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1.  The Ecology of Collective Behavior 
PLoS Biology  2014;12(3):e1001805.
Networks of local interactions regulate biological systems. Ecological constraints set by resource distribution, operating costs, and the threat of rupture produce similar collective behavior in ants, cells, and gene transcription.
Similar patterns of interaction, such as network motifs and feedback loops, are used in many natural collective processes, probably because they have evolved independently under similar pressures. Here I consider how three environmental constraints may shape the evolution of collective behavior: the patchiness of resources, the operating costs of maintaining the interaction network that produces collective behavior, and the threat of rupture of the network. The ants are a large and successful taxon that have evolved in very diverse environments. Examples from ants provide a starting point for examining more generally the fit between the particular pattern of interaction that regulates activity, and the environment in which it functions.
doi:10.1371/journal.pbio.1001805
PMCID: PMC3949665  PMID: 24618695
2.  Fast and Flexible: Argentine Ants Recruit from Nearby Trails 
PLoS ONE  2013;8(8):e70888.
Argentine ants (Linepithema humile) live in groups of nests connected by trails to each other and to stable food sources. In a field study, we investigated whether some ants recruit directly from established, persistent trails to food sources, thus accelerating food collection. Our results indicate that Argentine ants recruit nestmates to food directly from persistent trails, and that the exponential increase in the arrival rate of ants at baits is faster than would be possible if recruited ants traveled from distant nests. Once ants find a new food source, they walk back and forth between the bait and sometimes share food by trophallaxis with nestmates on the trail. Recruiting ants from nearby persistent trails creates a dynamic circuit, like those found in other distributed systems, which facilitates a quick response to changes in available resources.
doi:10.1371/journal.pone.0070888
PMCID: PMC3743883  PMID: 23967129
3.  Harvester Ant Colony Variation in Foraging Activity and Response to Humidity 
PLoS ONE  2013;8(5):e63363.
Collective behavior is produced by interactions among individuals. Differences among groups in individual response to interactions can lead to ecologically important variation among groups in collective behavior. Here we examine variation among colonies in the foraging behavior of the harvester ant, Pogonomyrmex barbatus. Previous work shows how colonies regulate foraging in response to food availability and desiccation costs: the rate at which outgoing foragers leave the nest depends on the rate at which foragers return with food. To examine how colonies vary in response to humidity and in foraging rate, we performed field experiments that manipulated forager return rate in 94 trials with 17 colonies over 3 years. We found that the effect of returning foragers on the rate of outgoing foragers increases with humidity. There are consistent differences among colonies in foraging activity that persist from year to year.
doi:10.1371/journal.pone.0063363
PMCID: PMC3662670  PMID: 23717415
4.  The Dynamics of Foraging Trails in the Tropical Arboreal Ant Cephalotes goniodontus 
PLoS ONE  2012;7(11):e50472.
The foraging behavior of the arboreal turtle ant, Cephalotes goniodontus, was studied in the tropical dry forest of western Mexico. The ants collected mostly plant-derived food, including nectar and fluids collected from the edges of wounds on leaves, as well as caterpillar frass and lichen. Foraging trails are on small pieces of ephemeral vegetation, and persist in exactly the same place for 4–8 days, indicating that food sources may be used until they are depleted. The species is polydomous, occupying many nests which are abandoned cavities or ends of broken branches in dead wood. Foraging trails extend from trees with nests to trees with food sources. Observations of marked individuals show that each trail is travelled by a distinct group of foragers. This makes the entire foraging circuit more resilient if a path becomes impassable, since foraging in one trail can continue while a different group of ants forms a new trail. The colony’s trails move around the forest from month to month; from one year to the next, only one colony out of five was found in the same location. There is continual searching in the vicinity of trails: ants recruited to bait within 3 bifurcations of a main foraging trail within 4 hours. When bait was offered on one trail, to which ants recruited, foraging activity increased on a different trail, with no bait, connected to the same nest. This suggests that the allocation of foragers to different trails is regulated by interactions at the nest.
doi:10.1371/journal.pone.0050472
PMCID: PMC3509047  PMID: 23209749
5.  Harvester ants use interactions to regulate forager activation and availability 
Animal behaviour  2013;86(1):197-207.
Social groups balance flexibility and robustness in their collective response to environmental changes using feedback between behavioural processes that operate at different timescales. Here we examine how behavioural processes operating at two timescales regulate the foraging activity of colonies of the harvester ant, Pogonomyrmex barbatus, allowing them to balance their response to food availability and predation. Previous work showed that the rate at which foragers return to the nest with food influences the rate at which foragers leave the nest. To investigate how interactions inside the nest link the rates of returning and outgoing foragers, we observed outgoing foragers inside the nest in field colonies using a novel observation method. We found that the interaction rate experienced by outgoing foragers inside the nest corresponded to forager return rate, and that the interactions of outgoing foragers were spatially clustered. Activation of a forager occurred on the timescale of seconds: a forager left the nest 3–8 s after a substantial increase in interactions with returning foragers. The availability of outgoing foragers to become activated was adjusted on the timescale of minutes: when forager return was interrupted for more than 4–5 min, available foragers waiting near the nest entrance went deeper into the nest. Thus, forager activation and forager availability both increased with the rate at which foragers returned to the nest. This process was checked by negative feedback between forager activation and forager availability. Regulation of foraging activation on the timescale of seconds provides flexibility in response to fluctuations in food abundance, whereas regulation of forager availability on the timescale of minutes provides robustness in response to sustained disturbance such as predation.
doi:10.1016/j.anbehav.2013.05.012
PMCID: PMC3767282  PMID: 24031094
collective behaviour; complex system; flexibility; foraging; interaction rate; Pogonomyrmex barbatus; regulation; robustness; temporal dynamics; timescale
6.  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.
doi:10.1371/journal.pbio.1001705
PMCID: PMC3818173  PMID: 24223521
7.  Nest site and weather affect the personality of harvester ant colonies 
Behavioral Ecology  2012;23(5):1022-1029.
Environmental conditions and physical constraints both influence an animal's behavior. We investigate whether behavioral variation among colonies of the black harvester ant, Messor andrei, remains consistent across foraging and disturbance situations and ask whether consistent colony behavior is affected by nest site and weather. We examined variation among colonies in responsiveness to food baits and to disturbance, measured as a change in numbers of active ants, and in the speed with which colonies retrieved food and removed debris. Colonies differed consistently, across foraging and disturbance situations, in both responsiveness and speed. Increased activity in response to food was associated with a smaller decrease in response to alarm. Speed of retrieving food was correlated with speed of removing debris. In all colonies, speed was greater in dry conditions, reducing the amount of time ants spent outside the nest. While a colony occupied a certain nest site, its responsiveness was consistent in both foraging and disturbance situations, suggesting that nest structure influences colony personality.
doi:10.1093/beheco/ars066
PMCID: PMC3431114  PMID: 22936841
behavioral syndromes; collective behavior; harvester ant; Messor andrei; nest structure; personality; plasticity; social insects; temperament
8.  Does an ecological advantage produce the asymmetric lineage ratio in a harvester ant population? 
Oecologia  2013;173(3):849-857.
In dependent-lineage harvester ant populations, two lineages interbreed but are genetically distinct. The offspring of a male and queen of the same lineage are female reproductives; the offspring of a male and queen of different lineages are workers. Geographic surveys have shown asymmetries in the ratio of the two lineages in many harvester ant populations, which may be maintained by an ecological advantage to one of the lineages. Using census data from a long-term study of a dependent-lineage population of the red harvester ant, Pogonomyrmex barbatus, we identified the lineage of 130 colonies sampled in 1997–1999, ranging in age from 1 to 19 years when collected, and 268 colonies sampled in 2010, ranging in age from 1 to 28 years when collected. The ratio of lineages in the study population is similar across an 11-year interval, 0.59 J2 in 1999 and 0.66 J2 in 2010. The rare lineage, J1, had a slightly but significantly higher number of mates of the opposite lineage than the common lineage, J2, and, using data from previous work on reproductive output, higher male production. Mature colonies of the two lineages did not differ in nest mound size, foraging activity, or the propensity to relocate their nests. There were no strong differences in the relative recruitment or survivorship of the two lineages. Our results show no ecological advantage for either lineage, indicating that differences between the lineages in sex ratio allocation may be sufficient to maintain the current asymmetry of the lineage ratio in this population.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-013-2690-z) contains supplementary material, which is available to authorized users.
doi:10.1007/s00442-013-2690-z
PMCID: PMC3824609  PMID: 23715745
Skewed lineage ratio; Pogonomyrmex; Sex ratio
9.  Interactions with Combined Chemical Cues Inform Harvester Ant Foragers' Decisions to Leave the Nest in Search of Food 
PLoS ONE  2013;8(1):e52219.
Social insect colonies operate without central control or any global assessment of what needs to be done by workers. Colony organization arises from the responses of individuals to local cues. Red harvester ants (Pogonomyrmex barbatus) regulate foraging using interactions between returning and outgoing foragers. The rate at which foragers return with seeds, a measure of food availability, sets the rate at which outgoing foragers leave the nest on foraging trips. We used mimics to test whether outgoing foragers inside the nest respond to the odor of food, oleic acid, the odor of the forager itself, cuticular hydrocarbons, or a combination of both with increased foraging activity. We compared foraging activity, the rate at which foragers passed a line on a trail, before and after the addition of mimics. The combination of both odors, those of food and of foragers, is required to stimulate foraging. The addition of blank mimics, mimics coated with food odor alone, or mimics coated with forager odor alone did not increase foraging activity. We compared the rates at which foragers inside the nest interacted with other ants, blank mimics, and mimics coated with a combination of food and forager odor. Foragers inside the nest interacted more with mimics coated with combined forager/seed odors than with blank mimics, and these interactions had the same effect as those with other foragers. Outgoing foragers inside the nest entrance are stimulated to leave the nest in search of food by interacting with foragers returning with seeds. By using the combined odors of forager cuticular hydrocarbons and of seeds, the colony captures precise information, on the timescale of seconds, about the current availability of food.
doi:10.1371/journal.pone.0052219
PMCID: PMC3540075  PMID: 23308106
10.  The Regulation of Ant Colony Foraging Activity without Spatial Information 
PLoS Computational Biology  2012;8(8):e1002670.
Many dynamical networks, such as the ones that produce the collective behavior of social insects, operate without any central control, instead arising from local interactions among individuals. A well-studied example is the formation of recruitment trails in ant colonies, but many ant species do not use pheromone trails. We present a model of the regulation of foraging by harvester ant (Pogonomyrmex barbatus) colonies. This species forages for scattered seeds that one ant can retrieve on its own, so there is no need for spatial information such as pheromone trails that lead ants to specific locations. Previous work shows that colony foraging activity, the rate at which ants go out to search individually for seeds, is regulated in response to current food availability throughout the colony's foraging area. Ants use the rate of brief antennal contacts inside the nest between foragers returning with food and outgoing foragers available to leave the nest on the next foraging trip. Here we present a feedback-based algorithm that captures the main features of data from field experiments in which the rate of returning foragers was manipulated. The algorithm draws on our finding that the distribution of intervals between successive ants returning to the nest is a Poisson process. We fitted the parameter that estimates the effect of each returning forager on the rate at which outgoing foragers leave the nest. We found that correlations between observed rates of returning foragers and simulated rates of outgoing foragers, using our model, were similar to those in the data. Our simple stochastic model shows how the regulation of ant colony foraging can operate without spatial information, describing a process at the level of individual ants that predicts the overall foraging activity of the colony.
Author Summary
Social insect colonies operate without any central control. Their collective behavior arises from local interactions among individuals. Here we present a simple stochastic model of the regulation of foraging by harvester ant (Pogonomyrmex barbatus) colonies, which forage for scattered seeds that one ant can retrieve on its own, so there is no need for pheromone trails to specific locations. Previous work shows that colony foraging activity is regulated in response to current food availability, using the rate of brief antennal contacts inside the nest between foragers returning with food and outgoing foragers. Our feedback-based algorithm estimates the effect of each returning forager on the rate at which foragers leave the nest. The model shows how the regulation of ant colony foraging can operate without spatial information, describing a process at the level of individual ants that predicts the overall foraging activity of the colony.
doi:10.1371/journal.pcbi.1002670
PMCID: PMC3426560  PMID: 22927811
11.  Colony variation in the collective regulation of foraging by harvester ants 
Behavioral Ecology  2011;22(2):429-435.
This study investigates variation in collective behavior in a natural population of colonies of the harvester ant, Pogonomyrmex barbatus. Harvester ant colonies regulate foraging activity to adjust to current food availability; the rate at which inactive foragers leave the nest on the next trip depends on the rate at which successful foragers return with food. This study investigates differences among colonies in foraging activity and how these differences are associated with variation among colonies in the regulation of foraging. Colonies differ in the baseline rate at which patrollers leave the nest, without stimulation from returning ants. This baseline rate predicts a colony's foraging activity, suggesting there is a colony-specific activity level that influences how quickly any ant leaves the nest. When a colony's foraging activity is high, the colony is more likely to regulate foraging. Moreover, colonies differ in the propensity to adjust the rate of outgoing foragers to the rate of forager return. Naturally occurring variation in the regulation of foraging may lead to variation in colony survival and reproductive success.
doi:10.1093/beheco/arq218
PMCID: PMC3071749  PMID: 22479133
behavioral reaction norm; behavioral syndrome; individual variation
12.  Chemical Defense by the Native Winter Ant (Prenolepis imparis) against the Invasive Argentine Ant (Linepithema humile) 
PLoS ONE  2011;6(4):e18717.
The invasive Argentine ant (Linepithema humile) is established worldwide and displaces native ant species. In northern California, however, the native winter ant (Prenolepis imparis) persists in invaded areas. We found that in aggressive interactions between the two species, P. imparis employs a potent defensive secretion. Field observations were conducted at P. imparis nest sites both in the presence and absence of L. humile. These observations suggested and laboratory assays confirmed that P. imparis workers are more likely to secrete when outnumbered by L. humile. Workers of P. imparis were also more likely to secrete near their nest entrances than when foraging on trees. One-on-one laboratory trials showed that the P. imparis secretion is highly lethal to L. humile, causing 79% mortality. The nonpolar fraction of the secretion was chemically analyzed with gas chromatography/mass spectrometry, and found to be composed of long-chain and cyclic hydrocarbons. Chemical analysis of dissected P. imparis workers showed that the nonpolar fraction is derived from the Dufour's gland. Based on these conclusions, we hypothesize that this chemical defense may help P. imparis to resist displacement by L. humile.
doi:10.1371/journal.pone.0018717
PMCID: PMC3079705  PMID: 21526231
13.  The effect of individual variation on the structure and function of interaction networks in harvester ants 
Social insects exhibit coordinated behaviour without central control. Local interactions among individuals determine their behaviour and regulate the activity of the colony. Harvester ants are recruited for outside work, using networks of brief antennal contacts, in the nest chamber closest to the nest exit: the entrance chamber. Here, we combine empirical observations, image analysis and computer simulations to investigate the structure and function of the interaction network in the entrance chamber. Ant interactions were distributed heterogeneously in the chamber, with an interaction hot-spot at the entrance leading further into the nest. The distribution of the total interactions per ant followed a right-skewed distribution, indicating the presence of highly connected individuals. Numbers of ant encounters observed positively correlated with the duration of observation. Individuals varied in interaction frequency, even after accounting for the duration of observation. An ant's interaction frequency was explained by its path shape and location within the entrance chamber. Computer simulations demonstrate that variation among individuals in connectivity accelerates information flow to an extent equivalent to an increase in the total number of interactions. Individual variation in connectivity, arising from variation among ants in location and spatial behaviour, creates interaction centres, which may expedite information flow.
doi:10.1098/rsif.2011.0059
PMCID: PMC3177612  PMID: 21490001
agent-based model; movement pattern; network analysis; Pogonomyrmex barbatus; spatial behaviour; weighted degree
14.  The devil to pay: a cost of mutualism with Myrmelachista schumanni ants in ‘devil's gardens’ is increased herbivory on Duroia hirsuta trees 
‘Devil's gardens’ are nearly pure stands of the myrmecophyte, Duroia hirsuta, that occur in Amazonian rainforests. Devil's gardens are created by Myrmelachista schumanni ants, which nest in D. hirsuta trees and kill other plants using formic acid as an herbicide. Here, we show that this ant–plant mutualism has an associated cost; by making devil's gardens, M. schumanni increases herbivory on D. hirsuta. We measured standing leaf herbivory on D. hirsuta trees and found that they sustain higher herbivory inside than outside devil's gardens. We also measured the rate of herbivory on nursery-grown D. hirsuta saplings planted inside and outside devil's gardens in ant-exclusion and control treatments. We found that when we excluded ants, herbivory on D. hirsuta was higher inside than outside devil's gardens. These results suggest that devil's gardens are a concentrated resource for herbivores. Myrmelachista schumanni workers defend D. hirsuta against herbivores, but do not fully counterbalance the high herbivore pressure in devil's gardens. We suggest that high herbivory may limit the spread of devil's gardens, possibly explaining why devil's gardens do not overrun Amazonian rainforests.
doi:10.1098/rspb.2006.0415
PMCID: PMC2124481  PMID: 17301016
ant–plant interactions; density dependence; diminishing returns; Janzen–Connell hypothesis; pure stands; resource concentration hypothesis

Results 1-14 (14)