Veromessor Pergandei Research Articles

Tissue dependence of variation in metabolic rates of harvester ants

Metabolic rates vary tremendously among individuals and across species, and the causes of this variation remain controversial and challenging to identify. We utilized an Agilent Seahorse system to measure the metabolic rates of brains, flight muscles, leg muscles, jaw muscles, digestive tract, fat and reproductive organs of harvester ants of different species, sex and caste, and compared these to whole body metabolic rates. Across Pogonomyrmex species varying an order of magnitude in body size, mass-specific brain metabolic rates declined dramatically in larger species, such that the brain accounted for 43% of whole body metabolism in the smallest species and 14% in the largest. In Veromessor pergandei, males have much higher mass-specific metabolic rates than queens or workers, with queens being slightly higher than workers. The tissue specific bases to metabolic rates varied with sex and caste. Males are "flying gonads", with flight muscle, fat and gonads accounting for 44, 25 and 20%, respectively, of resting metabolic rate, and tissue-specific rates were generally higher in males than females. For queens, which have by far the largest fat content, the fat body contributes the largest fraction of the total tissue metabolic rate (38%), with flight muscle, femoral muscle, brain and gut each contributing 13 – 15% of total cost. For workers, brains are the most important contributors to total tissue metabolic rate (38%), followed by fat body (24%) and gut (19%). Together these results demonstrate that variation in whole body metabolic rate within and across closely related species is strongly affected by size, sex and caste-specific differences in tissue function, likely associated with life history variation. Supported by NSF IOS-1953419. This is the full abstract presented at the American Physiology Summit 2024 meeting and is only available in HTML format. There are no additional versions or additional content available for this abstract. Physiology was not involved in the peer review process.

Route retracing: way pointing and multiple vector memories in trail-following ants.

Maintaining positional estimates of goal locations is a fundamental task for navigating animals. Diverse animal groups, including both vertebrates and invertebrates, can accomplish this through path integration. During path integration, navigators integrate movement changes, tracking both distance and direction, to generate a spatial estimate of their start location, or global vector, allowing efficient direct return travel without retracing the outbound route. In ants, path integration is accomplished through the coupling of pedometer and celestial compass estimates. Within path integration, it has been theorized navigators may use multiple vector memories for way pointing. However, in many instances, these navigators may instead be homing via view alignment. Here, we present evidence that trail-following ants can attend to segments of their global vector to retrace their non-straight pheromone trails, without the confound of familiar views. Veromessor pergandei foragers navigate to directionally distinct intermediate sites via path integration by orienting along separate legs of their inbound route at unfamiliar locations, indicating these changes are not triggered by familiar external cues, but by vector state. These findings contrast with path integration as a singular memory estimate in ants and underscore the system's ability to way point to intermediate goals along the inbound route via multiple vector memories, akin to trapline foraging in bees visiting multiple flower patches. We discuss how reliance on non-straight pheromone-marked trails may support attending to separate vectors to remain on the pheromone rather than attempting straight-line shortcuts back to the nest.

Role of the pheromone for navigation in the group foraging ant, Veromessor pergandei.

Navigation is comprised of a variety of strategies which rely on multiple external cues to shape a navigator's behavioral output. Here, we explored in the ant Veromessor pergandei, the interactions between the information provided by the pheromone trail and the home vector guided by the celestial compass. We found that a cross sensory interaction between the pheromone cue and the path integrator underlies correct orientation during the inbound journey. The celestial compass provides directional information, while the presence of the trail pheromone acts as a critical context cue, triggering distinct behaviors (vector orientation, search, and backtracking). While exposed to the pheromone, foragers orient to the vector direction regardless of vector state, while in the pheromone's absence, the current remaining vector determines the forager's navigational behavior. This interaction also occurs in foragers with no remaining path integrator, relying on the activation of a celestial compass-based memory of the previous trip. Such cue interactions maximize the foragers' return to the nest and inhibit movement off the pheromone trail. Finally, our manipulations continuously rotated foragers away from their desired heading, yet foragers were proficient at counteracting these changes, steering to maintain a correct compass heading even at rotational speeds of ~ 40°/s.

Desiccation limits recruitment in the pleometrotic desert seed-harvester ant Veromessor pergandei.

The desert harvester ant Veromessor pergandei displays geographic variation in colony founding with queens initiating nests singly (haplometrosis) or in groups (pleometrosis). The transition from haplo‐ to pleometrotic founding is associated with lower rainfall. Numerous hypotheses have been proposed to explain the evolution of cooperative founding in this species, but the ultimate explanation remains unanswered. In laboratory experiments, water level was positively associated with survival, condition, and brood production by single queens. Queen survival also was positively influenced by water level and queen number in a two‐factor experiment. Water level also was a significant effect for three measures of queen condition, but queen number was not significant for any measure. Foundress queens excavated after two weeks of desiccating conditions were dehydrated compared to alate queens captured from their natal colony, indicating that desiccation can be a source of queen mortality. Long‐term monitoring in central Arizona, USA, documented that recruitment only occurred in four of 20 years. A discriminant analysis using rainfall as a predictor of recruitment correctly predicted recruitment in 17 of 20 years for total rainfall from January to June (the period for mating flights and establishment) and in 19 of 20 years for early plus late rainfall (January–March and April–June, respectively), often with a posterior probability > 0.90. Moreover, recruitment occurred only in years in which both early and late rainfall exceeded the long‐term mean. This result also was supported by the discriminant analysis predicting no recruitment when long‐term mean early and late rainfall were included as ungrouped periods. These data suggest that pleometrosis in V. pergandei evolved to enhance colony survival in areas with harsh abiotic (desiccating) conditions, facilitating colonization of habitats in which solitary queens could not establish even in wet years. This favorable‐year hypothesis supports enhanced worker production as the primary advantage of pleometrosis.

Pheromone cue triggers switch between vectors in the desert harvest ant, Veromessor pergandei.

The desert harvester ant (Veromessor pergandei) employs a mixture of social and individual navigational strategies at separate stages of their foraging trip. Individuals leave the nest along a pheromone-based column, travelling 3-40m before spreading out to forage individually in a fan. Foragers use path integration while in this fan, accumulating a direction and distance estimate (vector) to return to the end of the column (column head), yet foragers' potential use of path integration in the pheromone-based column is less understood. Here we show foragers rely on path integration both in the foraging fan and while in the column to return to the nest, using separate vectors depending on their current foraging stage in the fan or column. Returning foragers displaced while in the fan oriented and travelled to the column head location while those displaced after reaching the column travel in the nest direction, signifying the maintenance of a two-vector system with separate fan and column vectors directing a forager to two separate spatial locations. Interestingly, the trail pheromone and not the surrounding terrestrial cues mediate use of these distinct vectors, as fan foragers briefly exposed to the pheromone cues of the column in isolation altered their paths to a combination of the fan and column vectors. The pheromone acts as a contextual cue triggering both the retrieval of the column-vector memory and its integration with the forager's current fan-vector.

Ants Sense, and Follow, Trail Pheromones of Ant Community Members.

Ants deposit trail pheromones that guide nestmates to food sources. We tested the hypotheses that ant community members (Western carpenter ants, Camponotus modoc; black garden ants, Lasius niger; European fire ants, Myrmica rubra) (1) sense, and follow, each other’s trail pheromones, and (2) fail to recognize trail pheromones of allopatric ants (pavement ants, Tetramorium caespitum; desert harvester ants, Novomessor albisetosus; Argentine ants, Linepithema humilis). In gas chromatographic-electroantennographic detection analyses of a six-species synthetic trail pheromone blend (6-TPB), La. niger, Ca. modoc, and M. rubra sensed the trail pheromones of all community members and unexpectedly that of T. caespitum. Except for La. niger, all species did not recognize the trail pheromones of N. albisetosus and Li. humilis. In bioassays, La. niger workers followed the 6-TPB trail for longer distances than their own trail pheromone, indicating an additive effect of con- and hetero-specific pheromones on trail-following. Moreover, Ca. modoc workers followed the 6-TPB and their own trail pheromones for similar distances, indicating no adverse effects of heterospecific pheromones on trail-following. Our data show that ant community members eavesdrop on each other’s trail pheromones, and that multiple pheromones can be combined in a lure that guides multiple species of pest ants to lethal food baits.

Same but different: Socially foraging ants backtrack like individually foraging ants but use different mechanisms

Diverse species may adopt behaviourally identical solutions to similar environmental challenges. However, the underlying mechanisms dictating these responses may be quite different and are often associated with the specific ecology or habitat of these species. Foraging desert ants use multiple strategies in order to successfully navigate. In individually foraging ants, these strategies are largely visually-based; this includes path integration and learned panorama cues, with systematic search and backtracking acting as backup mechanisms. Backtracking is believed to be controlled, at least in solitary foraging species, by three criteria: 1) foragers must have recent exposure to the nest panorama, 2) the path integrator must be near zero, and 3) the ant must be displaced to an unfamiliar location. Instead of searching for the nest, under these conditions, foragers head in the opposite compass direction of the one in which they were recently travelling. Here, we explore backtracking in the socially foraging desert harvester ant (Veromessor pergandei), which exhibits a foraging ecology consisting of a combination of social and individual cues in a column and fan structure. We find that backtracking in V. pergandei, similar to solitary foraging species, is dependent on celestial cues, and in particular on the sun’s position. However, unlike solitary foraging species, backtracking in V. pergandei is not mediated by the same criteria. Instead the expression of this behaviour is dependent on the presence of the social cues of the column and the proportion of the column that foragers have completed prior to displacement.

Not just going with the flow: foraging ants attend to polarised light even while on the pheromone trail.

The polarisation pattern of skylight serves as an orientation cue for many invertebrates. Solitary foraging ants, in particular, rely on polarised light to orient along with a number of other visual cues. Yet it is unknown, if this cue is actively used in socially foraging species that use pheromone trails to navigate. Here, we explore the use of polarised light in the presence of the pheromone cues of the foraging trail. The desert harvester ant, Veromessor pergandei, relies on pheromone cues and path integration in separate stages of their foraging ecology (column and fan, respectively). Here, we show that foragers actively orient to an altered overhead polarisation pattern, both while navigating individually in the fan and while on the pheromone-based column. These heading changes occurred during twilight, as well as in the early morning and late afternoon before sunset. Differences in shift size indicate that foragers attend to both the polarisation pattern and the sun's position when available, yet during twilight, headings are dominated by the polarisation pattern. Finally, when the sun's position was experimentally blocked before sunset, shift sizes increased similar to twilight testing. These findings show that celestial cues provide directional information on the pheromone trail.

Destruction of Spiderwebs and Rescue of Ensnared Nestmates by a Granivorous Desert Ant (Veromessor pergandei).

Prey species rarely seek out and dismantle traps constructed by their predators. In the current study, we report an instance of targeted trap destruction by an invertebrate and a novel context for rescue behavior. We found that foragers of the granivorous desert ant (Veromessor pergandei) identify and cooperatively dismantle spiderwebs (Araneae: Theridiidae, Steatoda spp., and Asagena sp.) During group foraging, workers ensnared in webs are recovered by sisters, which transport them to the nest and groom away their silk bindings. The presence of an ensnared nestmate and chemical alarm signal significantly increased the probability of web removal and nestmate retrieval. A subset of larger-bodied foragers participated in web removal, and 6.3% became tangled or were captured by spiders. Most animals that perform rescue behavior live in small groups, but V. pergandei colonies include tens of thousands of short-lived workers. To maintain their size, large colonies must collect enough seeds to produce 650 new ants each day. We hypothesize that the removal of spiderwebs allows for an unimpeded income of seeds on a single foraging path during a brief daily temperature window. Despite the cost to individuals, webs are recognized and removed only when workers are captured in them.

Odometry and backtracking: social and individual navigation in group foraging desert harvester ants (Veromessor pergandei).

Veromessor pergandei harvester ants are group foragers which use a combination of social cues (pheromone-marked columns) and individual cues (e.g., self-generated movement, visual cues) when exploring foraging areas for resources. Upon finding food, individuals navigate back to the column, which guides their return to the nest. The direction and length of columns change between foraging bouts, and hence the end of the column (unlike the nest location) is non-stationary. We conducted displacement tests on returning foragers and present three novel findings. First, returning individual ants accurately estimate their distance from the foraging area to the end of the column. Second, ants that reached the column but only traveled a small proportion of the distance to the nest either show homeward or random orientation; random orientation was seen when the column was long. Third, ants that have traveled most of the way back to the nest along the column show backtracking when they are displaced-orienting in the direction opposite to the nest-similar to Australian desert ants Melophorus bagoti. This commonality suggests that some navigation strategies are general across species, and are utilized by ants that navigate individually or socially.

The non-additive effects of body size on nest architecture in a polymorphic ant.

Like traditional organisms, eusocial insect societies express traits that are the target of natural selection. Variation at the colony level emerges from the combined attributes of thousands of workers and may yield characteristics not predicted from individual phenotypes. By manipulating the ratios of worker types, the basis of complex, colony-level traits can be reduced to the additive and non-additive interactions of their component parts. In this study, we investigated the independent and synergistic effects of body size on nest architecture in a seasonally polymorphic harvester ant, Veromessor pergandei Using network analysis, we compared wax casts of nests, and found that mixed-size groups built longer nests, excavated more sand and produced greater architectural complexity than single-sized worker groups. The nests built by polymorphic groups were not only larger in absolute terms, but larger than expected based on the combined contributions of both size classes in isolation. In effect, the interactions of different worker types yielded a colony-level trait that was not predicted from the sum of its parts. In nature, V. pergandei colonies with fewer fathers produce smaller workers each summer, and produce more workers annually. Because body size is linked to multiple colony-level traits, our findings demonstrate how selection acting on one characteristic, like mating frequency, could also shape unrelated characteristics, like nest architecture.This article is part of the theme issue 'Interdisciplinary approaches for uncovering the impacts of architecture on collective behaviour'.

The ecological and genetic basis of annual worker production in the desert seed harvesting ant, Veromessor pergandei

Colony size is an important predictor of annual survival and reproduction in social insects. By tracking monthly forager turn over, we measured the size-specific production rates necessary to counteract forager mortality in wild Veromessor pergandei colonies. Between 31,180 and 237,980 individuals appeared as foragers annually, representing an eightfold difference in production between neighboring nests. Highly productive colonies housed 26,000 foragers at one time, turned over 34,000 foragers in a single month, and produced 470 g of worker biomass during the year. Each forager population turned over approximately 20 times during the year, cumulatively returning 3.4 kg of biomass per hectare (with 14 nests per hectare). Forager longevity was not influenced by forager number, season, or pressure from neighboring conspecifics. Genotyping at three microsatellite loci revealed that all colonies contained a single queen and one to seven patrilines (mean m observed = 3.8; m e = 2.56). The most productive colonies had significantly fewer patrilines, a larger peak forager population, and a larger annual foraging range. Colonies varied in their ability to replace lost workers, adding anywhere from 2 to 42 new foragers per death during peak forager allocation. Seasonal increases in forager population size corresponded to decreases in worker body size, suggesting a trade-off during production earlier in the year. Together, these findings demonstrate how the combination of individual colony-member characteristics influence whole colony survival across multiple years. The survival of an animal society can depend on its size and stability. We measured the seasonal relationships between mortality and production of new colony members, with respect to foraging range size, paternity, neighbor pressure, and body size in a desert seed harvesting ant. Mortality rate was stable across seasons, but the ability of colonies to replace dead individuals corresponded to increased foraging range size, decreased patriline number, and seasonal decreases in body size. Our findings reveal the characteristics that allow colonies to respond to worker mortality on an annual scale.

Social selection and the evolution of a female weapon in queens of the antMessor pergandei(Hymenoptera: Formicidae)

The evolution of weaponry occurs less frequently in females than in males and is most often important for protecting ecological resources or offspring rather than winning mates. The purpose of female weapons is often confounded by the presence of similar weapons in males, so cases where only females need weapons provide important tests of our understanding of how and why weapons evolve. In some populations of the ant, Messor pergandei (Mayr), newly mated queens initiate new nests in social groups that subsequently break down when queens engage in battles for control. The incipient social environment differs geographically, so that lethal fighting occurs in some populations but not others. Consistent with the hypothesis that queens in populations where lethal fighting occurs should show selection for weaponry (broad heads and strong mandibles), we found that heads of queens from sites where lethal fighting occurs were broader than those at sites with non-fighting queens and a site with solitary queens. Evolution of weaponry is specific to queens, because regression results from workers often did not follow this pattern.

Variation in social structure alters queen body mass and productivity in the desert seed-harvester ant Messor pergandei

Parent–offspring conflict theory predicts conflict between parents and their offspring over per-offspring resource investment. Across the range of the desert seed-harvester ant, Messor pergandei, daughter queens use three different social strategies during colony founding that are expected to alter the optimal level of parental investment. To test whether social strategy variation is associated with shifts in body mass, we surveyed queen live mass over 3 years at 25 sites that spanned the range of behavioral strategies and founding group sizes. To test whether reduction in parental investment into individual offspring negatively impacts their productivity, queens were individually isolated and allowed to produce a single worker cohort under common garden conditions. Queen live mass was highly variable, from 24 mg on average at the site with the lightest queens to 1.5 times that size, 37 mg, at the site with the heaviest queens. As predicted by parent–offspring conflict over investment, solitary colony founding sites contained the heaviest queens, followed by secondary monogyny. Polygynous queens were lightest, with a strong negative relationship between group size and live mass. Reductions in body mass had a negative effect on queen productivity across all queen social types; however, queens from sites where queen–queen aggression is typical were significantly more efficient at brood rearing, resulting in lower mass loss during founding per unit offspring biomass. This may represent an adaptation to queen competition to gain a strength advantage over potential rivals.

Altered nitrogen and precipitation along urban gradients affect harvester ants and seed sources

We investigated the effects of nitrogen deposition and precipitation on Messor pergandei (Mayr) harvester ants and plants to identify alterations in the desert food web in California. We measured ant colony attributes and shrub fruit densities, as well as nitrogen and carbon concentrations and stable isotopes, at 18 sites along a nitrogen deposition gradient. Ant nest density increased from low to high deposition sites; however, ant nest mound size and the density of abandoned nests decreased as deposition increased. Nest mound size was positively correlated with the size and age of the colony; therefore, these results suggest that colonization has been more frequent with increased inter-colony competition in areas of high deposition. Nitrogen and carbon isotope values of perennial plant leaves and seeds, annual plant seeds, and ants were significantly enriched in the heavy isotopes from low to high nitrogen deposition regions, indicating the possibility of plants assimilating different sources of both elements, including anthropogenically-produced compounds. Plant carbon isotope discrimination also differed with the decrease in precipitation across the gradient. Considering that deserts are limited by both nitrogen and precipitation, our results suggest that altered nitrogen inputs in conjunction with precipitation may result in cascading effects through trophic levels and drive arid ecosystem change.

Chemical communication during foraging in the harvesting ants Messor pergandei and Messor andrei

We combined behavioral analyses in the laboratory and field to investigate chemical communication in the formation of foraging columns in two Nearctic seed harvesting ants, Messor pergandei and Messor andrei. We demonstrate that both species use poison gland secretions to lay recruitment trails. In M. pergandei, the recruitment effect of the poison gland is enhanced by adding pygidial gland secretions. The poison glands of both species contain 1-phenyl ethanol. Minute quantities (3μl of a 0.1ppm solution) of 1-phenyl ethanol drawn out along a 40cm long trail released trail following behavior in M. pergandei, while M. andrei required higher concentrations (0.5-1ppm). Messor pergandei workers showed weak trail following to 5ppm trails of the pyrazines 2,5-dimethylpyrazine and 2,3,5-trimethylpyrazine, whereas M. andrei workers showed no behavioral response. Minute quantities of pyrazines were detected in M. pergandei but not in M. andrei poison glands using single ion monitoring gas chromatography-mass spectrometry.

An empirically based simulation of group foraging in the harvesting ant, Messor pergandei

We present an empirically based group model of foraging interactions in Messor pergandei, the Sonoran desert harvesting ant. M. pergandei colonies send out daily foraging columns consisting of tens of thousands of individual ants. Each day, the directions of the columns may change depending on the resource availability and the neighbor interactions. If neighboring columns meet, ants fight, and subsequent foraging is suppressed. M. pergandei colonies face a general problem which is present in many systems: dynamic spatial partitioning in a constantly changing environment, while simultaneously minimizing negative competitive interactions with multiple neighbors.Our simulation model of a population of column foragers is spatially explicit and includes neighbor interactions. We study how different behavioral strategies influence resource exploitation and space use for different nest distributions and densities. Column foraging in M. pergandei is adapted to the spatial and temporal properties of their natural habitat. Resource and space use is maximized both at the colony and the population level by a model with a behavioral strategy including learning and fast forgetting rates.

Pygidial gland chemistry and potential alarm-recruitment function in column foraging, but not solitary, Nearctic Messor harvesting ants (Hymenoptera: Formicidae: Myrmicinae)

We investigated the role of the pygidial gland on foraging behavior in two ecologically dominant column foraging Nearctic harvesting ants (Messor pergandei and Messor andrei). Using chemical analyses and behavioral tests, we show that n-tridecane is the major biologically active compound of pygidial gland secretions in both species, and that this chemical functions as a powerful alarm-recruitment pheromone. Another major compound of pygidial gland contents is benzaldehyde; this substance does not release behavioral reactions in M. pergandei workers but might function as a defensive secretion. Six solitary foraging Nearctic Messor and two column foraging Palearctic Messor species, did not have large pygidial gland reservoirs.

Regional variation in queen and worker aggression in incipient colonies of the desert ant Messor pergandei

The fate of queen foundress associations in ants varies across taxa: in some, lethal fighting results in survival of a single queen, while in others, queens coexist long term. One hypothesis for this difference is that selection favors fighting when group sizes are small and tolerance when groups are large. In an experiment with the ant Messor pergandei, we formed small, medium, and large groups with newly mated queens from field populations that have different mean group sizes and differ in whether multiple queens occur in older established colonies. We found that whether queens are eliminated by fighting depends upon region of origin and not group size: regardless of co-foundress number, queens from sites with single-queen adult field colonies displayed agonistic behaviors and their colonies reduced to a single queen, while queens from sites with multiple-queen colonies did not fight and co-foundresses coexisted long term. Worker aggression towards and elimination of queens were also correlated with region of origin. Where fighting occurred, queens were as likely to be killed by workers as by other queens. An aggressive display was the most common form of agonistic interaction among queens, while fighting was relatively rare. We hypothesize that queen displays evolved in response to worker attacks because they increase the probability that workers will eliminate competitor queens. Our results suggest that the evolutionary interests of workers, as well as queens, could be important in determining the evolution and maintenance of queen elimination in foundress associations.

Relatedness does not explain geographic variation in queen cooperation in the seed-harvester ant Messor pergandei

The desert seed-harvester ant Messor pergandei shows sharp regional differences in social structure: in central Arizona, queens initially form group nests but become aggressive following worker emergence and reduce to a single queen (secondary monogyny). In much of the rest of the species range, however, co-founding queens do not display aggression and retain multiple queens throughout the colony lifecycle (primary polygyny). One hypothesis to explain why queen behavior differs between regions is that relatedness among co-foundresses and, therefore, the potential for kin-selected cooperation, varies geographically. To test whether primary polygyny is associated with greater kin association, we used highly polymorphic microsatellites to estimate within-group relatedness for co-foundress associations in the field at two secondarily monogynous sites and five primarily polygynous sites. To determine whether queens can potentially use nestmate identity as a proxy for genetic relatedness, we compared these values to similarly sized samples of worker nestmates from adult colonies at the same sites. We found that foundresses do not preferentially form groups with relatives regardless of the ultimate fate of foundress groups. Mean relatedness values for co-foundresses did not differ significantly from zero irrespective of social structure. In contrast, adult colony worker nestmates were significantly positively related at all sites. These results indicate that kin-selected benefits are not likely to be responsible for the absence of fatal competition in the polygynous region; instead, the cause of geographic variation in queen cooperation must lie in ecological factors that alter the costs and benefits of retaining additional queens into colony maturity.