possess ant-deterring silk. Our field assay also suggests that silk avoidance behavior is found in multiple ant species.