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1.  Behavioral plasticity mediates asymmetric competition between invasive wasps and native ants 
One of the most successful invasive species is the common wasp, Vespula vulgaris. We recently reported how foragers of this species have adopted previously unknown interference behavior when competing for food with native ants. Picking their opponents up in their mandibles, flying backward and dropping them some distance away from the disputed resource, wasps were shown to efficiently deal with a yet aggressive competitor and to modulate this behavior according to circumstances. Here we further discuss the nature and functioning of this unusual strategy. We first highlight the questions this interaction raises regarding the competitive advantages offered by asymmetries in body size and flight ability. Then, we argue that this study system illustrates the important role of behavioral plasticity in biological invasions; not only in the success of invaders but also in the ability of native species to coexist with these invaders.
PMCID: PMC3376045  PMID: 22808314
biological invasions; interference behavior; Prolasius advenus; social insects; Vespula vulgaris
2.  Strike Fast, Strike Hard: The Red-Throated Caracara Exploits Absconding Behavior of Social Wasps during Nest Predation 
PLoS ONE  2013;8(12):e84114.
Red-throated Caracaras Ibycter americanus (Falconidae) are specialist predators of social wasps in the Neotropics. It had been proposed that these caracaras possess chemical repellents that allow them to take the brood of wasp nests without being attacked by worker wasps. To determine how caracaras exploit nests of social wasps and whether chemical repellents facilitate predation, we: (1) video recorded the birds attacking wasp nests; (2) analyzed surface extracts of the birds' faces, feet, and feathers for potential chemical repellents; and (3) inflicted mechanical damage on wasp nests to determine the defensive behavior of wasps in response to varying levels of disturbance. During caracara predation events, two species of large-bodied wasps mounted stinging attacks on caracaras, whereas three smaller-bodied wasp species did not. The “hit-and-run” predation tactic of caracaras when they attacked nests of large and aggressive wasps reduced the risk of getting stung. Our data reveal that the predation strategy of caracaras is based on mechanical disturbance of, and damage to, target wasp nests. Caracara attacks and severe experimental disturbance of nests invariably caused wasps to abscond (abandon their nests). Two compounds in caracara foot extracts [sulcatone and iridodial] elicited electrophysiological responses from wasp antennae, and were also present in defensive secretions of sympatric arboreal-nesting Azteca ants. These compounds appear not to be wasp repellents but to be acquired coincidentally by caracaras when they perch on trees inhabited with Azteca ants. We conclude that caracara predation success does not depend on wasp repellents but relies on the absconding response that is typical of swarm-founding polistine wasps. Our study highlights the potential importance of vertebrate predators in the ecology and evolution of social wasps.
PMCID: PMC3873407  PMID: 24386338
3.  The Effect of Diet and Opponent Size on Aggressive Interactions Involving Caribbean Crazy Ants (Nylanderia fulva) 
PLoS ONE  2013;8(6):e66912.
Biotic interactions are often important in the establishment and spread of invasive species. In particular, competition between introduced and native species can strongly influence the distribution and spread of exotic species and in some cases competition among introduced species can be important. The Caribbean crazy ant, Nylanderia fulva, was recently introduced to the Gulf Coast of Texas, and appears to be spreading inland. It has been hypothesized that competition with the red imported fire ant, Solenopsis invicta, may be an important factor in the spread of crazy ants. We investigated the potential of interspecific competition among these two introduced ants by measuring interspecific aggression between Caribbean crazy ant workers and workers of Solenopsis invicta. Specifically, we examined the effect of body size and diet on individual-level aggressive interactions among crazy ant workers and fire ants. We found that differences in diet did not alter interactions between crazy ant workers from different nests, but carbohydrate level did play an important role in antagonistic interactions with fire ants: crazy ants on low sugar diets were more aggressive and less likely to be killed in aggressive encounters with fire ants. We found that large fire ants engaged in fewer fights with crazy ants than small fire ants, but fire ant size affected neither fire ant nor crazy ant mortality. Overall, crazy ants experienced higher mortality than fire ants after aggressive encounters. Our findings suggest that fire ant workers might outcompete crazy ant workers on an individual level, providing some biotic resistance to crazy ant range expansion. However, this resistance may be overcome by crazy ants that have a restricted sugar intake, which may occur when crazy ants are excluded from resources by fire ants.
PMCID: PMC3679061  PMID: 23776702
4.  A Specialist Herbivore Uses Chemical Camouflage to Overcome the Defenses of an Ant-Plant Mutualism 
PLoS ONE  2014;9(7):e102604.
Many plants and ants engage in mutualisms where plants provide food and shelter to the ants in exchange for protection against herbivores and competitors. Although several species of herbivores thwart ant defenses and extract resources from the plants, the mechanisms that allow these herbivores to avoid attack are poorly understood. The specialist insect herbivore, Piezogaster reclusus (Hemiptera: Coreidae), feeds on Neotropical bull-horn acacias (Vachellia collinsii) despite the presence of Pseudomyrmex spinicola ants that nest in and aggressively defend the trees. We tested three hypotheses for how P. reclusus feeds on V. collinsii while avoiding ant attack: (1) chemical camouflage via cuticular surface compounds, (2) chemical deterrence via metathoracic defense glands, and (3) behavioral traits that reduce ant detection or attack. Our results showed that compounds from both P. reclusus cuticles and metathoracic glands reduce the number of ant attacks, but only cuticular compounds appear to be essential in allowing P. reclusus to feed on bull-horn acacia trees undisturbed. In addition, we found that ant attack rates to P. reclusus increased significantly when individuals were transferred between P. spinicola ant colonies. These results are consistent with the hypothesis that chemical mimicry of colony-specific ant or host plant odors plays a key role in allowing P. reclusus to circumvent ant defenses and gain access to important resources, including food and possibly enemy-free space. This interaction between ants, acacias, and their herbivores provides an excellent example of the ability of herbivores to adapt to ant defenses of plants and suggests that herbivores may play an important role in the evolution and maintenance of mutualisms.
PMCID: PMC4105532  PMID: 25047551
5.  Ant-plant-homopteran mutualism: how the third partner affects the interaction between a plant-specialist ant and its myrmecophyte host 
By estimating relative costs and benefits, we explored the role of the homopteran partner in the protection mutualism between the myrmecophyte Leonardoxa africana T3, the ant Aphomomyrmex afer, and sap-sucking homopterans tended by ants in the tree's swollen hollow twigs. The ants obtain nest sites and food from their host-plant (food is obtained either directly by extrafloral nectar or indirectly via homopterans). Aphomomyrmex workers patrol the young leaves of L. africana T3 and protect them against phytophagous insects. Because ants tended, either solely or primarily, coccids in some trees and pseudococcids in others, we were able to study whether the nature of the interaction was dependent on the identity of the third partner. First, the type of homopteran affects the benefits to the tree of maintaining a large ant colony. Larger colony size (relative to tree size) confers greater protection against herbivory; this relationship is more pronounced for trees whose ants tend pseudococcids than for those in which ants tend coccids. Second, for trees (and associated ant colonies) of comparable size, homopteran biomass was much larger in trees harbouring coccids than in trees with pseudococcids. Thus, the cost to the tree of maintaining ants may be greater when ants are associated with coccids. The net benefits to the plant of maintaining ants appear to be much greater with pseudococcids as the third partner. To explore how the type of homopteran affects functioning of the system, we attempted to determine which of the resources (nest sites, extrafloral nectar, and homopterans) is likely to limit ant colony size. In trees where ants tended coccids, ant-colony biomass was strongly dependent on the number of extrafloral nectaries. In contrast, in trees whose ants tended only pseudococcids, colony biomass was not related to the number of nectaries and was most strongly determined by the volume of available nest sites. We present hypotheses to explain how the type of homopteran affects functioning of this symbiosis, and discuss the implications of our study for the evolutionary ecology of ant–plant–homopteran relationships.
PMCID: PMC1689010
6.  Termites, hemimetabolous diploid white ants? 
Frontiers in Zoology  2008;5:15.
Ants and termites are the most abundant animals on earth. Their ecological success is attributed to their social life. They live in colonies consisting of few reproducing individuals, while the large majority of colony members (workers/soldiers) forego reproduction at least temporarilly. Despite their apparent resemblance in social organisation, both groups evolved social life independently. Termites are basically social cockroaches, while ants evolved from predatory wasps. In this review, I will concentrate on termites with an ancestral life type, the wood-dwelling termites, to compare them with ants. Their different ancestries provided both groups with different life history pre-adaptations for social evolution. Like their closest relatives, the woodroaches, wood-dwelling termites live inside their food, a piece of wood. Thus, intensive costly food provisioning of their young is not necessary, especially as young instars are rather independent due to their hemimetabolous development. In contrast, ants are progressive food provisioners which have to care intensively for their helpless brood. Corresponding to the precocial – altricial analogy, helping by workers is selected in ants, while new evidence suggests that wood-dwelling termite workers are less engaged in brood care. Rather they seem to stay in the nest because there is generally low selection for dispersal. The nest presents a safe haven with no local resource competition as long as food is abundant (which is generally the case), while founding a new colony is very risky. Despite these differences between ants and termites, their common dwelling life style resulted in convergent evolution, especially winglessness, that probably accounts for the striking similarity between both groups. In ants, all workers are wingless and winglessness in sexuals evolved in several taxa as a derived trait. In wood-dwelling termites, workers are by default wingless as they are immatures. These immatures can develop into winged sexuals that disperse and found a new nest or into neotenic replacement reproductives that inherit the natal colony. Depending on the worker instar from which the latter develop, the neotenic reproductives are either apterous or brachypterous, but never winged. I propose that this wing polyphenism might present a basis for the evolution of social life in termites.
PMCID: PMC2564920  PMID: 18822181
7.  Non-additive benefit or cost? Disentangling the indirect effects that occur when plants bearing extrafloral nectaries and honeydew-producing insects share exotic ant mutualists 
Annals of Botany  2013;111(6):1295-1307.
Background and Aims
In complex communities, organisms often form mutualisms with multiple different partners simultaneously. Non-additive effects may emerge among species linked by these positive interactions. Ants commonly participate in mutualisms with both honeydew-producing insects (HPI) and their extrafloral nectary (EFN)-bearing host plants. Consequently, HPI and EFN-bearing plants may experience non-additive benefits or costs when these groups co-occur. The outcomes of these interactions are likely to be influenced by variation in preferences among ants for honeydew vs. nectar. In this study, a test was made for non-additive effects on HPI and EFN-bearing plants resulting from sharing exotic ant guards. Preferences of the dominant exotic ant species for nectar vs. honeydew resources were also examined.
Ant access, HPI and nectar availability were manipulated on the EFN-bearing shrub, Morinda citrifolia, and ant and HPI abundances, herbivory and plant growth were assessed. Ant-tending behaviours toward HPI across an experimental gradient of nectar availability were also tracked in order to investigate mechanisms underlying ant responses.
Key Results
The dominant ant species, Anoplolepis gracilipes, differed from less invasive ants in response to multiple mutualists, with reductions in plot-wide abundances when nectar was reduced, but no response to HPI reduction. Conversely, at sites where A. gracilipes was absent or rare, abundances of less invasive ants increased when nectar was reduced, but declined when HPI were reduced. Non-additive benefits were found at sites dominated by A. gracilipes, but only for M. citrifolia plants. Responses of HPI at these sites supported predictions of the non-additive cost model. Interestingly, the opposite non-additive patterns emerged at sites dominated by other ants.
It was demonstrated that strong non-additive benefits and costs can both occur when a plant and herbivore share mutualist partners. These findings suggest that broadening the community context of mutualism studies can reveal important non-additive effects and increase understanding of the dynamics of species interactions.
PMCID: PMC3662523  PMID: 23609021
Additive effects; Anoplolepis gracilipes; community context; extrafloral nectar; EFN; honeydew; indirect effects; invasive ants; Morinda citrifolia; mutualism; non-additive benefit; non-additive cost; simultaneous interactions
8.  Behavioural and chemical evidence for multiple colonisation of the Argentine ant, Linepithema humile, in the Western Cape, South Africa 
BMC Ecology  2011;11:6.
The Argentine ant, Linepithema humile, is a widespread invasive ant species that has successfully established in nearly all continents across the globe. Argentine ants are characterised by a social structure known as unicoloniality, where territorial boundaries between nests are absent and intraspecific aggression is rare. This is particularly pronounced in introduced populations and results in the formation of large and spatially expansive supercolonies. Although it is amongst the most well studied of invasive ants, very little work has been done on this ant in South Africa. In this first study, we investigate the population structure of Argentine ants in South Africa. We use behavioural (aggression tests) and chemical (CHC) approaches to investigate the population structure of Argentine ants within the Western Cape, identify the number of supercolonies and infer number of introductions.
Both the aggression assays and chemical data revealed that the Western Cape Argentine ant population can be divided into two behaviourally and chemically distinct supercolonies. Intraspecific aggression was evident between the two supercolonies of Argentine ants with ants able to discriminate among conspecific non-nestmates. This discrimination is linked to the divergence in cuticular hydrocarbon profiles of ants originating from the two supercolonies.
The presence of these two distinct supercolonies is suggestive of at least two independent introductions of this ant within the Western Cape. Moreover, the pattern of colonisation observed in this study, with the two colonies interspersed, is in agreement with global patterns of Argentine ant invasions. Our findings are of interest because recent studies show that Argentine ants from South Africa are different from those identified in other introduced ranges and therefore provide an opportunity to further understand factors that determine the distributional and spread patterns of Argentine ant supercolonies.
PMCID: PMC3041649  PMID: 21288369
9.  Disruption of Foraging by a Dominant Invasive Species to Decrease Its Competitive Ability 
PLoS ONE  2014;9(3):e90173.
Invasive species are a major threat to biodiversity when dominant within their newly established habitat. The globally distributed Argentine ant Linepithema humile has been reported to break the trade-off between interference and exploitative competition, achieve high population densities, and overpower nests of many endemic ant species. We have used the sensitivity of the Argentine ant to the synthetic trail pheromone (Z)-9-hexadecanal to investigate species interactions for the first time. We predicted that disrupting Argentine ant trail following behaviour would reduce their competitive ability and create an opportunity for three other resident species to increase their foraging success. Argentine ant success in the control was reduced with increasing pheromone concentration, as predicted, but interactions varied among competing resident species. These behavioural variations provide an explanation for observed differences in foraging success of the competing resident species and how much each of these individual competitors can increase their foraging if the competitive ability of the dominant invader is decreased. The mechanism for the observed increase in resource acquisition of resident species appears to be a decrease in aggressive behaviour displayed by the Argentine ant, which may create an opportunity for other resident species to forage more successfully. Our demonstration of species interactions with trail pheromone disruption is the first known case of reduced dominance under a pheromone treatment in ants.
PMCID: PMC3942413  PMID: 24594633
10.  Arboreal Ant Colonies as ‘Hot-Points’ of Cryptic Diversity for Myrmecophiles: The Weaver Ant Camponotus sp. aff. textor and Its Interaction Network with Its Associates 
PLoS ONE  2014;9(6):e100155.
Systematic surveys of macrofaunal diversity within ant colonies are lacking, particularly for ants nesting in microhabitats that are difficult to sample. Species associated with ants are generally small and rarely collected organisms, which makes them more likely to be unnoticed. We assumed that this tendency is greater for arthropod communities in microhabitats with low accessibility, such as those found in the nests of arboreal ants that may constitute a source of cryptic biodiversity.
Materials and Methods
We investigated the invertebrate diversity associated with an undescribed, but already threatened, Neotropical Camponotus weaver ant. As most of the common sampling methods used in studies of ant diversity are not suited for evaluating myrmecophile diversity within ant nests, we evaluated the macrofauna within ant nests through exhaustive colony sampling of three nests and examination of more than 80,000 individuals.
We identified invertebrates from three classes belonging to 18 taxa, some of which were new to science, and recorded the first instance of the co-occurrence of two brood parasitoid wasp families attacking the same ant host colony. This diversity of ant associates corresponded to a highly complex interaction network. Agonistic interactions prevailed, but the prevalence of myrmecophiles was remarkably low.
Our data support the hypothesis of the evolution of low virulence in a variety of symbionts associated with large insect societies. Because most myrmecophiles found in this work are rare, strictly specific, and exhibit highly specialized biology, the risk of extinction for these hitherto unknown invertebrates and their natural enemies is high. The cryptic, far unappreciated diversity within arboreal ant nests in areas at high risk of habitat loss qualifies these nests as ‘hot-points’ of biodiversity that urgently require special attention as a component of conservation and management programs.
PMCID: PMC4062527  PMID: 24941047
11.  Species-Specific Seed Dispersal in an Obligate Ant-Plant Mutualism 
PLoS ONE  2009;4(2):e4335.
Throughout lowland Amazonia, arboreal ants collect seeds of specific plants and cultivate them in nutrient-rich nests, forming diverse yet obligate and species-specific symbioses called Neotropical ant-gardens (AGs). The ants depend on their symbiotic plants for nest stability, and the plants depend on AGs for substrate and nutrients. Although the AGs are limited to specific participants, it is unknown at what stage specificity arises, and seed fate pathways in AG epiphytes are undocumented. Here we examine the specificity of the ant-seed interaction by comparing the ant community observed at general food baits to ants attracted to and removing seeds of the AG plant Peperomia macrostachya. We also compare seed removal rates under treatments that excluded vertebrates, arthropods, or both. In the bait study, only three of 70 ant species collected P. macrostachya seeds, and 84% of observed seed removal by ants was attributed to the AG ant Camponotus femoratus. In the exclusion experiment, arthropod exclusion significantly reduced seed removal rates, but vertebrate exclusion did not. We provide the most extensive empirical evidence of species specificity in the AG mutualism and begin to quantify factors that affect seed fate in order to understand conditions that favor its departure from the typical diffuse model of plant-animal mutualism.
PMCID: PMC2632754  PMID: 19194502
12.  Thermoregulation of water foraging wasps (Vespula vulgaris and Polistes dominulus) 
Journal of insect physiology  2009;55(10):959-966.
A comparison of the thermoregulation of water foraging wasps (Vespula vulgaris, Polistes dominulus) under special consideration of ambient temperature and solar radiation was conducted. The body surface temperature of living and dead wasps was measured by infrared thermography under natural conditions in their environment without disturbing the insects’ behaviour. The body temperature of both of them was positively correlated with Ta and solar radiation. At moderate Ta (22–28 °C) the regression lines revealed mean thorax temperatures (Tth) of 35.5–37.5 °C in Vespula, and of 28.6–33.7 °C in Polistes. At high Ta (30–39 °C) Tth was 37.2–40.6 °C in Vespula and 37.0–40.8 °C in Polistes. The thorax temperature excess (Tth–Ta) increased at moderate Ta by 1.9 °C (Vespula) and 4.4 °C (Polistes) per kW−1 m−2. At high Ta it increased by 4.0 °C per kW−1 m−2 in both wasps. A comparison of the living water foraging Vespula and Polistes with dead wasps revealed a great difference in their thermoregulatory behaviour. At moderate Ta (22–28 °C) Vespula exhibited distinct endothermy in contrast to Polistes, which showed only a weak endothermic activity. At high Ta (30–39 °C) Vespula reduced their active heat production, and Polistes were always ectothermic. Both species exhibited an increasing cooling effort with increasing insolation and ambient temperature.
PMCID: PMC3227726  PMID: 19589341
Wasp; Thermoregulation; Foraging; Thermography; Water
13.  Influence of plant genetic diversity on interactions between higher trophic levels 
Biology Letters  2013;9(3):20130133.
While the ecological consequences of plant diversity have received much attention, the mechanisms by which intraspecific diversity affects associated communities remains understudied. We report on a field experiment documenting the effects of patch diversity in the plant Baccharis salicifolia (genotypic monocultures versus polycultures of four genotypes), ants (presence versus absence) and their interaction on ant-tended aphids, ants and parasitic wasps, and the mechanistic pathways by which diversity influences their multi-trophic interactions. Five months after planting, polycultures (versus monocultures) had increased abundances of aphids (threefold), ants (3.2-fold) and parasitoids (1.7-fold) owing to non-additive effects of genetic diversity. The effect on aphids was direct, as plant genetic diversity did not mediate ant–aphid, parasitoid–aphid or ant–parasitoid interactions. This increase in aphid abundance occurred even though plant growth (and thus aphid resources) was not higher in polycultures. The increase in ants and parasitoids was an indirect effect, due entirely to higher aphid abundance. Ants reduced parasitoid abundance by 60 per cent, but did not affect aphid abundance or plant growth, and these top-down effects were equivalent between monocultures and polycultures. In summary, intraspecific plant diversity did not increase primary productivity, but nevertheless had strong effects across multiple trophic levels, and effects on both herbivore mutualists and enemies could be predicted entirely as an extension of plant–herbivore interactions.
PMCID: PMC3645048  PMID: 23485879
ant-tended aphids; aphid-tending ants; Baccharis salicifolia; monocultures; parasitic wasps; polycultures
14.  Do Leaf Cutting Ants Cut Undetected? Testing the Effect of Ant-Induced Plant Defences on Foraging Decisions in Atta colombica 
PLoS ONE  2011;6(7):e22340.
Leaf-cutting ants (LCAs) are polyphagous, yet highly selective herbivores. The factors that govern their selection of food plants, however, remain poorly understood. We hypothesized that the induction of anti-herbivore defences by attacked food plants, which are toxic to either ants or their mutualistic fungus, should significantly affect the ants' foraging behaviour. To test this “induced defence hypothesis,” we used lima bean (Phaseolus lunatus), a plant that emits many volatile organic compounds (VOCs) upon herbivore attack with known anti-fungal or ant-repellent effects. Our results provide three important insights into the foraging ecology of LCAs. First, leaf-cutting by Atta ants can induce plant defences: Lima bean plants that were repeatedly exposed to foraging workers of Atta colombica over a period of three days emitted significantly more VOCs than undamaged control plants. Second, the level to which a plant has induced its anti-herbivore defences can affect the LCAs' foraging behaviour: In dual choice bioassays, foragers discriminated control plants from plants that have been damaged mechanically or by LCAs 24 h ago. In contrast, strong induction levels of plants after treatment with the plant hormone jasmonic acid or three days of LCA feeding strongly repelled LCA foragers relative to undamaged control plants. Third, the LCA-specific mode of damaging leaves allows them to remove larger quantities of leaf material before being recognized by the plant: While leaf loss of approximately 15% due to a chewing herbivore (coccinelid beetle) was sufficient to significantly increase VOC emission levels after 24 h, the removal of even 20% of a plant's leaf area within 20 min by LCAs did not affect its VOC emission rate after 24 h. Taken together, our results support the “induced defence hypothesis” and provide first empirical evidence that the foraging behaviour of LCAs is affected by the induction of plant defence responses.
PMCID: PMC3140513  PMID: 21799831
15.  Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors 
eLife  2014;3:e01539.
The concerted evolution of morphological and behavioral specializations has compelling examples in ant castes. Unique to ants is a marked divergence between winged queens and wingless workers, but morphological specializations for behaviors on the ground have been overlooked. We analyzed thorax morphology of queens and workers in species from 21 of the 25 ant subfamilies. We uncovered unique skeletomuscular modifications in workers that presumably increase power and flexibility of head–thorax articulation, emphasizing that workers are not simply wingless versions of queens. We also identified two distinct types of queens and showed repeated evolutionary associations with strategies of colony foundation. Solitary founding queens that hunt have a more worker-like thorax. Our results reveal that ants invest in the relative size of thorax segments according to their tasks. Versatility of head movements allows for better manipulation of food and objects, which arguably contributed to the ants’ ecological and evolutionary success.
eLife digest
The size and shape of an animal, known as its morphology, often reflect the actions it can perform. A grasshopper’s long legs, for example, are well suited to hopping, whilst the streamlined body of a dolphin helps swimming through water. These specialized features result from the interplay between morphology and behavior during evolution. A change in morphology can make new behaviors possible, which can then expose the animal to new environments and selective pressures that, in turn, can lead to further changes in morphology.
The interplay between morphology and behavior is particularly interesting in social insects such as ants. Queens and workers within an ant colony have a similar set of genes, but they have dramatically different morphologies and very different roles within the colony. Queens are responsible for reproduction, and are larger and have wings, which allow them to fly and establish a new colony away from where they were born. Workers are smaller and lack wings, and they devote themselves to building the nest, feeding the young larvae and protecting the colony. This marked morphological divergence, unique to ants, has fascinated researchers for more than a century. However, most studies have focused on the presence or absence of wings and have overlooked the interactions between morphology and the actions performed on the ground.
Like all insects, an ant’s body is divided into three parts: the head, the thorax (to which the legs and wings are attached), and the abdomen. Now, Keller et al. have examined the shape of the thorax in many species of ants and found that workers are not just smaller wingless versions of queens: rather, the architecture of their thorax is unique among species of flying insects. The front end of the worker thorax is greatly enlarged and is filled by strong neck muscles that power the head and its jaws, and allow workers to hunt and carry prey many times their own weight.
Keller et al. also identified two distinct types of queens and went on to show that these two shapes evolved in association with the two types of strategy that lone queens use to found new colonies. In species where queens convert their own wing muscles into the food for the first generation of workers, the wing muscles are much enlarged and the neck segment is extremely reduced. In species where queens hunt to feed the new colony, the wing and neck muscles are more balanced in size. As such, for those ant species where very little is known about how new colonies are founded, Keller et al. show that we can use the shape of the queen’s thorax to help predict this behavior.
Taken together, the results of Keller et al. show that female ants invest in the relative size of the different segments of the thorax in a way that reflects their behavior as adults. These adaptations partly explain why ants have been so extraordinarily successful in nature, and underscore the importance of carefully analyzing an organism’s form to fully understand its biology.
PMCID: PMC3881093  PMID: 24399458
ants; Formicidae; social insects; Other
16.  Mechanism of synergistic activation of Arp2/3 complex by cortactin and N-WASP 
eLife  2013;2:e00884.
Nucleation promoting factors (NPFs) initiate branched actin network assembly by activating Arp2/3 complex, a branched actin filament nucleator. Cellular actin networks contain multiple NPFs, but how they coordinately regulate Arp2/3 complex is unclear. Cortactin is an NPF that activates Arp2/3 complex weakly on its own, but with WASP/N-WASP, another class of NPFs, potently activates. We dissect the mechanism of synergy and propose a model in which cortactin displaces N-WASP from nascent branches as a prerequisite for nucleation. Single-molecule imaging revealed that unlike WASP/N-WASP, cortactin remains bound to junctions during nucleation, and specifically targets junctions with a ∼160-fold increased on rate over filament sides. N-WASP must be dimerized for potent synergy, and targeted mutations indicate release of dimeric N-WASP from nascent branches limits nucleation. Mathematical modeling shows cortactin-mediated displacement but not N-WASP recycling or filament recruitment models can explain synergy. Our results provide a molecular basis for coordinate Arp2/3 complex regulation.
eLife digest
Cells constantly sense, and react to, their environments. They can monitor or alter their surroundings by taking up or secreting various substances, and may also migrate toward food supplies, or toward signaling molecules—for example, to clot blood or heal wounds. These actions depend on the cytoskeleton, a protein meshwork that gives cells their shape; allows them to transport materials into, out of, or across their cytoplasms; and enables them to move.
The filaments of the cytoskeleton are constructed from several different types of proteins, one of which is called actin. In response to signals, actin can assemble into linear filaments, or can form branches with one end anchored on an existing filament. Branch formation requires the Arp2/3 complex, which initiates and anchors branches on existing filaments, and also various ‘nucleation-promoting factors’ (NPFs), which turn on the branching activity of the Arp2/3 complex.
Two types of NPFs have been identified: type I interact with individual actin molecules, while type II bind to actin filaments. Previous work has shown that type I NPFs—including the N-WASP protein—have a specialized domain called VCA that binds to both the Arp2/3 complex and to actin molecules. VCA brings actin molecules to the branch site, which initiates branch formation, but how N-WASP collaborates with type II NPFs to build branches is not well understood.
Helgeson and Nolen now examine how a type II NPF called cortactin works with the Arp2/3 complex and N-WASP to construct new branches on actin filaments in vitro. Cortactin appears to displace the VCA domain of N-WASP to stimulate branch formation, and then to remain associated with—and stabilize—the growing branch. Helgeson and Nolen suggest that these NPFs work together to create branches using an “obligatory displacement” model. According to this scheme, N-WASP (or another type I NPF), the Arp2/3 complex and two actin molecules are bound at the site of a future branch on an actin filament, poised for branch formation. However, before more actin molecules can be added, N-WASP must be released, either slowly on its own—as Smith et al. also report in findings published concurrently in eLife—or rapidly with the help of cortactin or other type II NPFs.
Although the rationale for N-WASP removal is not yet understood, type I NPFs are generally attached to the plasma membrane. When N-WASP releases the mother filament, the membrane should no longer be able to block the addition of actin molecules to a growing branch.
PMCID: PMC3762189  PMID: 24015358
Arp2/3; actin; WASP; cortactin; single molecule; N-WASP; Mouse
17.  Ancient host shifts followed by host conservatism in a group of ant parasitoids 
While ant colonies serve as host to a diverse array of myrmecophiles, few parasitoids are able to exploit this vast resource. A notable exception is the wasp family Eucharitidae, which is the only family of insects known to exclusively parasitize ants. Worldwide, approximately 700 Eucharitidae species attack five subfamilies across the ant phylogeny. Our goal is to uncover the pattern of eucharitid diversification, including timing of key evolutionary events, biogeographic patterns and potential cophylogeny with ant hosts. We present the most comprehensive molecular phylogeny of Eucharitidae to date, including 44 of the 53 genera and fossil-calibrated estimates of divergence dates. Eucharitidae arose approximately 50 Ma after their hosts, during the time when the major ant lineages were already established and diversifying. We incorporate host association data to test for congruence between eucharitid and ant phylogenies and find that their evolutionary histories are more similar than expected at random. After a series of initial host shifts, clades within Eucharitidae maintained their host affinity. Even after multiple dispersal events to the New World and extensive speciation within biogeographic regions, eucharitids remain parasitic on the same ant subfamilies as their Old World relatives, suggesting host conservatism despite access to a diverse novel ant fauna.
PMCID: PMC3619522  PMID: 23554396
Eucharitidae; molecular dating; cophylogenetic reconstruction; diversification
18.  Water Stress Strengthens Mutualism Among Ants, Trees, and Scale Insects 
PLoS Biology  2013;11(11):e1001705.
When water is scarce, trees invest in the moderate carbon cost of supporting defensive ants to avoid the potentially high carbon cost of extremities being eaten.
Abiotic environmental variables strongly affect the outcomes of species interactions. For example, mutualistic interactions between species are often stronger when resources are limited. The effect might be indirect: water stress on plants can lead to carbon stress, which could alter carbon-mediated plant mutualisms. In mutualistic ant–plant symbioses, plants host ant colonies that defend them against herbivores. Here we show that the partners' investments in a widespread ant–plant symbiosis increase with water stress across 26 sites along a Mesoamerican precipitation gradient. At lower precipitation levels, Cordia alliodora trees invest more carbon in Azteca ants via phloem-feeding scale insects that provide the ants with sugars, and the ants provide better defense of the carbon-producing leaves. Under water stress, the trees have smaller carbon pools. A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season. Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism.
Author Summary
The strength of ecological interactions, measured as the costs or benefits sustained by each species, depends on the environmental context in which the interaction occurs. Stressful environmental conditions should favor trading between species that can produce a given resource or service at the lowest cost. Mutualisms, in which both interacting species incur a net benefit, may thus strengthen under stressful conditions. Here we examine an ant–plant mutualism, in which plants provide food and housing for ants and ants defend plants against leaf-eating insects, along a four-fold annual precipitation gradient comprising tropical sites in Mexico and Central America. We show that the strength of the mutualism, in terms of carbon investment by plants and leaf defense by ants, increases as water availability decreases. Carbon shortages are more frequent where water is scarce and increase the risk that plants will die if all of their leaves are eaten by herbivores. Trees appear to invest more in ant defenders when water is scarce to insure themselves against extreme herbivory. Water availability thus indirectly determines the outcomes of this ant–plant mutualism, which suggests that the increasing frequency of extreme climate events in the tropics will have important ecological consequences.
PMCID: PMC3818173  PMID: 24223521
19.  Leaf-cutting ant fungi produce cell wall degrading pectinase complexes reminiscent of phytopathogenic fungi 
BMC Biology  2010;8:156.
Leaf-cutting (attine) ants use their own fecal material to manure fungus gardens, which consist of leaf material overgrown by hyphal threads of the basidiomycete fungus Leucocoprinus gongylophorus that lives in symbiosis with the ants. Previous studies have suggested that the fecal droplets contain proteins that are produced by the fungal symbiont to pass unharmed through the digestive system of the ants, so they can enhance new fungus garden growth.
We tested this hypothesis by using proteomics methods to determine the gene sequences of fecal proteins in Acromyrmex echinatior leaf-cutting ants. Seven (21%) of the 33 identified proteins were pectinolytic enzymes that originated from the fungal symbiont and which were still active in the fecal droplets produced by the ants. We show that these enzymes are found in the fecal material only when the ants had access to fungus garden food, and we used quantitative polymerase chain reaction analysis to show that the expression of six of these enzyme genes was substantially upregulated in the fungal gongylidia. These unique structures serve as food for the ants and are produced only by the evolutionarily advanced garden symbionts of higher attine ants, but not by the fungi reared by the basal lineages of this ant clade.
Pectinolytic enzymes produced in the gongylidia of the fungal symbiont are ingested but not digested by Acromyrmex leaf-cutting ants so that they end up in the fecal fluid and become mixed with new garden substrate. Substantial quantities of pectinolytic enzymes are typically found in pathogenic fungi that attack live plant tissue, where they are known to breach the cell walls to allow the fungal mycelium access to the cell contents. As the leaf-cutting ant symbionts are derived from fungal clades that decompose dead plant material, our results suggest that their pectinolytic enzymes represent secondarily evolved adaptations that are convergent to those normally found in phytopathogens.
PMCID: PMC3022778  PMID: 21194476
20.  Emergence of altruism behavior in army ant-based social evolutionary system 
SpringerPlus  2014;3:712.
Army ants perform the altruism behavior that an ant sacrifices its own well-being for the benefit of another ants. They build bridges using their own bodies along the path from a food to the nest. We developed the army ant inspired social evolutionary system by using Swarm library. The system has 2 kinds of ant agents, ‘Major ant’ and ‘Minor ant’. They communicate with each other via pheromones. Army ant can recognize them as the signals from the other ants. The pheromones evaporate with the certain ratio and diffused into the space of neighbors stochastically. If the optimal bridge is found, the path through the bridge is the shortest route from the food to the nest. We define the probability for an ant to leave a bridge as to the number of neighboring ants. The constructing method of the optimal route has been proposed. In this paper, the behaviors of ant under the environment with two or more feeding spots were observed. Some experimental results show the behaviors of great interest with respect to altruism of ants. The knowledge discovery of social evolutionary process from some computer simulation results is described in this paper.
Electronic supplementary material
The online version of this article (doi:10.1186/2193-1801-3-712) contains supplementary material, which is available to authorized users.
PMCID: PMC4320217
Artificial life simulation system; Army ant; Altruism behavior
21.  Low levels of nestmate discrimination despite high genetic differentiation in the invasive pharaoh ant 
Frontiers in Zoology  2010;7:20.
Ants typically distinguish nestmates from non-nestmates based on the perception of colony-specific chemicals, particularly cuticular hydrocarbons present on the surface of the ants' exoskeleton. These recognition cues are believed to play an important role in the formation of vast so-called supercolonies that have been described for some invasive ant species, but general conclusions about the role of these cues are hampered by only few species being studied. Here we use data on cuticular hydrocarbons, aggression and microsatellite genetic markers to investigate the interdependence of chemical recognition cues, genetic distance and nestmate discrimination in the pharaoh ant (Monomorium pharaonis), a widespread pest species, and ask whether introduced populations of this species are genetically differentiated and exhibit intraspecific aggression.
Microsatellite analyses of a total of 35 colonies from four continents revealed extremely high levels of genetic differentiation between almost all colonies (FST = 0.751 ± 0.006 SE) and very low within-colony diversity. This implies that at least 34 and likely hundreds more independent lineages of this ant have spread worldwide. Aggression tests involving workers from 14 different colonies showed only low levels of aggression, even between colonies that were geographically and/or genetically very distant. Chemical analyses of groups of worker ants showed that all colonies had the same cuticular compounds, which varied only quantitatively among colonies. There was a positive correlation between geographical and genetic distance, but no other significant relationships were detected between aggression, chemical profile, genetic distance and geographical distance.
The pharaoh ant has a global invasion history of numerous independent introductions resulting in genetically highly differentiated colonies typically displaying surprisingly low levels of intraspecific aggression, a behaviour that may have evolved in the native range or by lineage selection in the introduced range.
PMCID: PMC2907370  PMID: 20591186
22.  Weeding and grooming of pathogens in agriculture by ants. 
The ancient mutualism between fungus-growing ants and the fungi they cultivate for food is a textbook example of symbiosis. Fungus-growing ants' ability to cultivate fungi depends on protection of the garden from the aggressive microbes associated with the substrate added to the garden as well as from the specialized virulent garden parasite Escovopsis. We examined ants' ability to remove alien microbes physically by infecting Atta colombica gardens with the generalist pathogen Trichoderma viride and the specialist pathogen Escovopsis. The ants sanitized the garden using two main behaviours: grooming of alien spores from the garden (fungus grooming) and removal of infected garden substrate (weeding). Unlike previously described hygienic behaviours (e.g. licking and self-grooming), fungus-grooming and garden-removal behaviours are specific responses to the presence of fungal pathogens. In the presence of pathogens, they are the primary activities performed by workers, but they are uncommon in uninfected gardens. In fact, workers rapidly eliminate Trichoderma from their gardens by fungus grooming and weeding, suggesting that these behaviours are the primary method of garden defence against generalist pathogens. The same sanitary behaviours were performed in response to the presence of the specialist pathogen Escovopsis. However, the intensity and duration of these behaviours were much greater in this treatment. Despite the increased effort, the ants were unable to eliminate Escovopsis from their gardens, suggesting that this specialized pathogen has evolved counter-adaptations in order to overcome the sanitary defences of the ants.
PMCID: PMC1088705  PMID: 11375087
23.  Caterpillars and Fungal Pathogens: Two Co-Occurring Parasites of an Ant-Plant Mutualism 
PLoS ONE  2011;6(5):e20538.
In mutualisms, each interacting species obtains resources from its partner that it would obtain less efficiently if alone, and so derives a net fitness benefit. In exchange for shelter (domatia) and food, mutualistic plant-ants protect their host myrmecophytes from herbivores, encroaching vines and fungal pathogens. Although selective filters enable myrmecophytes to host those ant species most favorable to their fitness, some insects can by-pass these filters, exploiting the rewards supplied whilst providing nothing in return. This is the case in French Guiana for Cecropia obtusa (Cecropiaceae) as Pseudocabima guianalis caterpillars (Lepidoptera, Pyralidae) can colonize saplings before the installation of their mutualistic Azteca ants. The caterpillars shelter in the domatia and feed on food bodies (FBs) whose production increases as a result. They delay colonization by ants by weaving a silk shield above the youngest trichilium, where the FBs are produced, blocking access to them. This probable temporal priority effect also allows female moths to lay new eggs on trees that already shelter caterpillars, and so to occupy the niche longer and exploit Cecropia resources before colonization by ants. However, once incipient ant colonies are able to develop, they prevent further colonization by the caterpillars. Although no higher herbivory rates were noted, these caterpillars are ineffective in protecting their host trees from a pathogenic fungus, Fusarium moniliforme (Deuteromycetes), that develops on the trichilium in the absence of mutualistic ants. Therefore, the Cecropia treelets can be parasitized by two often overlooked species: the caterpillars that shelter in the domatia and feed on FBs, delaying colonization by mutualistic ants, and the fungal pathogen that develops on old trichilia. The cost of greater FB production plus the presence of the pathogenic fungus likely affect tree growth.
PMCID: PMC3105098  PMID: 21655182
24.  Ecological consequences of interactions between ants and honeydew-producing insects 
Interactions between ants and honeydew-producing hemipteran insects are abundant and widespread in arthropod food webs, yet their ecological consequences are very poorly known. Ant–hemipteran interactions have potentially broad ecological effects, because the presence of honeydew-producing hemipterans dramatically alters the abundance and predatory behaviour of ants on plants. We review several studies that investigate the consequences of ant–hemipteran interactions as ‘keystone interactions’ on arthropod communities and their host plants. Ant–hemipteran interactions have mostly negative effects on the local abundance and species richness of several guilds of herbivores and predators. In contrast, out of the 30 studies that document the effects of ant–hemipteran interactions on plants, the majority (73%) shows that plants actually benefit indirectly from these interactions. In these studies, increased predation or harassment of other, more damaging, herbivores by hemipteran-tending ants resulted in decreased plant damage and/or increased plant growth and reproduction. The ecological consequences of mutualistic interactions between honeydew-producing hemipterans and invasive ants relative to native ants have rarely been studied, but they may be of particular importance owing to the greater abundance, aggressiveness and extreme omnivory of invasive ants. We argue that ant–hemipteran interactions are largely overlooked and underappreciated interspecific interactions that have strong and pervasive effects on the communities in which they are embedded.
PMCID: PMC1685857  PMID: 17148245
ants; hemipterans; mutualism; indirect effects; tritrophic interactions; conditionality
25.  Behavioral Strategies of Phorid Parasitoids and Responses of Their Hosts, the Leaf-Cutting Ants 
Host-searching and oviposition behaviors of parasitoids, and defensive responses of the hosts, are fundamental in shaping the ecology of host-parasitoid interactions. In order to uncover key behavioral features for the little known interactions between phorid parasitoids (Diptera: Phoridae) and their leaf-cutting ant hosts (Formicidae: Attini), host-related behavioral strategies (i.e., host searching and oviposition) for 13 phorid species, and host defensive responses (i.e., hitchhikers and particular body postures) for 11 ant species, were studied. Data was collected at 14 localities, one of them characterized by its high species richness for this host-parasitoid system. Phorid species showed both great variation and specificity in attacking behaviors. Some chose their hosts using either an ambush or an actively searching strategy, while some species attacked ants on different body parts, and specialized on ants performing different tasks, such as when ants were foraging, removing wastes to refuse piles, or repairing the nest. Combining all the behaviors recorded, most phorid species differed in performance in at least one, making it possible to recognize species in the field through their behavior. Phorid species that attacked hosts with greater activity levels showed overall higher attack rates, although there was no significant correlation between attack rates by most phorid species and ant activity outside the nest while parasitoids were attacking. The presence of phorids was a significant determinant for the presence of defensive behaviors by the ants. Although ant species varied in the incidence levels of these defensive behaviors, most ant species reacted against different phorids by utilizing similar behaviors, in contrast to what parasitoids do. General features of the observed phorid-ant interactions were parasitoid specialization and corresponding high interspecific variation in their behaviors, while their hosts showed generalized responses to attacks with high intraspecific variation. Behavioral patterns as well as specific features of these ant-parasitoid interactions are described, and their ecological importance discussed.
PMCID: PMC3658278  PMID: 23448343

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