Effects of division of labour on immunity in workers of the ant <Emphasis Type="Italic">Cataglyphis cursor</Emphasis>

Workers in social insects perform different roles, and the environment they experience differs markedly according to the tasks performed. Life history theory predicts that individuals should adapt investment in immune defences according to their cost relative to the risk of pathogen infection. Workers, which forage outside the nest, face harsher environmental conditions with increased risk of injury and infection. We then might expect higher immune defences in foragers than in intra-nidal workers which remain in the relative sanctity of the nest. However, task partitioning in social insects is often age-based, and foragers are usually the oldest individuals. Hence if immune defences degenerate with age, foragers could have lower immune defences than intra-nidal workers. In this study, we examined the difference in immune defences as assessed by the level of phenoloxidase activity (PO) between intra-nidal workers and foragers in the ant Cataglyphis cursor. In three out of four colonies tested, foragers and intra-nidal workers did not differ in their level of PO. In the final colony, the level of workers PO overall was higher than in the other three colonies, and foragers displayed a lower level of PO than intra-nidal workers. These results may suggest that, when a sustained colonial PO activity is necessary, foragers may be less able than intra-nidal workers to activate their PO. Our results are discussed in the light of previous studies that underline the diversity of PO activity patterns in social insects. The variation observed among studies and even colonies clearly emphasizes the plasticity of immune parameters.     

Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity

Hemocytes and the (prophenol-) phenoloxidase system constitute the immediate innate immune system in insects. These components of insect immunity are present at any post-embryonic life stage without previous infection. Differences between individuals and species in these immune parameters can reflect differences in infection risk, life expectancy, and biological function. In honeybees which show an age-related division of labor within the worker caste, previous studies demonstrated that foragers show a strongly reduced number of hemoctyes compared to the younger nurse bees. This loss of immune competence has been regarded advantageous with respect to an already high mortality rate due to foraging and to redistribution of energy costs at the colony level. Based on the idea that abandoning hemocytes in all adults would be a reasonably direct regulatory mechanism, we posed the hypothesis that abandoning hemocytic immunity is not restricted to worker honeybees. We tested our hypotheses by performing a comprehensive analysis of hemocyte number and phenoloxidase (PO)-activity levels in immunologically naive workers, queens, and drones. We found that in all three adult phenotypes hemocyte number is dramatically reduced in early adult life. In contrast, we found that the dynamics of PO-activity levels have sex and caste-specific characteristics. In workers, PO activity reached a plateau within the first week of adult life, and in queens enzyme levels continuously increased with age and reached levels twice as high as those found in workers. PO-activity levels slightly declined with age in drones. These data support our hypothesis, from which we infer that the previously reported reduction of hemocyte in foragers is not worker specific but represents a general phenomenon occurring in all honeybee adult phenotypes.     

Bumble bees (Bombus terrestris) store both food and information in honeypots

Social insect foragers often transmit information about foodsources to nest mates. In bumble bees (Bombus terrestris), forexample, successful foragers use excited motor displays anda pheromone as communication signals. In addition, bees couldmake use of an indirect pathway of information flow, via thehoney stores. We show here that, indeed, bees in the nest continuouslymonitor honeypots and sample their contents, thus obtaininginformation on supply and demand of nectar. When there is aninflux of nectar into the nest, the colony deploys more workersfor foraging. The number of new foragers depends on sugar concentration.Foragers returning with high-quality sugar solution displaymore "excited runs" on the nest structure. The recruits' response,however, does not depend on modulated behavior by foragers:more workers start to forage with high quality of incoming nectar,even when this nectar is brought by a pipette. Moreover, weshow that the readiness of bees to respond to recruitment signalsor incoming nectar also depends on colony demand. When colonynectar stores are full, the response of bees to equal amountsof nectar influx is smaller than when stores are empty. Whencolony nectar stores are depleted, foragers spend more timerunning excitedly and less time probing pots in the nest andrun with higher average speed, possibly to disperse the alertingpheromone more efficiently. However, more bees respond to nectarinflux to empty stores, whether or not this is accompanied byforager signals. Thus, honeypots serve to store informationas well as food.     

Information needs at the beginning of foraging: grass-cutting ants trade off load size for a faster return to the nest

Background

Acquisition of information about food sources is essential for animals that forage collectively like social insects. Foragers deliver two commodities to the nest, food and information, and they may favor the delivery of one at the expenses of the other. We predict that information needs should be particularly high at the beginning of foraging: the decision to return faster to the nest will motivate a grass-cutting ant worker to reduce its loading time, and so to leave the source with a partial load.

Principal Findings

Field results showed that at the initial foraging phase, most grass-cutting ant foragers (Acromyrmex heyeri) returned unladen to the nest, and experienced head-on encounters with outgoing workers. Ant encounters were not simply collisions in a probabilistic sense: outgoing workers contacted in average 70% of the returning foragers at the initial foraging phase, and only 20% at the established phase. At the initial foraging phase, workers cut fragments that were shorter, narrower, lighter and tenderer than those harvested at the established one. Foragers walked at the initial phase significantly faster than expected for the observed temperatures, yet not at the established phase. Moreover, when controlling for differences in the fragment-size carried, workers still walked faster at the initial phase. Despite the higher speed, their individual transport rate of vegetable tissue was lower than that of similarly-sized workers foraging later at the same patch.

Conclusions/Significance

At the initial foraging phase, workers compromised their individual transport rates of material in order to return faster to the colony. We suggest that the observed flexible cutting rules and the selection of partial loads at the beginning of foraging are driven by the need of information transfer, crucial for the establishment and maintenance of a foraging process to monopolize a discovered resource.     

The Old Ladies of the Seed Harvester ant Pogonomyrmex Rugosus: Foraging Performed by Two Groups of Workers

We examined temporal polyethism in Pogonomyrmex rugosus, predicting a pattern of decreasing age from foragers to nest maintenance workers to individuals that were recruited to harvest a temporary food source. Nest maintenance workers were younger than foragers, as indicated by their heavier mass and lower mandibular wear. In contrast, recruited foragers were similar in mass to foragers but they displayed higher mandibular wear, suggesting that they were at least as old as foragers. Longevity estimates for marked individuals of these two latter task groups showed mixed results. Higher mandibular wear of recruited foragers suggests that they did not follow the normal sequence for temporal polyethism, but rather that they functioned as seed-millers, which should more quickly abrade their dentition. This would be the first demonstration of specialist milling individuals in a monomorphic seed-harvester ant.     

Experience Based Use of Landmark and Vector Based Orientation During Homing by the Ant Formica cunicularia (Hymenoptera: Formicidae)

Homing paths of Formica cunicularia foragers from an artificial food reward were analyzed on a familiar terrain and in displacement experiments on a familiar and an unfamiliar terrain. Foragers were tested either when relatively new to a foraging route (untrained group) or after a day’s experience with it (trained group). Untrained foragers followed direct homing paths to the nest site when tested in the familiar terrain but followed tortuous paths when displaced to the unfamiliar terrain. Trained foragers behaved similarly to untrained ones when tested from the food reward to the nest site in the familiar terrain but their behavior changed in displacements. Irrespective of the familiarity of the displacement site, these foragers followed paths taking them to the expected nest sites. The results showed that foragers did not rely on chemical cues for homing and revealed that untrained foragers disregarded path integration and were directed to the nest site when it is in their visual panorama. On the contrary, trained foragers may have relied on path integration on familiar and unfamiliar terrain. The results also demonstrated that experience greatly affected the preferential use of visual and vector based cues by foragers during homing.     

Interactions Increase Forager Availability and Activity in Harvester Ants

Social insect colonies use interactions among workers to regulate collective behavior. Harvester ant foragers interact in a chamber just inside the nest entrance, here called the ''entrance chamber''. Previous studies of the activation of foragers in red harvester ants show that an outgoing forager inside the nest experiences an increase in brief antennal contacts before it leaves the nest to forage. Here we compare the interaction rate experienced by foragers that left the nest and ants that did not. We found that ants in the entrance chamber that leave the nest to forage experienced more interactions than ants that descend to the deeper nest without foraging. Additionally, we found that the availability of foragers in the entrance chamber is associated with the rate of forager return. An increase in the rate of forager return leads to an increase in the rate at which ants descend to the deeper nest, which then stimulates more ants to ascend into the entrance chamber. Thus a higher rate of forager return leads to more available foragers in the entrance chamber. The highest density of interactions occurs near the nest entrance and the entrances of the tunnels from the entrance chamber to the deeper nest. Local interactions with returning foragers regulate both the activation of waiting foragers and the number of foragers available to be activated.     

The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge

The honey bee, Apis mellifera, is an ideal system for investigating ontogenetic changes in the immune system, because it combines holometabolous development within a eusocial caste system. As adults, male and female bees are subject to differing selective pressures: worker bees (females) exhibit temporal polyethism, while the male drones invest in mating. They are further influenced by changes in the threat of pathogen infection at different life stages. We investigated the immune response of workers and drones at all developmental phases, from larvae through to late stage adults, assaying both a constitutive (phenoloxidase, PO activity) and induced (antimicrobial peptide, AMP) immune response. We found that larval bees have low levels of PO activity. Adult workers produced stronger immune responses than drones, and a greater plasticity in immune investment. Immune challenge resulted in lower levels of PO activity in adult workers, which may be due to the rapid utilisation and a subsequent failure to replenish the constitutive phenoloxidase. Both adult workers and drones responded to an immune challenge by producing higher titres of AMPs, suggesting that the cost of this response prohibits its constant maintenance. Both castes showed signs of senescence in immune investment in the AMP response. Different sexes and life stages therefore alter their immune system management based on the combined factors of disease risk and life history.     

The effects of colony characteristics on life span and foraging behavior of individual wasps (Polybia occidentalis,Hymenoptera: Vespidae)

Summary We studied the effects of intrinsic colony characteristics and an imposed contingency on the life span and behavior of foragers in the swarm-founding social waspPolybia occidentalis. Data were collected on marked, known-age workers introduced into four observation colonies.To test the hypothesis that colony demographic features affect worker life span, we examined the relationships of colony age and size with worker life span using survivorship analysis. Colony age and size had positive relationships with life span; marked workers from two larger, older colonies had longer life spans (¯X = 24.7 days) than those from two smaller, younger colonies (¯X = 20.1 days).We quantified the effects of experimentally imposed nest damage on forager behavior, to determine which of three predicted behavioral responses by foragers to this contingency (increased probability of foraging for building material, increased rate of foraging, or decrease in age of onset of foraging) would be employed. Increasing the colony level of need for materials used in nest construction (wood pulp and water) by damaging the nests of two colonies did not cause an increase in either the proportion of marked workers that gathered nest materials or in foraging rates of marked individuals, when compared with introduced workers in two simultaneously observed control colonies. Instead, nest damage caused a decrease in the age at which marked workers first foraged for pulp and water. The response to an increase in the need for building materials was an acceleration of behavioral development in some workers.     

The allocation of foragers in red wood ants

Abstract. 1. We studied how colonies of the red wood ant, Formica polyctena , adjust the numbers of foragers allocated to different foraging trails. In a series of field experiments, foragers were marked and transferred from one nest to another, related nest, where they joined the foraging force. Transferred workers acted as a reserve of uncommitted, available foragers.
2. Previous work shows that each individual forager habitually uses one trail. We found that for an uncommitted forager, the influence of recruitment initially is stronger than that of directional fidelity. Transferred workers were likely to use trails leading to new food sources. When transferred to a new nest, foragers were not likely to use a trail in the same direction as their original trail in the donor nest.
3. After a week, transferred foragers tended to develop route fidelity. Even after bait was no longer present, they continued to use the trail that had formerly led to a bait source.
4. We examined how colonies adjust numbers on a trail by experimentally depleting some trails. Colonies usually did not compensate for depletion: foragers were not recruited to depleted trails.
5. In general, the dynamics of foraging in this species facilitate a consistent foraging effort rather than rapid adjustments of forager allocation.     

Division of labor in post-emergence colonies of the primitively eusocial waspPolistes instabilis de Saussure (Hymenoptera: Vespidae)

Polyethism was quantified in post-emergence colonies of the primitively eusocial wasp,Polistes instabilis, and compared to polyethism in a sympatric advanced eusocial wasp,Polybia occidentalis. Like P.occidentalis, P. instabilis foragers collected food (nectar and prey) and nest materials (wood pulp and water).P. instabilis foragers showed some evidence of specialization with respect to which materials they gathered, but most foragers, divided their effort among food and nest materials, a pattern that is rarely seen inP. occidentalis. In colonies of both species, more foragers collected nectar than any other material; in contrast, most water foraging was performed by one or two workers. Upon returning to the nest,P. instabilis foragers gave up part or all of most nectar, prey, and pulp loads to nestmates, while water was rarely partitioned. Prey loads were most likely to be given up entirely.P. instabilis workers show evidence of conflict over the handling of materials at the nest. The frequency with which workers took portions of nectar loads from forgers was positively correlated with their frequency of aggressive dominant behavior, and with their frequency of taking other foraged materials. Compared to polyethism inP. occidentalis P. instabilis showed less individual specialization on foraging tasks and less partitioning of foraged materials with nestmates, suggesting that these characteristics of polyethism have been modified during the evolution of advanced insect societies.     

Waste Management in the Leaf-Cutting Ant <Emphasis Type="Italic">Acromyrmex lobicornis</Emphasis>: Division of Labour,Aggressive Behaviour,and Location of External Refuse Dumps

In leaf-cutting ants, the handling of waste materials from the fungus culture increases the risk of infection. Consequently, ants should manage their waste in a way that minimizes the spread of diseases. We investigated whether in Acromyrmex lobicornis, waste-worker ants (a) also perform roles in foraging or mound maintenance, (b) are morphologically different than other ant workers, and (c) are aggressively discriminated by other worker ants from the same colony. In addition, we investigated whether the location of external waste piles minimizes the probability that wastes spread to the ant nest. In the field, we (a) marked with different colours waste-workers, foragers and mound-workers and monitored whether these ants interchanged their tasks; (b) measured head width, head length, hind femur length and total length of waste-workers; foragers and mound-workers; (c) forced field encounters between waste-workers and foragers, and (d) measured the cardinal orientation of the waste piles in relation to the colony mound. Waste-worker ants did not perform other function outside the nest; neither foragers nor mound-workers managed the waste. Moreover, waste-workers were smaller than foragers and mound-workers, and were attacked if they tried to enter their nest using foraging entrances. The location of external refuse dumps also appears to reduce contamination risks. Waste piles always were down-slope, and often followed the prevailing wind direction. The importance of behaviours such as the division of labour, aggressions against waste-workers and nest compartmentalization (i.e., the orientation of external waste piles) to minimize the spread of pathogens is discussed.     

Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency?

Bumblebee workers vary greatly in size, unlike workers of most other social bees. This variability has not been adequately explained. In many social insects, size variation is adaptive, with different-sized workers performing different tasks (alloethism). Here we established whether workers of the bumblebee, Bombus terrestris (L.) (Hymenoptera; Apidae), exhibit alloethism. We quantified the size of workers engaging in foraging compared to those that remain in the nest, and confirmed that it is the larger bees that tend to forage (X±SE thorax widths 4.34±0.01 mm for nest bees and 4.93±0.02 mm for foragers). We then investigated whether large bees are better suited to foraging because they are able to transport heavier loads of food back to the nest. Both pollen and nectar loads of returning foragers were measured, demonstrating that larger bees do return with a heavier mass of forage. Foraging trip times were inversely related to bee size when collecting nectar, but were unrelated to bee size for bees collecting pollen. Overall, large bees brought back more nectar per unit time than small bees, but the rate of pollen collection appeared to be unrelated to size. The smallest foragers had a nectar foraging rate close to zero, presumably explaining why foragers tend to be large. Why might larger bees be better at foraging? Various explanations are considered: larger bees are able to forage in cooler conditions, may be able to forage over larger distances, and are perhaps also less vulnerable to predation. Conversely, small workers are presumably cheaper to produce and may be more nimble at within-nest tasks. Further research is needed to assess these possibilities. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Heat stress during development affects immunocompetence in workers,queens and drones of Africanized honey bees (Apis mellifera L.) (Hymenoptera: Apidae)

Though social insects generally seem to have a reduced individual immunoresponse compared to solitary species, the impact of heat stress on that response has not been studied. In the honey bee, the effect of heat stress on reproductives (queens and males/drones) may also vary compared to workers, but this is currently unknown. Here, we quantified the activity of an enzyme linked to the immune response in insects and known to be affected by heat stress in solitary species: phenoloxidase (PO), in workers, queens and drones of Africanized honey bees (AHBs) experimentally subjected to elevated temperatures during the pupal stage. Additionally, we evaluated this marker in individuals experimentally infected with the entomopathogenic fungus Metarhizium anisopliae. Differences in PO activity were found between sexes and castes, with PO activity generally higher in workers and lower in reproductives. Such differences are associated with the likelihood of exposure to infection and the role of different individuals in the colony. Contrary to our expectation, heat stress did not cause an increase in PO activity equally in all classes of individual. Heat stress during the pupal stage significantly decreased the PO activity of AHB queens, but not that of workers or drones, which more frequently engage in extranidal activity. Experimental infection with Metarhizium anisopliae reduced PO activity in queens and workers, but increased it in drones. Notably, heat stressed workers lived significantly shorter after infection despite exhibiting greater PO activity than queens or drones. We suggest that this discrepancy may be related to trade-offs among immune response cascades in honey bees such as between heat shock proteins and defensin peptides used in microbial defence. Our results provide evidence for complex relationships among humoral immune responses in AHBs and suggest that heat stress could result in a reduced life expectancy of individuals.     

Dispersed central place foraging in Australian meat ants

Summary Australian meat ants often inhabit colonies with widely dispersed nest holes, and this study examines how resource is harvested and distributed in a colony ofIridomyrmex sanguineus Smith (Formicidae: Dolichoderinae). The three principal types of foragers (tenders, honeydew transporters, scavengers) exhibited nest hole fidelity, where harvested resource was consistently delivered to the same nest hole by each foraging individual. Australian meat ants thus use a harvesting system based on dispersed central place foraging. Evidence of frequent larval transport among nest holes, age polyethism developing in the direction of foraging, and the tendency for nest-associated workers to accept new nest holes more readily than foragers, suggests that workers develop fidelity to the particular nest hole in which they eclose. Coupled with larval transport, nest hole fidelity may allow a colony with widely dispersed nest holes to adjust its structure to more efficiently harvest a resource distributed unevenly in space or time.     

Introduction of a scented carbohydrate resource into the nest increases departure rate in Polybia occidentalis

Social wasps do not possess a sophisticated, signal-based mechanism for recruiting foragers to food resources. Instead, in some species na?ve potential foragers use cues, specifically the scent of a resource obtained from successful foragers, to help locate the resource in the field. Prior studies have focused on the effectiveness of this mechanism on increasing the number of foragers at an artificial resource in the field; the increase is typically modest. Here, we focus on the activity at the nest in Polybia occidentalis, a tropical social wasp, and quantify the magnitude of the effect an influx of a known amount of scented carbohydrate solution added directly to the nest has on activating foragers to leave the nest in search of the resource. Under our experimental conditions, adding a scented 2.0 M sucrose solution to the nest doubled the average rate of departure. No increase occurred when the same amount of water was added as a control. This mass activation of foragers may give colonies of this species a competitive edge by enhancing their ability to rapidly exploit new resources.     

Task-Related Variation of Cuticular Hydrocarbon Profiles Affect Nestmate Recognition in the Giant ant Dinoponera quadriceps

Recognition seems to be one of the more remarkable characteristics of social groups. In social insects, cuticular hydrocarbons are important for colonial recognition by providing a chemical signature for colony members. The acceptance threshold model predicts that colony members will accept conspecifics when the levels of nest mate cues dissimilarities are below the acceptance threshold. We tested the hypothesis that the encounter of a guard ant worker with a nurse may cause a delay in the process of recognition, because nurses from distinct colonies may share greater amount of chemical compounds. Dinoponera quadriceps guard workers decreased their effectiveness to recognize nurses rather than did to foragers. Alien foragers received significantly more bites and other stronger acts than non-nestmate nurses when they were experimentally introduced. In addition, guards took significantly more time to react against non-nestmate nurses than against alien foragers. Analysis of the cuticular hydrocarbon profiles corroborated our behavioural analysis that nurses from distinct colonies overlap greater amount of cuticular hydrocarbons.     

The effects of age and social interactions on innate immunity in a leaf-cutting ant

Both developmental and environmental factors shape investment in costly immune defences. Social insect workers have different selection pressures on their innate immune system compared to non-social insects because workers do not reproduce and their longevity affects the fitness of relatives. Furthermore, hygienic behavioural defences found in social insects can result in increased survival after fungal infection, although it is not known if there is modulation in physiological immune defence associated with group living vs. solitary living.Here we investigated whether physiological immune defence is affected by both age and the short-term presence or absence of nestmates in the leaf-cutting ant Acromyrmex octospinosus. We predicted that older ants would show immune senescence and that group living may result in prophylactic differences in immune defence compared to solitarily kept ants. We kept old and young workers alone or in nestmate groups for 48 h and assayed a key innate immune system enzyme, expressing phenoloxidase (PO) and its stored precursor (proPO), a defence that acts immediately, i.e. it is constitutive. Short-term solitary living did not affect PO or proPO levels relative to group living controls and we found no evidence for immunosenescence in proPO. However, we found a significant increase in active PO in older workers, which is consistent with two non-mutually exclusive explanations: it could be an adaptive response or indicative of immunosenescence. Our results suggest that future studies of immunosenescence should consider both active immune effectors in the body, such as PO, and the stored potential to express immune defences, such as proPO.     

Growth-related changes in predation behavior in incipient colonies of the ponerine antEctatomma tuberculatum (Olivier)

Summary We traced the development in the laboratory of 18 young colonies of the arboricolous ponerine antEctatomma tuberculatum. Colony foundation is of the partially-claustral type. During the early stages, when the colony is entirely dependent on the queen's behavior, the growth of the colony in terms of number of workers produced over time was relatively predictable. Afterwards, divergence in colony growth in function of the time increases as fast as the number of workers influences the efficiency of colony provisioning.Comparative analysis indicated clear changes in the predation behavior of foundresses and workers as colonies developed. For any stage of colony growth, all individuals provisioned the nest with dead prey or sugar-rich substances in the same way. However, prey hunting involves two different strategies. Foundresses and nanitic workers (originating from colonies with 9–15 workers) foraged actively, catching prey as the result of random encounters. Post-nanitic foragers (originating from colonies with 20–30 workers) and those from nature colonies developed an ambush strategy. Workers in these colonies gained experience at catching and handling prey during a period when they acted as nest guards, and so tended to be more efficient hunters than poorly experienced foundresses or nanitic foragers. The change in strategy was also positively correlated with an increase in the size of workers as the colony matured. A stable maximum in workers size is apparently reached only after the appearance of efficiently hunting foragers, presumably in numbers sufficient to provide adequate quantity and quality of larval food. Such a correlation between worker size and colony growth, assumed general for all ants, has not been demonstrated for Ponerinae before this work.     

Use of terrestrial chemical trails for nest orientation in an open nesting wasp, <Emphasis Type="Italic">Dolichovespula saxonica</Emphasis> F.

Summary The long-cheeked wasp Dolichovespula saxonica typically constructs exposed nests which can be reached by flying. Usually foragers do not walk on substrates in the close vicinity of the nests as cavity breeding wasps do (Steinmetz et al., 2002). Unexpectedly, when forced to walk outside the nest instead of flying in an artificial tunnel system, D. saxonica foragers lay a terrestrial trail and use it for orientation in the nest area in our experiments. 41% of the foragers followed the trail in a direction they were not accustomed to. We suggest that the foragers have employed the same orientation cues normally used for orientation in the close vicinity of the nest when approaching a free-hanging nest by flying, for example nest odour. Nest odour substances may have been transferred to the substrate as a trail as a consequence of foragers walking through the tunnels.Received 23 August 2002; revised 27 January 2003; accepted 30 April 2003.