The influence of social structure on brood survival and development in a socially polymorphic ant: insights from a cross‐fostering experiment

Animal societies vary in the number of breeders per group, which affects many socially and ecologically relevant traits. In several social insect species, including our study species Formica selysi, the presence of either one or multiple reproducing females per colony is generally associated with differences in a suite of traits such as the body size of individuals. However, the proximate mechanisms and ontogenetic processes generating such differences between social structures are poorly known. Here, we cross‐fostered eggs originating from single‐queen (= monogynous) or multiple‐queen (= polygynous) colonies into experimental groups of workers from each social structure to investigate whether differences in offspring survival, development time and body size are shaped by the genotype and/or prefoster maternal effects present in the eggs, or by the social origin of the rearing workers. Eggs produced by polygynous queens were more likely to survive to adulthood than eggs from monogynous queens, regardless of the social origin of the rearing workers. However, brood from monogynous queens grew faster than brood from polygynous queens. The social origin of the rearing workers influenced the probability of brood survival, with workers from monogynous colonies rearing more brood to adulthood than workers from polygynous colonies. The social origin of eggs or rearing workers had no significant effect on the head size of the resulting workers in our standardized laboratory conditions. Overall, the social backgrounds of the parents and of the rearing workers appear to shape distinct survival and developmental traits of ant brood.     

E-β-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera)

BACKGROUND: In honey bee colony, the brood is able to manipulate and chemically control the workers in order to sustain their own development. A brood ester pheromone produced primarily by old larvae (4 and 5 days old larvae) was first identified as acting as a contact pheromone with specific effects on nurses in the colony. More recently a new volatile brood pheromone has been identified: E-β-ocimene, which partially inhibits ovary development in workers. METHODOLOGY AND PRINCIPAL FINDING: Our analysis of E-β-ocimene production revealed that young brood (newly hatched to 3 days old) produce the highest quantity of E-β-ocimene relative to their body weight. By testing the potential action of this molecule as a non-specific larval signal, due to its high volatility in the colony, we demonstrated that in the presence of E-β-ocimene nest workers start to forage earlier in life, as seen in the presence of real brood. CONCLUSIONS/SIGNIFICANCE: In this way, young larvae are able to assign precedence to the task of foraging by workers in order to increase food stores for their own development. Thus, in the complexity of honey bee chemical communication, E-β-ocimene, a pheromone of young larvae, provides the brood with the means to express their nutritional needs to the workers.     

Effects of brood parasitism on host reproductive success: evidence from larval interactions among dung beetles

This paper investigates the effect of brood parasitism in a dung beetle assemblage in an arid region of Spain. The study was conducted during the spring season (March-May 1994-1998) using mesh cylinders buried into the ground, filled with sand and with sheep dung on top. We quantified the proportion of nests containing larvae of parasitic beetles and their effect on host larvae survival. Experiments on the effect of parasitic larvae on host-larvae survival were conducted by placing scarab brood masses (raised from captive scarabs in the laboratory) in containers with and without aphodiid larvae. During the spring, dung desiccation is rapid, preventing aphodiids nesting in the dung, and forcing these species to adopt brood parasitism as a nesting strategy. Parasitic aphodiids were found in 12-47% of scarab nests of three species. The incidence of brood parasitization was positively related with the number of brood masses contained in the nests, being also higher in the most abundant species. Field data and experiments showed that brood parasites significantly reduced host larvae survival from 74.8% in non-parasitized nests to 8.8% in parasitized nests. Because different rates of nest parasitization and mortality were caused by parasites, brood parasitism had a differential effect on different host species. Thus, brood parasitism constitutes an important mortality factor reducing the reproductive success of the host species and potentially affecting the beetle abundance in the area.     

Drone and Worker Brood Microclimates Are Regulated Differentially in Honey Bees,Apis mellifera

Background

Honey bee (Apis mellifera) drones and workers show differences in morphology, physiology, and behavior. Because the functions of drones are more related to colony reproduction, and those of workers relate to both survival and reproduction, we hypothesize that the microclimate for worker brood is more precisely regulated than that of drone brood.

Methodology/Principal Findings

We assessed temperature and relative humidity (RH) inside honey bee colonies for both drone and worker brood throughout the three-stage development period, using digital HOBO^® Data Loggers. The major findings of this study are that 1) both drone and worker castes show the highest temperature for eggs, followed by larvae and then pupae; 2) temperature in drones are maintained at higher precision (smaller variance) in drone eggs and larvae, but at a lower precision in pupae than the corresponding stages of workers; 3) RH regulation showed higher variance in drone than workers across all brood stages; and 4) RH regulation seems largely due to regulation by workers, as the contribution from empty honey combs are much smaller compared to that from adult workers.

Conclusions/Significance

We conclude that honey bee colonies maintain both temperature and humidity actively; that the microclimate for sealed drone brood is less precisely regulated than worker brood; and that combs with honey contribute very little to the increase of RH in honey bee colonies. These findings increase our understanding of microclimate regulation in honey bees and may have implications for beekeeping practices.     

Caste regulation in the pharaoh's ant Monomorium pharaonis: recognition and cannibalism of sexual brood by workers

Abstract In colonies of the pharaoh's ant Monomorium pharaonis (L), new males and queens can be produced at any time by the removal of the inhibitory effect of the presence of existing fertile queens. When queens are absent, workers rear sexual larvae and will also accept sexual larvae introduced from other nests. However, in the presence of fertile queens workers cannibalize sexual brood, and will not accept male or queen larvae or pre-pupae from other nests, although worker brood is always accepted and reared. Worker larvae are covered in bifurcated hairs, whereas sexual larvae are essentially hairless. Workers may use these morphological cues to distinguish between sexual and worker brood stages.     

The influence of brood type on activity cycles inLeptothorax allardycei (Hymenoptera: Faruicidae)

We investigated the effect that different categories of brood had on the production of periodic activity within artificial aggregates of the ant,Leptothorax allardycei. Colonies of this species exhibit periodic patterns of movement activity with a period of approximately 20–30 min. Artificial aggregates of this species show that periodic activity appears gradually as the number of workers in the aggregate increases to 15 workers. In addition, it has been noted that the presence of brood with the workers makes the periodic activity more pronounced. In this paper we investigate the effect that four categories of brood had on the periodic activity of worker ants. Eggs, small larvae, large larvae, and pupae were tested with four different-sized aggregates of workers. We hypothesized that brood care is responsible for the increase in periodic activity and therefore that larvae (which require more tending) would be more effective at increasing periodic activity than eggs or pupae. Contrary to our expectations, eggs and both size categories of larvae were equally effective in enhancing periodicity in our experimental aggregates. Pupae, in contrast, were completely ineffective at enhancing periodic activity. We discuss some possible reasons for the differential effects of eggs, larvae, and pupae on the behavior of worker ants.     

Behavioural and chemical studies of discrimination processes in the leaf-cutting ant Acromyrmex laticeps nigrosetosus (Forel, 1908).

Leaf-cutting ants live in symbiosis with a basidiomycete fungus that is exploited as a source of nutrients for ant larvae. Tests of brood transport revealed that Acromyrmex laticeps nigrosetosus workers did not discriminate a concolonial brood from an alien brood. The same result was observed with tests of fungus transport. Adult workers showed no aggressive behaviour to workers from other alien colonies (non-nestmates). There was no qualitative variation in the chemical profiles of larvae, pupae and adult workers from the different colonies. However, quantitative differences were observed between the different colonies. Hypotheses about the lack of intraspecific aggression in this subspecies of ants are discussed.     

Honey bee hygienic behaviour does not incur a cost via removal of healthy brood

In the honey bee, hygienic behaviour, the removal of dead or diseased brood from capped cells by workers, is a heritable trait that confers colony‐level resistance against brood diseases. This behaviour is quite rare. Only c. 10% of unselected colonies show high levels of hygiene. Previous studies suggested that hygiene might be rare because it also results in the removal of healthy brood, thereby imposing an ongoing cost even when brood diseases are absent. We tested this hypothesis by quantifying hygienic behaviour in 10 colonies using a standard technique, the freeze‐killed brood (FKB) bioassay. At the same time, we also quantified the removal of untreated brood. The study colonies showed a wide range in hygienic behaviour, removing 19.7–100% of the FKB. The removal of untreated brood ranged from 2% to 44.4%. However, there was no correlation between the two removal rates for any of the four age groups of untreated brood studied (eggs, young larvae, older larvae from uncapped cells and larvae/pupae from capped cells). These results do not support the cost‐to‐healthy‐brood hypothesis for the rarity of hygienic behaviour.     

Behavioral and developmental homeostasis in the fire ant, Solenopsis invicta

The von Bertalanffy rule (1960) predicts that low incubation temperature during larval development will result in larger adult body size. If larval development in social insects followed this rule, then low incubation temperature would induce the development of larger workers and possibly even sexuals. To test this prediction, the effect of incubation temperature on larval development, larval meal size, larval tending and worker recruitment to food in the fire ant, Solenopsis invicta was investigated. Temperatures tested where within the range at which brood remains viable.Contrary to the predictions of the von Bertalanffy rule, worker size was unaffected by incubation temperature, and sexuals were reared at the high rather than the low incubation temperature. Moreover, larval meal size, the rate of larval tending by workers and the total number of workers recruited to food were unaffected by temperature.Mechanisms regulating developmental and behavioral homeostasis were as follows: the duration of larval development and the rate of larval growth changed proportionately with temperature such that the mean and variation of pupal size was unaffected by incubation temperature. Larvae solicited at the same rate, swallowed at the same rate and swallowed for the same duration such that meal size was unaffected by incubation temperature. On the brood pile, fewer workers tended brood at higher incubation temperatures, but worker tempo increased; as a result, brood tending was not adversely affected by incubation temperature. The rate of worker recruitment to food sites outside the nest increased with temperature, but the duration of the recruitment effort decreased such that, over time, the same total number of workers was employed to retrieve food.Incubation humidity was also investigated. When brood chambers were less than 100% humid, workers recruited to food and tended larvae (retrieved, sorted and groomed them), but did not feed larvae. Eventually, larvae died of starvation and were cannibalized.     

Effects of boric acid,fipronil, hydramethylnon,and diflubenzuron baits on colonies of ghost ants (Hymenoptera: Formicidae)

Laboratory colonies of the ghost ant, Tapinoma melanocephalum (F.) were administered sugar solution (10%) baits containing the insecticides boric acid, fipronil (REGENT), hydramethylnon (SIEGE), or diflubenzuron (DIMILN). Colonies were exposed to the baits for 21 d, and development of workers, queens, and brood (larvae and pupae) was observed for 4 wk. Fipronil (0.05%) caused 100% mortality in all colonies the first week. With boric acid (0.5%), 100% mortality of workers, queens, and brood was reached at the end of the third week. With hydramethylnon (2%), 83% of the colonies disappeared at the end of the fourth week, but some queens were still alive 9 wk after the trial started. Diflubenzuron (1%) behaved similarly to the control, although in some colonies, the brood production increased, whereas in other colonies, the queens disappeared. In the control colonies, workers, queens, and brood were always observed even up to 9 wk.     

Nonrandom visitation of brood cells by worker honey bees (Hymenoptera: Apidae)

The visitation pattern by worker honey bees to cells in the brood nest was monitored on an artificially created brood pattern consisting of about one-fourth brood cells evenly distributed among empty cells. The majority (63 %) of the observed workers selectively entered larval cells. In contrast, some workers avoided egg cells when presented a choice of egg vs empty cells. The results suggest that larvae produce a general signal indicating their presence to worker bees. Eggs also seem to produce a signal, which is perceived to be different from the one from larvae.     

Larval cannibalism during the late developmental stages of a facultatively gregarious encyrtid endoparasitoid

• 1 The larvae of many gregarious parasitoid species are usually non‐aggressive when they develop in or on a host, but those of Metaphycus flavus are one of the few exceptions known. Herein we describe their aggressive behaviour and the conditions under which it occurs, using observations in which larval development and physical conflict within parasitised and superparasitised hosts were mapped daily.
• 2 Metaphycus flavus larvae often engaged in physical conflict that resulted in consumption of the losing larvae (= cannibalism ) in superparasitised hosts, whereas such conflict and consumption occurred rarely when a single brood developed in a host.
• 3 Cannibalism among M. flavus larvae only occurred after the host resources had become scarce. Typically it occurred after the sixth day of development (fourth‐instar larvae) when the larvae in a clutch had separated from their aeroscopic plate and were freed of their attachment to the host's cuticle.
• 4 Female larvae in the initial clutch appeared more aggressive than male larvae when a second clutch was allocated 4 h after the first clutch. The probability of a larva being attacked and consumed by a brood mate increased as the number of larvae increased in the host. This partial tolerance might allow the members of the initial brood to defend themselves from offspring of a superparasitising female (= competitors ). Such post‐ovipositional regulation of brood size might be interpreted as high‐density intolerance among female offspring.

     

Energetics and development of incipient colonies of the harvester termite, <Emphasis Type="Italic">Trinervitermes trinervoides</Emphasis> (Sjöstedt) (Termitidae,Nasutitermitinae)

Energy dynamics within incipient colonies of the southern African mound dwelling harvester termite Trinervitermes trinervoides (Sj?stedt) (Termitidae: Nasutitermitinae) were investigated. Development of incipient colonies established from field collected alates and changes in energy content of reproductives and brood were studied over a 25 week period in the laboratory. Colonies were then transferred into the field to study the established of the first mound. An initial four-week egg-laying cycle started within a week of pairing. Hatching occurred six weeks later. Two lines emerged from first instar undifferentiated larvae. Small larvae moulted first into minor presoldiers and then minor soldiers. Large larvae developed into major workers. Foraging began once second instar major workers had differentiated 20 weeks after colony foundation. First instar major workers did not forage but there is evidence of pre-foraging utilisation of soil humus. The epigeous mound was produced after three years. The energy available to maintain incipient termite colonies until the first workers start foraging is crucial to their survival. The royal pair of T. trinervoides does not feed during the rearing of the first brood, the fate of which depends largely on the reproductives accumulated energy reserves. The males and females expended 84.54 and 83.07% respectively of their total energy during this period. Once foraging started, the energy content of the royal pair increased and a second egg-laying cycle began. Received 25 July 2007; revised 19 March and 22 May 2008; accepted 4 September 2008.     

Unequal partitioning of reproduction and investment between cooperating queens in the fire ant,Solenopsis invicta,as revealed by microsatellites

Social insects provide ideal systems for investigating how kinship and ecological factors affect cooperation and conflict. In many ant species, unrelated queens cooperate to initiate new colonies. However, fights between queens break out after the eclosion of the first workers, leading to the death of all but one queen. Queens within associations potentially face a trade-off. On one hand, a queen should restrain her investment in brood production and care if this helps her to maintain fighting ability. On the other hand, a queen may benefit by increasing her contribution to brood production if having more daughter workers than her cofoundresses enhances her chances of taking over the colony. Increased investment is also beneficial because a large brood enhances colony survival. Using microsatellites, we determined the maternity of workers (adults and larvae) at the time of queen execution in the fire ant, Solenopsis invicta. Differential mass loss by initially equal nestmates affected survival, with the queen losing less body mass being more likely to survive. Surprisingly, the queen which lost less body mass, that is the one which provided the lowest energy investment, was the one which achieved higher maternity. A control experiment indicated that interactions among queens are responsible for this differential partitioning of reproductive and investment tasks between nestmates. The finding that the queen most likely to win the fights is the one with above-average maternity may explain why workers apparently do not attempt to influence the outcome of fights.     

Changing colony growth rates inCamponotus floridanus as a behavioral response to conspecific presence (Hymenoptera: Formicidae)

Previous work with the antCamponotus floridanus demonstrated that perception of competition can be clearly differentiated from effects of mortality and decreased resources. That is, brood biomass in ant colonies decreases as a consequence of a behavioral decision(s) rather than because of limited food availability or reduced numbers of brood tenders. The experiments presented here extend that work. Under experimental conditions, colony growth inC. floridanus is modified by distance between brood and unrelated conspecifics and by worker age distribution. When nonnestmates are encountered at the nest versus at a separate foraging site, less brood is maintained by a colony. Although colonies with older workers maintain a brood biomass similar to that of colonies with younger workers, that biomass is concentrated in fewer, larger, more rapidly maturing larvae. These effects seem to be due entirely to worker control.     

Evidence of intracolony transmission of Thelohania solenopsae (Microsporidia: Thelohaniidae) in red imported fire ants (Hymenoptera: Formicidae) and the first report of spores from pupae.

Red imported fire ant, Solenopsis invicta, colonies were infected horizontally by introducing live brood (mainly larvae and pupae) infected with Thelohania solenopsae. Live, infected brood introduced into uninfected colonies were adopted and raised to adulthood instead of being executed by the recipient colony. Introductions of infected larvae with uninfected pupae, which eclose into adult worker caste fire ants, resulted in an 80% infection rate of the inoculated colonies. Infections from introductions of infected pupae with uninfected larvae resulted in a 37.5% infection of inoculated colonies. Infections were also detected in 11.6 and 3.7% of the adult worker caste ants that eclosed from uninfected large larvae and pupae, respectively, that were held with infected adult workers. Microscopic examination of infected brood revealed sporoblasts and large numbers of spores of T. solenopsae in S. invicta pupae.     

Effects of colony-level attributes on larval feeding in the fire ant, Solenopsis invicta

Summary: Do colony attributes modulate individual behavior? The effects of colony size and worker:brood ratio on the rate of worker-to-larva trophallaxis in the fire ant, Solenopsis invicta, were investigated. Neither colony size ranging from 100 to 10,000 nor worker:brood ratio ranging from 1:1 to 16:1 affected the density of workers on the brood pile, nor the rate or duration of worker-to-larva trophallaxis. The demands of hungry larvae were met even in groups as small as 100 workers in worker:brood ratios as small as 1. Only when the worker:brood ratio was less than 1, were larvae tended or fed at reduced rates. Under natural conditions, this occurs only in incipient colonies. Otherwise, in post-incipient colonies, the flow of food to larvae was unmodified by colony attributes. The implications of this finding are two-fold: First, it reinforces previous research demonstrating that social feeding in the fire ant emerges from localized interactions rather than mass communication. Second, it highlights the resiliency of this weedy species. Hypothetically, colonies drastically reduced by catastrophic events such as flooding should still be able to produce sexuals.     

Functional flexibility of the honey bee hypopharyngeal gland in a dequeened colony

The role of the worker honey bee Apis mellifera L. changes depending on age after eclosion (age polyethism): young workers (nurse bees) take care of their brood by synthesizing and secreting brood food (royal jelly), while older workers (foragers) forage for nectar and process it into honey. Previously, we showed that the major proteins synthesized in the hypopharyngeal gland of the worker change from brood food proteins to alpha-glucosidase at the single secretory cell level in parallel with this age polyethism [Kubo et al., J. Biochem. 119, 291-295 (1996); Ohashi et al., Eur. J. Biochem. 249, 797-802 (1997)]. Here, we examined whether the function of the hypopharyngeal gland has flexibility depending on the colony conditions, by creating a dequeened colony in which the older workers were compelled to feed the drone larvae. It was found that most of the older workers in the dequeened colony synthesized brood food proteins as did nurse bees. Furthermore, the percentage of workers that synthesized brood food proteins was maintained at 80-90% of the total workers for at least two months, as in a normal colony. These results indicate that the function of the hypopharyngeal gland cells of the worker has flexibility and can, if necessary, be maintained as that of the nurse bee, depending on the condition of the colony.     

Sociometry and sociogenesis of colonies of the harvester ant, Pogonomyrmex badius: distribution of workers, brood and seeds within the nest in relation to colony size and season

1. The vertical distribution in the nest of chambers, workers, callow workers, brood and seeds was studied in the harvester ant, Pogonomyrmex badius, in northern Florida. On each of four sample dates (May, July, October, January), six to seven colonies, chosen to represent the full range of sizes, were excavated. All chamber contents were collected and counted. Chambers were mapped and measured. In a preliminary study, two nests were excavated after preventing vertical migration by driving barriers into the wall of a pit next to the nest, severing the vertical tunnels. The vertical distribution of these barrier-nests differed little from unrestrained nests, indicating that unrestrained excavation produced a reasonable picture of vertical distributions. 2. Nest depth, chamber number and total area increased with colony size. Chamber area declined sharply with depth, as did chamber number, such that more than half of the total area was found in the upper quarter of the nest. 3. The proportion of dark-coloured (older) workers also declined strongly with depth, but this decline was weaker in the spring, and depended to a modest degree on colony size. Conversely, in the distribution of callow (young) workers, the proportion increased towards the bottom of the nest. Mean worker age was inversely related to the depth at which workers were found. The proportion of the brood also increased towards the bottom of the nest, with worker brood, sexual brood, pupae and larvae all being distributed similarly. 4. By contrast, seeds were stored at a preferred absolute depth between 40 and 100 cm. Colonies shallower than 100 cm stored seeds in their deepest chambers. Larger colonies stored most seeds in the upper third of the nest, but patterns were somewhat erratic because chambers were either filled completely with seeds or were empty. 5. Because chamber area decreased sharply with depth, the densities (individuals cm^–2) of all colony members, including dark workers, were lowest near the surface and highest in the deepest parts of the nest. Here, worker densities ranged from 2 to 8 cm^–2, and brood from 2 to 25 cm^–2. 6. The regularity of the patterns of distribution suggests that harvester ant colonies have considerable spatial and temporal structure, which serves or is the outcome of important colony processes. A simple mechanism that could generate several of these patterns is discussed. New workers produced deep in the nest move upwards as they age. As they leave the brood zone they change from brood care to general nest duties, including increased nest excavation, leading to the top-heavy pattern of nest area. As they appear at the surface, they change to guarding and foraging. Thus, age polyethism may be partly the result of this upward migration of workers.     

Dung burial activity and development of ivermectin exposedDiastellopalpus quinquedens in a field experiment

The amount of cattle dung buried in the field by afrotropical dung beetles, mainlyDiastellopalpus quinquedens Bates, was not affected by previous subcutaneous injection of the cattle with 0.2 mg kg⁻¹ ivermectin. The numbers ofD. quinquedens larvae developing in brood masses, however, were reduced; only 28% of the brood masses made of dung voided two days after treatment of the cattle contained live larvae. When the brood masses were made of dung excreted 8 and 16 days after treatment 90 and 94%, respectively, contained live larvae.