Worker connectivity: a review of the design of worker communication systems and their effects on task performance in insect societies

Within-group communication is a fundamental feature of animal societies. In order for animal groups to function as adaptive units, the members must share information such that group mates respond appropriately to each others’ behavior. One important function of social communication is to affect the allocation of tasks among group members. Theoretical and empirical findings on a diverse array of social insect taxa show that interactions among workers often play important roles in structuring division of labor. We review worker interactions that regulate division of labor in insect societies, which we refer to as worker connectivity. We present a framework for synthesizing and analyzing the study of worker connectivity. The widespread reliance on worker connectivity among eusocial insect taxa and the diversity of communicative mechanisms used to recruit workers suggest that the nature of worker interactions has evolved by natural selection. We suggest that colony-level selection acting on variation in task allocation has been an important force in the evolution of mechanisms for worker connectivity. We also propose that there are important links between individual worker cognition and task allocation at the colony level. Evolutionary changes in the cognitive aspects of worker responses may affect task allocation as much as changes in the communicative signals themselves. Received 9 December 2006; revised 18 May 2007; accepted 30 May 2007.     

Worker reproductive competition affects division of labor in a primitively social paperwasp (Polistes instabilis)

Social insects are premier models for studying the evolution of self-organization in animal societies. Primitively social species may be informative about the early stages of social evolution and transitions in self-organization. Previous worker removal studies in Polistes instabilis paper wasps suggested that dominant but non-egglaying workers play an important role in regulating rates of task performance by inducing foraging in subordinates. We extend previous worker removal studies by quantifying changes in individuals’ behavior following removals, and by measuring associations between behavioral change and individuals’ reproductive capacity (ovary development). Workers changed their rates of aggressive behaviors more than queens following the dominant worker removals. Increases in worker’s rates of aggressive behaviors were correlated with decreases in their foraging rates. Changes in individual rates of social aggression were associated with their reproductive capacity: worker females with well-developed ovaries increased their rates of aggression. Further changes in rates of aggression after the dominant workers were returned also depended on ovary development. These patterns suggest that task performance and potential fecundity are linked in workers, and that worker interactions play a strong role in regulating task performance. We conclude that worker reproductive competition may have influenced the evolution of colony organization in social insects. Received 6 June 2008; revised 11 August 2008; accepted 12 August 2008.     

Worker demography in a large-colony,swarm-founding wasp

Neotropical swarm-founding wasps build nests enclosed in a covering envelope, which makes it difficult to count individual births and deaths. Thus, knowledge of worker demography is very limited for swarm-founding species compared with that for independent-founding species. In this study, we explored the worker demography of the swarm-founding wasp Polybia paulista, the colony size of which usually exceeds several thousand adults. We considered each wasp colony as an open-population and estimated the survival probability, recruitment rate, and population size of workers using the developments of the Cormack–Jolly–Seber model. We found that capture probability varied considerably among the workers, probably due to age polyethism and/or task specialization. The daily survival rate of workers was high (around 0.97) throughout the season and was not related to the phase of colony development. On the other hand, the recruitment rate ranged from 0 to 0.37, suggesting that worker production was substantially less important than worker survival in determining worker population fluctuations. When we compared survival rates among worker groups of one colony, the mean daily survival rate was lower for founding workers than for progeny workers and tended to be higher in progeny workers that emerged in winter. These differences in survivorship patterns among worker cohorts would be related to worker foraging activity and/or level of parasitism.     

The influence of the vibration signal on worker interactions with the nest and nest mates in established and newly founded colonies of the honey bee, Apis mellifera

Honey bees adjust cooperative activities to colony needs, based in part on information acquired through interactions with the nest and nest mates. We examined the role of the vibration signal in these interactions by investigating the influence of the signal on the movement rates, cell inspection activity, and trophallaxis behavior of workers in established and newly founded colonies of the honey bee, Apis mellifera. Compared to non-vibrated control bees, vibrated recipients in both colony types exhibited increased movement through the nest and greater cell inspection activity, which potentially increased contact with stimuli that enhanced task performance. Also, compared to controls, recipients in both colony types showed increased rates of trophallactic interactions and spent more time engaged in trophallaxis, which potentially further increased the acquisition of information about colony needs. The vibration signal may therefore help to organize labor in honey bees in part by increasing the rate at which workers obtain information about their colony. Vibrated recipients in the established and newly founded colonies did not differ in any aspect of behavior examined, suggesting that colony developmental state did not influence the degree to which individual workers responded to the signal. However, previous work has demonstrated that newly founded colonies have increased levels of vibration signal behavior. Thus, the vibration signal may help to adjust worker activity to colony conditions partly by stimulating greater numbers of bees to acquire information about colony needs, rather than by altering the level at which individual recipients react to the signal. Received 23 October 2006; revised 15 January 2007; accepted 7 February 2007.     

Socially peaceful: foragers of the eusocial bee Lasioglossum malachurum are not aggressive against non-nestmates in circle-tube arenas

Due to the universally found nestmate recognition in eusocial insects, it is predictable that non-nestmates interact aggressively. In sweat bees (Hymenoptera: Halictidae), this trend was largely shown for queen–queen interactions, but data on worker–worker interactions are still scarce and somehow controversial. We studied behavioural interactions between foragers of the eusocial and ground-nesting bee Lasioglossum malachurum within circle-tubes. Independently of colony membership, bees exhibited high frequencies of cooperative behaviours, together with lack of aggression and moderate avoidance of social interactions. The cooperative mutual passing was the most frequently recorded behaviour. Size difference between the opponents had no effects on cooperation or avoidance. In a heterospecific experiment, bee foragers were observed to react more aggressively and to pass very rarely towards cuckoo bees, suggesting that our results were not biased by the circle-tube methodology. Our results and comparisons with other bee species suggest that studying worker interactions may be not enough to predict the social organisation in bees. Whatever the evolutionary meaning of this generalised tolerance towards conspecifics, the present findings are somehow in agreement with recent studies showing that L. malachurum colonies may have imperfect nestmate recognition and often include a mixture of related and unrelated workers.     

Workers, sexuals, or both? Optimal allocation of resources to reproduction and growth in annual insect colonies

Understanding decisions about the allocation of resources into colony growth and reproduction in social insects is one of the challenging issues in sociobiology. In their seminal paper, Macevicz and Oster predicted that, for most annual insect colonies, a bang–bang strategy should be favoured by selection, i.e. a strategy characterised by an “ergonomic phase” with exponential colony growth followed by a “reproductive phase” with all resources invested into the production of sexuals. Yet, there is empirical evidence for the simultaneous investment into the production of workers and sexuals in annual colonies (graded control). We, therefore, re-analyse and extend the original model of Macevicz and Oster. Using basic calculus, we can show that sufficiently strong negative correlation between colony size and worker efficiency or increasing mortality of workers with increasing colony size will favour the evolution of graded allocation strategies. By similar reasoning, graded control is predicted for other factors limiting colony productivity (for example, if queens’ egg laying capacity is limited).     

Potential and realized reproduction by different worker castes in queen-less and queen-right colonies of <Emphasis Type="Italic">Pogonomyrmex badius</Emphasis>

Workers of the Florida harvester ant (Pogonomyrmex badius), the only North American Pogonomyrmex with a polymorphic worker caste, produce males when colonies are orphaned. In this study,we assessed the reproductive potential of workers of each caste group, minors and majors, in the presence and absence of the queen, and tested whether males produced in natural queen-right colonies are derived from workers. Worker size was positively correlated with ovariole number such that major workers had approximately double the number of ovarioles as minor workers. The number of vitellogenic oocytes, a measure of reproductive potential, was greater in major compared to minor workers and increased in both worker castes when queens were removed. Major workers have greater reproductive potential than minors although they represent a minority within the colony (~5% of workers are majors). Worker produced eggs were visible in colonies 28 – 35 days after queen removal. This time lag, from queen removal to egg production, is similar to other ants and bees. Though workers are capable of producing viable eggs, we found no evidence that they do so in queen-right colonies, suggesting that worker reproduction is controlled via some social mechanism (self restraint, policing, or inhibition). This result supports predictions of kin selection theory – that due to multiple mating by the queen workers are more related to queen-produced males than most worker-produced males and should thus favor reproduction by the queen and inhibit reproduction by other workers. Received 25 January 2007; revised 1 May 2007; accepted 21 May 2007.     

Queen–worker caste ratio depends on colony size in the pharaoh ant (<Emphasis Type="Italic">Monomorium pharaonis</Emphasis>)

The success of an ant colony depends on the simultaneous presence of reproducing queens and non-reproducing workers in a ratio that will maximize colony growth and reproduction. Despite its presumably crucial role, queen–worker caste ratios (the ratio of adult queens to workers) and the factors affecting this variable remain scarcely studied. Maintaining polygynous pharaoh ant (Monomorium pharaonis) colonies in the laboratory has provided us with the opportunity to experimentally manipulate colony size, one of the key factors that can be expected to affect colony level queen–worker caste ratios and body size of eclosing workers, gynes and males. We found that smaller colonies produced more new queens relative to workers, and that these queens and workers both tended to be larger. However, colony size had no effect on the size of males or on the sex ratio of the individuals reared. Furthermore, for the first time in a social insect, we confirmed the general life history prediction by Smith and Fretwell (Am Nat 108:499–506, 1974) that offspring number varies more than offspring size. Our findings document a high level of plasticity in energy allocation toward female castes and suggest that polygynous species with budding colonies may adaptively adjust caste ratios to ensure rapid growth.     

Queen replacement in African and European honey bee colonies with and without afterswarms

We examined the dynamics of the queen replacement process in African and European colonies that did and did not produce afterswarms. In colonies without afterswarms, the queen replacement process was completed in 24–48 hours, the first-emerging virgin queen (VQ) typically inherited the natal nest even if multiple queens emerged, workers performed few vibration signals on emerged queens, and all signaling activity was directed toward early emerging VQs. In contrast, if colonies did produce afterswarms, the queen replacement process required 5–6 days, there was no advantage for first-emerging queens, vibration rates on emerged queens were 25 times greater, and signaling activity was directed toward all VQs. Although vibration signal activity was more pronounced in colonies with afterswarms, the signal was consistently associated with increased VQ survival under all conditions. These trends were exhibited similarly in the African and European colonies, suggesting that they have broad applicability to queen-replacement decisions over a range of environmental and racial conditions. However, the African and European colonies differed in the total number of queens involved in the elimination process and the relative importance of queen duels and pre-emergence destruction under the different reproductive strategies. Taken together, our results suggest that worker behavior is a major determinant for the outcome of queen replacement, either through reduced interactions that allow first-emerged queens to rapidly eliminate rivals, or through increased use of interactions such as the vibration signal, which may allow workers to influence the ultimate fate of each emerged VQ. We discuss the possibility that these behavior patterns may reflect the roles of cooperation and conflict in shaping honey bee reproductive decisions. Received 8 May 2007; revised 7 November 2007; accepted 20 November 2007.     

A trade-off in task allocation between sensitivity to the environment and response time

Task allocation is the process that adjusts the number of workers in each colony task in response to the environment. There is no central coordination of task allocation; instead workers use local cues from the environment and from other workers to decide which task to perform. We examine two aspects of task allocation: the sensitivity to the environment of task distribution, and the rate of response to environmental changes. We investigate how these two aspects are influenced by: (1) colony size, and (2) behavioral rules used by workers, i.e. how a worker uses cues from the environment and from social interactions with other workers in deciding which task to perform. We show that if workers use social cues in their choice of task, response time decreases with increasing colony size. Sensitivity of task distribution to the environment may decrease or not with colony size, depending on the behavioral rules used by workers. This produces a trade-off in task allocation: short response times can be achieved by increasing colony size, but at the cost of decreased sensitivity to the environment. We show that when a worker's response to social interactions depends on the local environment, sensitivity of task distribution to the environment is not affected by colony size and the trade-off is avoided.     

A modeling approach to swarming in honey bees (Apis mellifera)

Identifying the mechanisms of colony reproduction is essential to understanding the sociobiology of honey bees. Although several proximate causes leading to the initiation of queen rearing – an essential prerequisite to swarming – have been proposed, none have received unequivocal empirical support. Here we model the main proximate hypotheses (colony size, brood comb congestion, and worker age distribution) and show that all proposed swarming triggers occur as a function of the ultimate cause of a colony reaching replacement stability, the point at which the queen has been laying eggs at her maximal rate. We thus present a reproductive optimization model of colony swarming based on evolutionary principles. All models produce results remarkably similar both to each other and to empirically-determined swarming patterns. An examination of the fit between the individual models and swarm-preventing techniques used by beekeepers indicates that the reproductive optimization model has a relatively broad explanatory range. These results suggest that an examination into the behavioral correlates of a queen’s maximum egg laying rate may provide a unified proximate mechanistic trigger leading predictably to colony fission. Generating a predictive model for this very well studied animal is the first step in producing a model of colony fission applicable to other swarm-founding eusocial animals. Received 16 November 2004; revised 31 May 2005; accepted 27 June 2005.     

How brood influences caste aggregation patterns in the dimorphic ant species Pheidole pallidula

Spatial distribution of ant workers and, notably their aggregation/segregation behaviour, is a key-element of the colony social organization contributing to the efficiency of task performance and division of labour. In polymorphic species, specialized worker castes notably differ in their intrinsic aggregation behaviour. In this context, knowing the preponderant role of minors in brood care, we investigate how a stimulus such as brood can influence the spatial patterns of Pheidole pallidula worker castes. In a homogeneous area without brood, it was shown that minors display only a low level of aggregation while majors form large clusters in the central area. Here we find out that these aggregation patterns of both minors and majors can be deeply influenced by the presence of brood. For minors, it nucleates or enhances the formation of a large stable cluster. Such high sensitivity of minors to brood stimuli fits well with their role as main brood tenders in the colony. For majors, interattraction between individuals still remains the prevailing aggregation factor while brood strongly influences the localisation of their cluster. We discuss how the balance between interattraction and sensitivity to environmental stimuli determines the mobility of each worker castes and, consequently, the availability of minors and majors to participate in everyday colony tasks. Moreover, we will evoke the functional value of majors’ cluster location close to the brood, namely with respect to social regulation of the colony caste ratio. Received 30 May 2005; revised 11 January 2006; accepted 13 January 2006.     

<Emphasis Type="Italic">Polistes japonicus</Emphasis> (Hymenoptera,Vespidae) queens monopolize ovipositing but are not the most active aggressor in dominant-subordinate interactions

In order to elucidate the dominant–subordinate relationship between the foundress and workers, five colonies of the paper wasp Polistes japonicus were observed in a netted and covered cage located outdoors. The number of workers in each colony ranged from four to eight. Workers were divided into first and second broods. Abdominal wagging and ovipositing were performed almost exclusively by the foundress throughout colony development. However, an analysis of aggressive encounters indicated that although the foundress hardly received dominance behaviors (aggression) from workers, it lacked either partially or completely the following characteristics of the queen that are usually seen in paper-wasp colonies with independent-founding queens (except in one colony that produced no second brood): the queen being socially dominant over any worker (the queen had more wins than losses in one-on-one dominance contests with any worker), exhibiting the highest frequency of dominance behaviors, and directing dominance behaviors primarily toward the socially most-dominant worker. In particular, during the mixed-brood period (when all first- and second-brood workers were present on the nest) the foundress hardly exhibited dominance behaviors toward socially dominant workers (mainly second brood) but frequently directed dominance behaviors toward socially subordinate workers (mainly first brood). The foundress disappeared in two colonies before the reproductives emerged; in these colonies the socially most-dominant worker inherited the colony and laid many eggs. The frequency of abdominal wagging by these two foundresses decreased during colony development, while it did not in the other colonies. This suggests that abdominal wagging provides information about the vigor of the performer. The superseder was socially dominant over all other workers, but spent little time wagging its abdomen and allowed some workers to lay eggs.     

Respiratory rhythms in stingless bee workers: circadian and ultradian components throughout adult development

The workers of the stingless bee, Melipona quadrifasciata, assume different tasks during their adult life. Newly emerged individuals remain inside the nest, without contact with the external environment. Maturing workers go to more peripheral regions and only the oldest, the foragers, leave the nest. As this diversity of activities implies different metabolic patterns, oxygen consumption has been measured in workers of three different ages: 24–48 h (nurses), 10–15 days (builders), and older than 25 days (foragers). Oxygen consumption of individually isolated workers was determined by intermittent respirometry, under constant darkness and temperature of 25 ± 1°C. Sets of 24-h measurements were obtained from individuals belonging to each of the three worker groups. Rhythmicity has been assessed in the daily (24 h) and ultradian (5–14 h) domains. This experimental design allowed detection of endogenous rhythms without the influence of the social group and without inflicting stress on the individuals, as would be caused by their longer isolation from the colony. Significant 24-h rhythms in oxygen consumption were present in nurses, builders and foragers; therefore, workers are rhythmic from the age of 24–48 h. However, the amplitude of the circadian rhythm changed according to age: nurses showed the lowest values, while foragers consistently presented the largest ones, about ten times larger than the amplitude of nurses’ respiratory rhythm. Ultradian frequencies were detected for all worker groups, the power and frequencies of which varied little with age. This means that the ultradian strength was relatively larger in nurses and apparently maintains some relationship with the queen’s oviposition episodes.     

Optimal Reproduction Strategies in Two Species of Mound-Building Termites

We formulate a mathematical model for food collection and production of workers and nymphs in 2 species of mound building termites. We maximise the number of nymphs (reproductives) produced by each colony over its lifetime with respect to the proportion of eggs that hatch as nymphs as opposed to workers. The results predict that food storage has a very important influence on the pattern of nymph and worker production. Food storage affects the part of the year that nymph production dominates, whether nymphs and workers are produced at the same time or not, and the existence of a final phase in the colony’s life when a very large number of nymphs but no workers are produced.     

Social inhibition and the regulation of temporal polyethism in honey bees.

Honey bee division of labor is characterized by temporal polyethism, in which young workers remain in the hive and perform tasks there, whereas old workers perform more risky outside tasks, mainly foraging. We present a model of honey bee division of labor based on (1) an intrinsic process of behavioral development and (2) inhibition of development through social interactions among the workers in a colony. The model shows that these two processes can explain the main features of honey bee temporal polyethism: the correlation between age and task performance; the age at which a worker first forages and how this age varies among hives; the balanced allocation of workers to hive tasks and foraging; the recovery of a colony from demographic perturbations; and the differentiation of workers into different behavioral roles. The model provides a baseline picture of individual and colony behavior that can serve as the basis for studies of more fine-grained regulation of division of labor.     

Prey weight and overwhelming difficulty impact the choice of retrieval strategy in the Neotropical ant <Emphasis Type="Italic">Gnamptogenys sulcata</Emphasis> (F. Smith)

By regulating both the choice between solitary or collective retrieval and the level of nestmate investment for heavy prey transport, individual hunters of the ant Gnamptogenys sulcata are able to increase the foraging efficiency of the whole society, despite the extremely small size of this elite group (1 –4 hunters per colony). Their predatory behavior changes according to the static (weight, size, shape) and dynamic (mobility, escape behaviors) characteristics of the prey. The behavioral sequences resemble those of other poneromorph ants, but palpation after the approach phase is absent, probably because of the swiftness of the attack. Hunting is always performed by solitary workers but, independently of prey type and mobility, small, light prey trigger solitary retrieval whereas large, heavy prey trigger collective retrieval. For intermediate prey weights (8.5 to 21 times the hunter’s weight), some variability in the strategy choice is encountered. Both static and dynamic factors are involved in assessing the difficulty of handling living prey as shown by the number of stings delivered by the hunter for prey immobilization. However, the lack of any stinging against already dead prey indicates that these factors must be uncoupled when selecting retrieval strategies. Prey weight has a major role in this choice. For a given prey size always triggering solitary retrieval, a two-fold increase in prey weight is sufficient to trigger collective transport. Conversely, for a given prey size always triggering collective retrieval, a decrease in prey weight can trigger solitary transport. Moreover, presenting hunters with prey of “infinite” weight triggers several waves of recruitment, so that the number of recruited workers compensates for the “apparent” prey weight. Despite the inability to finely match the number of recruits to the weight of retrieved prey, recruitment strategies adopted by G. sulcata may reflect an evolutionary primitive step towards the finely graded recruitment behavior observed in closely related poneromorph species. Received 5 February 2007; revised 25 May 2007; accepted 15 June 2007.     

Worker policing in the common wasp Vespula vulgaris is not aimed at improving colony hygiene

In insect societies, eggs laid by workers are frequently killed by other workers – a behaviour known as “worker policing”. The traditional explanation of worker policing is that it is a mechanism to resolve intracolony conflict, and maintain the reproductive monopoly of the queen. Recently, Pirk et al. (2004) proposed that worker policing instead is aimed at removing unviable worker-laid eggs and is ultimately just another example of hygienic behaviour. Here we test this hypothesis for the common wasp Vespula vulgaris, a species with highly effective worker policing. We show that worker-laid eggs from queenless colonies have a lower hatch rate (68%) than queen-laid eggs (82%). Analysis of egg laying rates of queens and workers, however, shows that the difference is not big enough to explain the apparent absence of adult worker-derived males in this species. Received 30 January 2006; revised 2 May 2006; accepted 5 May 2006.     

Absence of Nepotism in Worker–Queen Care in Polygynous Colonies of the Ant Ectatomma tuberculatum

The question of the occurrence of nepotism in insect societies is central to inclusive fitness theory. Here we investigated the existence of nepotism in the facultative polygynous ant Ectatomma tuberculatum because various characteristics of this species may have favored the evolution of nepotistic behavior toward queens. We thus studied worker–queen care toward their mother queen vs. an unrelated unfamiliar queen, to determine if workers cared preferentially for their mother. Although we tried to facilitate the expression of nepotistic behaviors, we did not detect significant nepotism confirming the general trend of an absence of nepotism in social insects. We discuss about the specific causes that can explain the absence of nepotism in E. tuberculatum regarding the particular social organization of this species and its ecological dominance in the mosaic of arboreal ants.     

Development rate and brood production in haplo- and pleometrotic colonies of <Emphasis Type="Italic">Oecophylla smaragdina</Emphasis>

Pleometrosis (colony founding by multiple queens) may improve life history characteristics that are important for early colony survival. When queens unite their initial brood, the number of workers present when incipient colonies open may be higher than for single queen colonies. Further, the time until the first worker emerges may shorten. For territorial species and species that rob brood from neighbouring colonies, a faster production of more workers may improve the chance of surviving intraspecific competition. In this study, the time from the nuptial flight to the emergence of the first worker in incipient Oecophylla smaragdina Fabr. colonies founded by 1–5 queens was compared and the production of brood during the first 68 days after the nuptial flight was assessed. Compared to haplometrotic colonies, pleometrotic colonies produced 3.2 times more workers, their first worker emerged on average 4.3 days (8%) earlier and the queen’s per capita egg production almost doubled. Further, colony production was positively, correlated with the number of founding queens and time to worker emergence was negatively correlated. These results indicate that pleometrotic O. smaragdina colo-nies are competitively superior to haplometrotic colonies as they produce more workers faster and shorten the claustral phase, leading to increased queen fecundity.