Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus

Deeply conserved molecular mechanisms regulate food-searching behaviour in response to nutritional cues in a wide variety of vertebrates and invertebrates. Studies of the highly eusocial honey bee have shown that nutritional physiology and some conserved nutrient signalling pathways, especially the insulin pathway, also regulate the division of labour between foraging and non-foraging individuals. Typically, lean workers leave the nest to forage for food, and well-nourished workers perform tasks inside the nest. Here we provide the first direct test of whether similar mechanisms operate in a primitively eusocial insect in an independently evolved social lineage, the paper wasp Polistes metricus. We found that food deprivation caused reduced lipid stores and higher levels of colony and individual foraging. Individuals with greatly reduced lipid stores foraged at extremely elevated levels. In addition, brain expression of several foraging-related genes was influenced by food deprivation, including insulin-like peptide 2 (ilp2). Together with previous findings, our results demonstrate that nutrition regulates foraging division of labour in two independently evolved social insect lineages (bees and wasps), despite large differences in social organization. Our results also provide additional support for the idea that nutritional asymmetries among individuals, based on differences in nutritional physiology and expression of conserved nutrient signalling genes in the brain, are important in the division of labour in eusocial societies.     

The short-term regulation of foraging in harvester ants

In the seed-eating ant Pogonomyrmex barbatus, the return ofsuccessful foragers stimulates inactive foragers to leave thenest. The rate at which successful foragers return to the nestdepends on food availability; the more food available, the morequickly foragers will find it and bring it back. Field experimentsexamined how quickly a colony can adjust to a decline in therate of forager return, and thus to a decline in food availability,by slowing down foraging activity. In response to a brief, 3-to 5-min reduction in the forager return rate, foraging activityusually decreased within 2–3 min and then recovered within5 min. This indicates that whether an inactive forager leavesthe nest on its next trip depends on its very recent experienceof the rate of forager return. On some days, colonies respondedmore to a change in forager return rate. The rapid colony responseto fluctuations in forager return rate, enabling colonies toact as risk-averse foragers, may arise from the limited intervalover which an ant can track its encounters with returning foragers.     

Parallel foraging cycles for different resources in leaf‐cutting ants: a clue to the mechanisms of rhythmic activity

1. Leaf‐cutting ants display regular diel cycles of foraging, but the regulatory mechanisms underlying these cycles are not well known. There are, however, some indications in the literature that accumulation of leaf tissue inside a nest dampens recruitment of foragers, thereby providing a negative feedback that can lead to periodic foraging. We investigated two foraging cycles occurring simultaneously in an Atta colombica colony, one involving leaf harvesting and the other exploiting an ephemeral crop of ripe fruit. 2. Leaf harvesting followed a typical diel pattern of a 10–12 h foraging bout followed by a period of inactivity, while fruit harvesting occurred continuously, but with a regular pre‐dawn dip in activity that marked a 24 h cycle. 3. Although the results of the present study are drawn from a single field colony, the difference found is consistent with a mechanism of negative feedback regulation acting in parallel on two resources that differ in their rates of distribution and processing, creating cycles of formation and depletion of material caches. 4. This hypothesis should provoke further interest from students of ant behaviour and some simple manipulative experiments that would begin to test it are outlined. Any role of resource caches in regulating foraging by Atta colonies may have similarities to the logistics of warehouse inventories in human economic activity.     

白蚁采食行为中的信息交流

白蚁作为社会性昆虫, 其采食个体间依赖各种信息交流机制进行联系与协作, 其中包括踪迹、 警戒、 食物信息、 同伴识别和助食等。通常的联系信号为挥发性或半挥发性化学物质或者一定频谱和功率的机械振动波。其中踪迹信息素、 蚁源烃类、 警戒信息素、 助食素和机械振动信号等都在白蚁采食过程中起着重要作用。白蚁采食过程中食物定向和食物品质信息的传达主要依靠腹板腺分泌的踪迹信息素, 已发现有十二碳烯醇类、 降碳倍半萜类和大环二萜类。蚁源的机械振动也在食物品质表达方面起到一定作用, 但食物品质的表达机制还不明确。白蚁采食协作的基础是同伴识别, 蚁源烃类（C21~C35）是同伴识别的主要信息物质, 采食个体分泌的助食素则可促成共同取食。警戒信息素传递白蚁采食的安全信息, 通常为一些兵蚁源的萜类物质, 但得到功能鉴定的结构还不多。近来研究还发现特殊的蚁源机械振动也可起到示警作用。已初步证实各种信息交流机制间存在交互作用, 但交互作用的机理有待进一步解析。生物物理因素在白蚁采食行为中的作用值得更多重视。本文以白蚁的采食行为为线索, 评述白蚁采食个体间信息交流机制的研究进展及利用问题, 并对今后的研究提出展望。     

Influence of temporal fluctuations in seed abundance on the foraging behaviour of harvester ants (Pogonomyrmex spp.) in the central Monte desert,Argentina

The simultaneous study of the temporal dynamics of foraging behaviour, diet and seed abundance is essential to assess the way in which resources affect the behaviour and ecology of harvester ants. Here, we evaluate how fluctuations in grass seed abundance during three consecutive growing seasons influenced the foraging behaviour and diet of the harvester ants Pogonomyrmex rastratus, P. mendozanus and P. inermis in the central Monte desert, Argentina. Seed abundance of the most consumed grasses varied greatly through ant activity season, and ants altered their foraging behaviour in response to those changes. Foragers spent more time travelling and searching for food, and their foraging trips took longer during the low seed availability season. Foraging distance was very similar among species and, contrary to our expectations, did not vary between seasons. Foraging success of P. rastratus and P. inermis increased during the high availability season. This matched the seasonal pattern of foraging activity, suggesting that colonies may detect seed abundance and regulate their foraging effort with the rate of forager success. Although grass seeds were the main item in the diet of the three species, P. mendozanus, and to a lesser extent P. rastratus, turned more generalist when grass seeds were scarce. In contrast, P. inermis showed a very narrow diet breadth, only harvesting grass seeds in both seasons. Our results indicate the relevance of seed availability on foraging behaviour of harvester ants, which should be taken into account when predicting and evaluating the effect of ants on seed resources as well as numerical responses of harvester ant populations to the temporal and spatial variations in grass seed abundance.     

Nest architecture shapes the collective behaviour of harvester ants

Structures influence how individuals interact and, therefore, shape the collective behaviours that emerge from these interactions. Here I show that the structure of a nest influences the collective behaviour of harvester ant colonies. Using network analysis, I quantify nest architecture and find that as chamber connectivity and redundancy of connections among chambers increase, so does a colony''s speed of recruitment to food. Interestingly, the volume of the chambers did not influence speed of recruitment, suggesting that the spatial organization of a nest has a greater impact on collective behaviour than the number of workers it can hold. Thus, by changing spatial constraints on social interactions organisms can modify their behaviour and impact their fitness.     

Individual foraging components of harvester ants: movement patterns and seed patch fidelity

Summary We investigated individual foraging components of the western harvester ant,Pogonomyrmex occidentalis, in the native seed background of a shrub-steppe environment. Our study identified factors affecting foraging movements and seed selection by individual ants. Some assumptions and predictions of central-place foraging theory and a correlated random walk were evaluated for individual foragers. Results showed that ant size was only weakly correlated with the seed sizes harvested; seed size was a more important constraint than a predictor of seed selection. Individual ants spent more time in localized search behavior than traveling between search areas and nests.P. occidentalis foragers encountered seeds randomly with respect to time, and handled a mean of 1.7 seeds/trip. A correlation of increased search effort with greater travel distances was consistent with central-place foraging theory but, contrary to it, search and travel effort were not associated with energetic reward.Individual ants exhibited fidelity in both search site and native seed species. Spatial analyses of foraging movements showed a highly oriented travel path while running, and an area-restricted path while searching. Searching ants moved in a manner consistent with a correlated random walk. The deterministic component of patch fidelity and the stochastic component of search may override energetic foraging decisions in individualP. occidentalis ants.     

Consequences of climate and body size on the foraging performance of seed‐eating ants

1. Changes in climatic factors could have major effects on the foraging performance of animals. To date, however, no study has attempted to examine the concurrent effect of different climatic factors on foraging performance of individual organisms. 2. In the present study, this issue was addressed by studying changes in foraging performance of seed‐eating ant colonies of the genus Messor in response to variation in precipitation and ambient temperature along a macroecological gradient. In addition, we examined the way three colony‐level attributes, foraging distance, forager number, and variance in worker‐size, could affect foraging performance in those ants. Foraging performance was measured as size matching, i.e. the correlation between forager size and load size. The study was carried out for 2 years in six sites along a south‐north productivity gradient in a semi‐arid region of the Eastern‐Mediterranean. 3. Size matching increased with increased precipitation as well as with an increase in worker‐size variability, but slightly decreased with increasing temperatures, as predicted by foraging‐decision models. In contrast, foraging distance had no effect on size matching. Interestingly, size matching showed a unimodal relationship with forager number. 4. These results indicate that interplay between climate and body size affects foraging performance either directly via physiological constraints, or indirectly through their effect on food availability. Moreover, this is one of the first evidences to support the assumption that ant colonies can differ in their ability to optimally allocate their workforce in natural environments. This emphasises the importance of studying the way foraging strategies vary across environmental gradients at macroecological scales.     

Alarm behaviour in Eciton army ants

The effective communication of alarm can be critical for social animals so that they are able to deal with threats posed by predators and competitors. In the case of many of the most ecologically dominant, large‐colony ant species, these alarm responses are aggressive and coordinated by alarm pheromones, produced generally from the mandibular glands. In the present study, the alarm behaviour of two Neotropical army ant species is examined, the swarm raiding Eciton burchellii (Westwood) and the column raiding Eciton hamatum (Fabricius). Both species exhibit aggressive alarm responses in response to crushed heads, suggesting that the alarm pheromone is indeed produced by the mandibular glands in these ants. The most abundant component of the mandibular gland secretion, 4‐methyl‐3‐heptanone (10 µL on a rubber septum), stimulates a substantial alarm response, although this is less than the response to a single crushed head. This suggests that 4‐methyl‐3‐heptanone may be an alarm‐stimulating compound in Eciton. The alarm response of E. burchellii involves more workers than that of E. hamatum, although major workers play a much greater role in the response of the latter species. The differences in the alarm response of the two closely‐related species may relate to their foraging strategies, with E. burchellii relying more on quantity rather than the caste of ants responding and possibly using alarm pheromones for offensive as well as defensive functions.     

Colony‐level behavioural variation correlates with differences in expression of the foraging gene in red imported fire ants

Among social insects, colony‐level variation is likely to be widespread and has significant ecological consequences. Very few studies, however, have documented how genetic factors relate to behaviour at the colony level. Differences in expression of the foraging gene have been associated with differences in foraging and activity of a wide variety of organisms. We quantified expression of the red imported fire ant foraging gene (sifor) in workers from 21 colonies collected across the natural range of Texas fire ant populations, but maintained under standardized, environmentally controlled conditions. Colonies varied significantly in their behaviour. The most active colonies had up to 10 times more active foragers than the least active colony and more than 16 times as many workers outside the nest. Expression differences among colonies correlated with this colony‐level behavioural variation. Colonies with higher sifor expression in foragers had, on average, significantly higher foraging activity, exploratory activity and recruitment to nectar than colonies with lower expression. Expression of sifor was also strongly correlated with worker task (foraging vs. working in the interior of the nest). These results provide insight into the genetic and physiological processes underlying collective differences in social behaviour. Quantifying variation in expression of the foraging gene may provide an important tool for understanding and predicting the ecological consequences of colony‐level behavioural variation.     

昆虫基因表达的调控

昆虫的基因表达过程十分复杂,受多种调控因子的调节,随着分子生物学研究新技术在昆虫学上的应用,昆虫基因表达的调控也取得了较快进展,本文以一些特征清楚的系统为例,讨论昆虫基因表达调控的研究现状,旨在为其它昆虫表达的调控研究提供借鉴。     

Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis

Multiple mating by females characterizes most insect species, but is relatively uncommon in social insects. Females may mate with multiple mates because they experience the direct benefits of increased survival or fecundity, to acquire high quality mates, or to lower the risk of reduced fecundity by mating with incompatible males. We used the extensive natural variation in mating frequency in the western harvester ant, Pogonomyrmex occidentalis , to test the hypothesis that increased mating by the queen leads to an increase in colony performance. Colonies with greater genetic diversity began to forage earlier in the day and foraged for longer time periods. The workers which initiated foraging were a nonrandom subset of the genotypes present in the colony. We used a statistical approach to correctly predict the direction and magnitude of the correlation between genetic diversity and colony foraging activity.     

Colony variation in the collective regulation of foraging by harvester ants

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.     

The importance of location and visual cues during foraging in the German wasp (Vespula germanica F.) (Hymenoptera: Vespidae)

Abstract

The way in which foraging wasps use cues for prey location and choice appears to depend on both the context and on the type of prey. Vespula germanica is an opportunistic, generalist prey forager, and individual wasp foragers often return to hunt at sites of previous hunting success. In this paper, we studied which cues are used by this wasp when relocating a food source. Particularly we analysed the response to a displaced visual cue versus a foraging location at which either honey or cat food had been previously presented. We conclude that location is used over a displaced visual cue for directing wasp hovering, although the landing response is directed differently according to bait type. When wasps are exploiting cat food, location also elicits landing, but if they are exploiting honey, a displaced visual cue elicits landing more frequently than location.     

Flexible task allocation and the organization of work in ants

Flexibility in task performance is essential for a robust system of division of labour. We investigated what factors determine which social insect workers respond to colony-level changes in task demand. We used radio-frequency identification technology to compare the roles of corpulence, age, spatial location and previous activity (intra-nest/extra-nest) in determining whether worker ants (Temnothorax albipennis) respond to an increase in demand for foraging or brood care. The less corpulent ants took on the extra foraging, irrespective of their age, previous activity or location in the nest, supporting a physiological threshold model. We found no relationship between ants that tended the extra brood and corpulence, age, spatial location or previous activity, but ants that transported the extra brood to the main brood pile were less corpulent and had high previous intra-nest activity. This supports spatial task-encounter and physiological threshold models for brood transport. Our data suggest a flexible task-allocation system allowing the colony to respond rapidly to changing needs, using a simple task-encounter system for generalized tasks, combined with physiologically based response thresholds for more specialized tasks. This could provide a social insect colony with a robust division of labour, flexibly allocating the workforce in response to current needs.     

The expression and impact of antifungal grooming in ants

Parasites can cause extensive damage to animal societies in which many related individuals frequently interact. In response, social animals have evolved diverse individual and collective defences. Here, we measured the expression and efficiency of self-grooming and allo-grooming when workers of the ant Formica selysi were contaminated with spores of the fungal entomopathogen Metarhizium anisopliae. The amount of self-grooming increased in the presence of fungal spores, which shows that the ants are able to detect the risk of infection. In contrast, the amount of allo-grooming did not depend on fungal contamination. Workers groomed all nestmate workers that were re-introduced into their groups. The amount of allo-grooming towards noncontaminated individuals was higher when the group had been previously exposed to the pathogen. Allo-grooming decreased the number of fungal spores on the surface of contaminated workers, but did not prevent infection in the conditions tested (high dose of spores and late allo-grooming). The rate of disease transmission to groomers and other nestmates was extremely low. The systematic allo-grooming of all individuals returning to the colony, be they contaminated or not, is probably a simple but robust prophylactic defence preventing the spread of fungal diseases in insect societies.     

Adaptive foraging of leaf‐cutter ants to spatiotemporal changes in resource availability in Neotropical savannas

1. Generalist herbivores feed on a wide and diverse set of species, but fine‐scale foraging patterns may be affected by the interplay between the quality, quantity and spatial distribution of host plants. 2. The foraging patterns of a prevalent Neotropical herbivore, the leaf‐cutter ant Atta laevigata, in the Brazilian Cerrado savannas were examined in order to determine if patterns observed are in concert with central‐place foraging predictions. 3. The results showed that A. laevigata acts as a polyphagous but highly selective herbivore, with ant attacks often resulting in partial defoliation of less‐preferred species and full defoliation of preferred ones. It was found, for the first time, that there is a strong and positive relationship between the relative attack frequency on plants from preferred species and foraging distance to the nest. This suggests a balance between the quality of plant resources harvested and costs involved in their transportation. It was also observed that colonies focused their harvest on preferred species in months with low availability of young leaves. Consequently, high herbivory rate was more frequent in plants attacked far away from the nest and in dry months. 4. These assessments highlight the fact that Atta colonies may become more selective as foraging distance to the nest increases and in response to fluctuations in the availability of palatable resources throughout the year. The results also show some dissimilarities in the foraging behaviours of A. laevigata when compared with other locations, suggesting that widely distributed herbivores may modify foraging strategies across their geographic range.     

Age- and task-dependent foraging gene expression in the bumblebee Bombus terrestris

In eusocial insects, the division of labor within a colony, based on either age or size, is correlated with a differential foraging (for) gene expression and PKG activity. This article presents in the first part a study on the for gene, encoding a cGMP-dependent protein kinase (PKG) in the bumblebee Bombus terrestris. Cloning of the open reading frame allowed phylogenetic tracing, which showed conservation of PKGs among social insects. Our results confirm the proposed role for PKGs in division of labor. Btfor gene expression is significantly higher in the larger foragers compared with the smaller sized nurses. More importantly, we discovered an age-related decrease in Btfor expression in both nursing and foraging bumblebees. We therefore speculate that the presence of BtFOR is required for correct adaptation to new external stimuli and rapid learning for foraging. In a second series of experiments, worker bumblebees of B. terrestris were treated with two insecticides imidacloprid and kinoprene, which have shown to cause impaired foraging behavior. Compared with controls, only the latter treatment resulted in a decreased Btfor expression, which concurs with a stimulation of ovarian growth and a shift in labor toward nest-related tasks. The data are discussed in relation to Btfor expression in the complex physiological event of foraging and side-effects by pesticides.