Onset Of Foraging Research Articles

Proteome of Clothianidin Exposed Honey Bees Reveals a Possible Mechanism Behind Impairment of Sucrose Responsiveness

ABSTRACTNeonicotinoids (NNIs) are the most commonly used insecticides in the world and clothianidin, a type of NNI, is commonly found in honey bee collected pollen. Clothianidin has several negative effects on honey bee health and behaviour, but whether and how it might impact learning and memory remains unclear. Therefore, we exposed honey bee workers to a field‐realistic oral dose of clothianidin for 7 days to assess their sugar responsiveness, and olfactory learning and memory using the proboscis extension response paradigm. Sugar responsiveness impacts important colony‐level traits, such as onset of foraging, that help maintain colony homeostasis as well as impacts learning and memory. We then measured how clothianidin alters protein expression in the brain in an effort to understand the mechanism(s) of clothianidin's effects. Clothianidin‐exposed bees had impaired sugar responsiveness, but no effect was seen on learning and memory. We identified 5069 protein groups and showed that the exposed bees had fewer detectable proteins. The exposed bees also had fewer mitochondrial respiration proteins, as well as reduced levels of nicotinic acetylcholine receptor α7 (nAChRα7) subunit (one of the targets of clothianidin) and reduced levels of acetylcholinesterase and acetylcholinesterase‐2 levels. In the exposed bees, the levels of nAChRα7 subunit positively correlated with sugar responsiveness, providing evidence for a possible mechanical explanation.

Honeybee lifespan: the critical role of pre-foraging stage.

Assessing the various anthropogenic pressures imposed on honeybees requires characterizing the patterns and drivers of natural mortality. Using automated lifelong individual monitoring devices, we monitored worker bees in different geographical, seasonal and colony contexts creating a broad range of hive conditions. We measured their life-history traits and notably assessed whether lifespan is influenced by pre-foraging flight experience. Our results show that the age at the first flight and onset of foraging are critical factors that determine, to a large extent, lifespan. Most importantly, our results indicate that a large proportion (40%) of the bees die during pre-foraging stage, and for those surviving, the elapsed time and flight experience between the first flight and the onset of foraging is of paramount importance to maximize the number of days spent foraging. Once in the foraging stage, individuals experience a constant mortality risk of 9% and 36% per hour of foraging and per foraging day, respectively. In conclusion, the pre-foraging stage during which bees perform orientation flights is a critical driver of bee lifespan. We believe these data on the natural mortality risks in honeybee workers will help assess the impact of anthropogenic pressures on bees.

Young bumblebees may rely on both direct pollen cues and early experience when foraging.

An adequate supply of macro- and micronutrients determines health and reproductive success in most animals. Many bee species, for example, collect nectar and pollen to satisfy their demands for carbohydrates, protein and fat, respectively. Bees can assess the quality of pollen by feeding on it, but also pre-digestively by means of chemotactile assessment. Whether they additionally use larval nutritional experience, as has been shown for Drosophila melanogaster and Bombyx mori, is unknown. In this study, we tested whether pollen selection of bumblebee foragers is affected by nutritional experience (acquired before the onset of foraging) or solely by food quality. Bumblebee larvae were fed with one out of three different pollen blends. As adults, they were offered all three blends when they started foraging for the first time. We found all treatment groups to prefer one out of the three blends. This blend provided the highest nutritional quality and increased the bees' lifespan, as shown by feeding studies with microcolonies. Besides, bees also chose the pollen blend fed during their larval stage more often than expected, indicating a significant effect of pre-foraging experience on adult pollen foraging behaviour. The combination of both direct pollen quality assessment and pre-foraging experience (i.e. during the larval phase or as early imagines) seems to allow foraging bumblebees to efficiently select the most suitable pollen for their colony.

Measuring ontogenetic shifts in central-place foragers: A case study with honeybees.

Measuring time-activity budgets over the complete individual life span is now possible for many animals with the recent advances of life-long individual monitoring devices. Although analyses of changes in the patterns of time-activity budgets have revealed ontogenetic shifts in birds or mammals, no such technique has been applied to date on insects. We tested an automated breakpoint-based procedure to detect, assess and quantify shifts in the temporal pattern of the flight activities in honeybees. We assumed that the learning and foraging stages of honeybees will differ in several respects, to detect the age at onset of foraging (AOF). Using an extensive dataset covering the life-long monitoring of 1,167 individuals, we compared the AOF outputs with the more conventional approaches based on arbitrary thresholds. We further evaluated the robustness of the different methods comparing the foraging time-activity budget allocations between the presumed foragers and confirmed foragers. We revealed a clear-cut learning-foraging ontogenetic shift that differs in duration, frequency and time of occurrence of flights. Although AOF appeared to be highly plastic among bees, the breakpoint-based procedure seems better capable to detect it than arbitrary threshold-based methods that are unable to deal with inter-individual variation. We developed the aof r-package including a broad range of examples with both simulated and empirical datasets to illustrate the simplicity of use of the procedure. This simple procedure is generic enough to be derived from any individual life-long monitoring devices recording the time-activity budgets, and could propose new ecological applications of bio-logging to detect ontogenetic shifts in the behaviour of central-place foragers.

The effect of nest topology on spatial organization and recruitment in the red ant Myrmica rubra.

Nests of social insects are an important area for the exchange of food and information among workers. We investigated how the topology of nest chambers (as opposed to nest size or environmental factors) affects the spatial distribution of nestmates and the foraging behavior of Myrmica rubra ant colonies. Colonies were housed in artificial nests, each with same-sized chambers differing in the spatial arrangement of galleries. A highly connected central chamber favored higher occupancy rates and a more homogeneous distribution of ants across chambers. In contrast, a chain of successive chambers led to a more heterogeneous distribution of ants, with the occupancy of a chamber chiefly mediated by its distance to the entrance. Irrespective of nest topology, the entrance chamber housed the largest proportion of ants, often including the queen, which exhibited a preference for staying in densely populated chambers. Finally, we investigated how nest topology influenced nestmate recruitment. Surprisingly, a highly connected chamber in the center of the nest did not promote greater recruitment nor activation of ants. At the onset of foraging, the largest number of moving ants was reached in the topology where the most connected chamber was the nest entrance. Later in the process, we found that a chain of successive chambers was the best topology for promoting ant's mobilization. Our work demonstrates that nest topology can shape the spatial organization and the collective response of ant colonies, thereby taking part in their adaptative strategies to exploit environmental resources.

Developmental stability, age at onset of foraging and longevity of Africanized honey bees (Apis mellifera L.) under heat stress (Hymenoptera: Apidae)

Beekeeping with the western honey bee (Apis mellifera) is important in tropical regions but scant information is available on the possible consequences of global warming for tropical beekeeping. We evaluated the effect of heat stress on developmental stability, the age at onset of foraging (AOF) and longevity in Africanized honey bees (AHBs) in the Yucatan Peninsula of Mexico, one of the main honey producing areas in the Neotropics, where high temperatures occur in spring and summer. To do so, we reared worker AHB pupae under a fluctuating temperature regime, simulating current tropical heatwaves, with a high temperature peak of 40.0 °C for 1 h daily across six days, and compared them to control pupae reared at stable temperatures of 34.0–35.5 °C. Heat stress did not markedly affect overall body size, though the forewing of heat-stressed bees was slightly shorter than controls. However, bees reared under heat stress showed significantly greater fluctuating asymmetry (FA) in forewing shape. Heat stress also decreased AOF and reduced longevity. Our results show that changes occur in the phenotype and behavior of honey bees under heat stress, with potential consequences for colony fitness.

Transcriptomic analysis of instinctive and learned reward-related behaviors in honey bees.

We used transcriptomics to compare instinctive and learned, reward-based honey bee behaviors with similar spatio-temporal components: mating flights by males (drones) and time-trained foraging flights by females (workers), respectively. Genome-wide gene expression profiling via RNA sequencing was performed on the mushroom bodies, a region of the brain known for multi-modal sensory integration and responsive to various types of reward. Differentially expressed genes (DEGs) associated with the onset of mating (623 genes) were enriched for the gene ontology (GO) categories of Transcription, Unfolded Protein Binding, Post-embryonic Development, and Neuron Differentiation. DEGs associated with the onset of foraging (473) were enriched for Lipid Transport, Regulation of Programmed Cell Death, and Actin Cytoskeleton Organization. These results demonstrate that there are fundamental molecular differences between similar instinctive and learned behaviors. In addition, there were 166 genes with strong similarities in expression across the two behaviors - a statistically significant overlap in gene expression, also seen in Weighted Gene Co-Expression Network Analysis. This finding indicates that similar instinctive and learned behaviors also share common molecular architecture. This common set of DEGs was enriched for Regulation of RNA Metabolic Process, Transcription Factor Activity, and Response to Ecdysone. These findings provide a starting point for better understanding the relationship between instincts and learned behaviors. In addition, because bees collect food for their colony rather than for themselves, these results also support the idea that altruistic behavior relies, in part, on elements of brain reward systems associated with selfish behavior.

Cheating workers with large activated ovaries avoid risky foraging

Eusocial insects undoubtedly evolved from solitary ancestors, but how this occurred is not well established. The Ground Plan hypothesis suggests that gene networks that once regulated the oviposition and foraging phases of an ancestral solitary insect’s life cycle have been co-opted to establish the queen–worker dimorphism in extant eusocial insects; queens permanently express genes that were once expressed during the oviposition phase, whereas workers express genes that were once associated with foraging. An extension of the Ground Plan hypothesis, the Reproductive Ground Plan-forager hypothesis, proposes that foraging specialization by worker honey bees for either pollen or nectar is controlled by the same reproductive gene networks. According to the Reproductive Ground Plan-forager hypothesis, workers with more ovarioles forage early in life and specialize in pollen collection. Here we find that among workers of a highly reproductive honey bee subspecies, Apis mellifera capensis, there is a positive correlation between ovariole number and age at onset of foraging, and no association between ovariole number and foraging preference, thus contradicting key aspects of the Reproductive Ground Plan-forager hypothesis. We also find a negative association between ovariole number and ovary activation, suggesting that high ovariole number is not directly related to reproductive potential as previously assumed.

TEMPERATURE DOES NOT RESTRICT BULL ANT ACTIVITIES

Myrmecia aren't known as bull ants for nothing. `They are very ferocious, they have good eyes and a very painful sting,' explains Jochen Zeil from the Australian National University. However, despite their aggressive nature, two of these closely related species have achieved an arrangement that allows them to live in close proximity: Myrmecia croslandi forage by day while Myrmecia pyriformis only forage after sunset. Zeil explains that this partitioning of time could be explained by a number of factors such as competition and avoiding predators. However, Zeil points out that another factor could be responsible for the ants' lifestyles. `It could be that the night-active animals avoid the heat of the day and the day-active animals avoid the cool of the night,' he says. Intrigued by this possibility, Zeil and his colleagues Piyankarie Jayatilaka, Ajay Narendra and Paul Cooper decided to monitor the ants' activity patterns over a year and to measure their thermal tolerances to find out whether the insects' thermal tolerances influenced their lifestyle choices (p. 2730).Finding M. croslandi and M. pyriformis nests on the university campus, Jayatilaka, Narendra and Samuel Reid monitored the ants as they set off foraging in the surrounding trees. Over a year, the team saw that the day-active M. croslandi were active at temperatures ranging from 10 to 35°C and their foraging pattern varied across the year. On hot summer days, the insects emerged from the nest at about 8 am and returned to the nest for a midday siesta before heading out a second time and finally turning in at 5 pm. However, in the cooler spring and autumn the ants stayed out foraging all day and as the temperatures dropped further in winter the ants closed the nest and hibernated. M. croslandi were extremely temperature sensitive and Zeil says, `There was a clear correlation with temperature at sunrise and the onset of foraging.'However, the nocturnal M. pyriformis's behaviour was much less variable and they seemed completely unaffected by temperature as the year progressed. `They always came out about 20 minutes after sunset and they were active throughout the winter,' says Zeil, who adds, `Their foraging is determined by the light level at sunset time.'Next, the team decided to find out whether the insects' foraging patterns were influenced by their thermal tolerance, so they measured the temperature at which the insects lose the ability to move. Filming M. croslandi as the temperature rose gradually, Jayatilaka, Cooper and Zeil were surprised to see that the ants suddenly began rushing around at about 35°C before collapsing later at 48.5°C. The ants seemed to be trying to escape the heat and Zeil says, `The increase in walking speed when they encounter an uncomfortable temperature is a much better predictor of the temperatures they stop being active outdoors.' After allowing the ants to recover from the high temperature, the team reversed the experiment and found that the ants were incapacitated at 10.4°C.The team also repeated the same experiments with the nocturnal M. pyriformis, and the ants functioned well from 41.6°C down to 8.2°C.`It is very clear to us that the physiology of these animals does not limit them to their activity schedules,' says Zeil: M. pyriformis could handle the heat of the day and M. croslandi could cope with cooler nights. The team suspects that the ants are restricted by their visual system instead, with the bright light of day sending M. pyriformis back to the nest and dim night conditions keeping M. croslandi out of M. pyriformis's way.

Chemical communication in the honeybee (Apis mellifera L.): a review

An important area of physiology of the honeybee (Apis mellifera) is chemical communication between individuals and castes in the swarm, which maintains its integrity and function. The highly complex social organization of honeybees is mediated through pheromones. Releaser pheromones cause rapid changes in the behaviour of the recipient, while primer pheromones have relatively slow and long-term effects on the physiology and behaviour of the recipient. Queen retinue pheromone (QRP) is a blend of the nine compounds (9-oxo-(E)-2-decenoic acid, (R)- and (S)-9-hydroxy-(E)-2-decenoic acid, methyl p-hydroxybenzoate, 4-hydroxy-3-methyoxyphenylethanol, methyl oleate, coniferyl alcohol, palmityl alcohol, and linolenic acid) and acts as a releaser pheromone by attracting worker bees to the queen. QRP also acts as a primer pheromone by physiologically inhibiting the ovary development of worker bees. An essential component of QRP, 9-oxo-(E)-2-decenoic acid, acts as a long-distance sex pheromone. Defensive behaviour of honeybees is induced and modulated by alarm pheromones. The essential alarm pheromone component is isopentyl acetate (IPA). The unsaturated derivative of IPA, 3-methyl-2-buten-1-yl acetate, was found in colonies of Africanized honeybees. The Nasanov gland of worker bees produces a pheromone (a blend of nerol, geraniol, (E)- and (Z)-citral, nerolic acid, geranic acid and (E,E)-farnesol) that acts as an attracting signal. This pheromone is used for aggregation (during swarming). Adult worker bees also produce a substance, ethyl oleate, that has a priming effect. Ethyl oleate is produced by adult forager bees and acts as a chemical inhibitory factor to delay age at onset of foraging (the presence of older worker bees causes a delayed onset of foraging in younger individuals). Chemical cues on the surface of larvae called a brood pheromone (ethyl and methyl esters of palmitic, linoleic, linolenic, stearic, and oleic acids, E-β-ocimene) are important in the communication between brood and worker bees. This pheromone modulates the feeding behaviour of worker bees, inhibits the activation of the worker ovary, induces worker bees to cap brood cells, increases the activity of the hypopharyngeal glands of nurse bees and modulates the behavioural maturation of worker bees.

Life expectancy and onset of foraging in the honeybee (Apis mellifera)

Predictions that precocious foraging in honeybee workers is a result of shortening of their life expectancy were tested in both laboratory and field experiments. In the laboratory experiment, we assessed the impact of anaesthesia with CO2 and infection with Nosema apis on the lifespan of workers. In the field experiment, the age at onset of foraging was observed in groups of workers with different expected lifespans. In both the experiments, workers originating from one queen inseminated with the semen of one drone were divided into five groups. The first group was anaesthetized with CO2 on the first day of life. Workers from the other three groups were individually inoculated with a constant number of N. apis spores on the 1st, 6th and 11th days of life. Workers from the fifth control group were neither treated with CO2 nor inoculated in any way. Both the laboratory and field experiments revealed that anaesthetized and infected workers had shorter expected lifespans compared to control bees. Amongst infected workers, those inoculated earlier in life survived for a significantly shorter period of time in comparison to those infected later in life. In agreement with the expectation, the field experiment showed that anaesthetized and infected workers with shorter expected lifespan start foraging earlier than control workers. Amongst the infected workers, age at inoculation correlated with age at onset of foraging. This means that short-lived workers complete safe nest tasks and begin riskier foraging earlier in life. Our results provide a strong support for the hypothesis that the division of labour in eusocial insects is a consequence of the different expected worker lifespan and different risk associated with their tasks; however, they do not contradict other existing explanations.

Signaling Who Does Which Chores

Honey bees divvy up the labor of obtaining food and feeding the young by age: Young adult "nurse" bees feed the larvae, whereas older bees forage. The transition from nurse to forager, which can be accelerated or slowed in response to the needs of the hive, is accompanied by a decrease in nutrient stores. Noting that abundant nutrient stores typically promote synthesis of insulin [or insulin-like peptides (ILPs) in insects] and that insulin/insulin-like growth factor signaling (IIS) has been implicated in the central regulation of feeding-related behavior in Drosophila , Ament et al . investigated the role of IIS in honey-bee behavioral maturation. The abundance of mRNAs encoding the ILP AmIlp1 in brain and the ILP receptors AmInR1 and AmInR2 in abdomen was greater in foragers than in nurses (despite their decreased adiposity). This increase depended on nutritional status; immature bees fed on sugar (which led to forager-like lipid stores) expressed more brain ilp1 and brain and abdominal inR1 than their counterparts fed a more nutrient-rich diet of sugar and pollen. IIS stimulates TOR (target of rapamycin), and administration of the TOR inhibitor rapamycin elicited a seasonally dependent delay in the onset of foraging. Although insulin signaling is typically associated with increased energy metabolism, the expression of genes encoding proteins involved in energy metabolism--notably, five of six in the citrate cycle--was enhanced in the brains of nurse bees compared with foragers, although foragers have higher overall metabolic rates. The authors conclude that, in the honey bee, IIS--which is involved in regulation of metabolism and of feeding behavior in a solitary insect--is associated with regulation of social behavior. S. A. Ament, M. Corona, H. S. Pollock, G. E. Robinson, Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. U.S.A. 105 , 4226-4231 (2008). [Abstract] [Full Text]

Endocrine modulation of a pheromone-responsive gene in the honey bee brain

Pheromones cause dramatic changes in behavior and physiology, and are critical for honey bee colony organization. Queen mandibular pheromone (QMP) regulates multiple behaviors in worker bees (Slessor et al. in J Chem Ecol 31(11):2731-2745, 2005). We also identified genes whose brain expression levels were altered by exposure to QMP (Grozinger et al. in Proc Natl Acad Sci USA 100(Suppl 2):14519-14525, 2003). Krüppel-homolog 1 (Kr-h1) RNA levels were significantly downregulated by QMP, and were higher in foragers than in nurses (Whitfield et al. in Science 302(5643):296-299, 2003). Here we report on results of behavioral and pharmacological experiments that characterize factors regulating expression of Kr-h1. Foragers have higher brain levels of Kr-h1 than in-hive bees, regardless of age and pheromone exposure. Furthermore, forager Kr-h1 levels were not affected by QMP. Since the onset of foraging is caused, in part, by increasing juvenile hormone blood titers and brain octopamine levels, we investigated the effects of octopamine and methoprene (a juvenile hormone analog) on Kr-h1 expression. Methoprene produced a marginal (not significant) increase in Kr-h1 expression, but Kr-h1 brain levels in methoprene-treated bees were no longer downregulated by QMP. Octopamine did not modulate Kr-h1 expression. Our results demonstrate that the gene expression response to QMP is not hard-wired in the brain but is instead dependent on worker behavioral state.

Nutritional status influences socially regulated foraging ontogeny in honey bees

In many social insects, including honey bees, worker energy reserve levels are correlated with task performance in the colony. Honey bee nest workers have abundant stored lipid and protein while foragers are depleted of these reserves; this depletion precedes the shift from nest work to foraging. The first objective of this study was to test the hypothesis that lipid depletion has a causal effect on the age at onset of foraging in honey bees (Apis mellifera L.). We found that bees treated with a fatty acid synthesis inhibitor (TOFA) were more likely to forage precociously. The second objective of this study was to determine whether there is a relationship between social interactions, nutritional state and behavioral maturation. Since older bees are known to inhibit the development of young bees into foragers, we asked whether this effect is mediated nutritionally via the passage of food from old to young bees. We found that bees reared in social isolation have low lipid stores, but social inhibition occurs in colonies in the field, whether young bees are starved or fed. These results indicate that although social interactions affect the nutritional status of young bees, social and nutritional factors act independently to influence age at onset of foraging. Our findings suggest that mechanisms linking internal nutritional physiology to foraging in solitary insects have been co-opted to regulate altruistic foraging in a social context.

Development of the Blood and Muscle Oxygen Stores in Gray Seals (Halichoerus grypus): Implications for Juvenile Diving Capacity and the Necessity of a Terrestrial Postweaning Fast

To successfully transition from nursing to foraging, phocid seal pups must develop adequate diving physiology within the limited time between birth and their first independent foraging trip to sea. We studied the postpartum development of oxygen stores in gray seals (Halichoerus grypus, n=40) to better understand the ontogeny of diving capacity in phocids. Hemoglobin (Hb), hematocrit (Hct), blood volume (BV), and myoglobin (Mb) levels in newborn (3 d postpartum [DPP]) and newly weaned (17+/-0.4 DPP) pups were among the lowest measured across age classes. During the pups' terrestrial postweaning fast (PWF), Hb, Hct, mass-specific BV, and Mb increased by 28%, 21%, 13%, and 29%, respectively, resulting in a 35% increase in total body mass-specific oxygen stores and a 23% increase in calculated aerobic dive limit (CADL). Although Hb and Hct levels at the end of the PWF were nearly identical to those of yearlings, total body mass-specific oxygen stores and CADL of weaned pups departing for sea were only 66%-67% and 32%-62%, respectively, of those for yearlings and adult females. The PWF represents an integral component of the physiological development of diving capacity in phocids; however, newly independent phocids still appear to have limited diving capabilities at the onset of foraging.

Behavior and the limits of genomic plasticity: power and replicability in microarray analysis of honeybee brains

Transcription is slow relative to many post-transcriptional processes in the brain. Using the rich system of division of labor in the honeybee (Apis mellifera), we found extreme differences in the extent to which behavioral occupations of different durations were associated with gene-expression differences in the brain. Nursing and foraging, occupations lasting > 1 week, were associated with significant expression differences for nearly one-quarter of the genes tested (1208 of 5563 cDNAs tested; P < 0.01, anova), consistent with previous results. In contrast, transitional occupations, performed for 1-2 days after nursing and before the onset of foraging, were associated with either no differences (guards vs. undertakers; 19 cDNAs, fewer than the expectation of 56 false-positives) or few differences (comb builders vs. guards and undertakers; 248 cDNAs), but extensive differences relative to both nursing and foraging (> 500 cDNAs, all contrasts). Statistical power analysis indicated that expression differences of two-, 1.5- and 1.25-fold should have been detected in 100, 92 and 37% of cases, respectively. Replication of previous results at these magnitudes was 95, 71 and 51%, with no genes showing differences in the opposite direction. These results indicate that behavioral plasticity over different time-scales may be associated with substantial differences in the extent of genomic plasticity in the brain.

Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees

Previous research showed that the presence of older workers causes a delayed onset of foraging in younger individuals in honey bee colonies, but a specific worker inhibitory factor had not yet been identified. Here, we report on the identification of a substance produced by adult forager honey bees, ethyl oleate, that acts as a chemical inhibitory factor to delay age at onset of foraging. Ethyl oleate is synthesized de novo and is present in highest concentrations in the bee's crop. These results suggest that worker behavioral maturation is modulated via trophallaxis, a form of food exchange that also serves as a prominent communication channel in insect societies. Our findings provide critical validation for a model of self-organization explaining how bees are able to respond to fragmentary information with actions that are appropriate to the state of the whole colony.

Worker-worker inhibition of honey bee behavioural development independent of queen and brood

Foragers inhibit the behavioural development of young adult worker honey bees, delaying the age at onset of foraging. But the similar effect caused by pheromones produced by both the queen and brood raised the possibility that some of the previously attributed forager effects might be due to queen, brood, or both. Here we studied whether physical contacts between young bees and old foragers can inhibit behavioural development while controlling for queen and brood effects. Results demonstrated that foragers inhibit the behavioural development of young adult worker bees independent of the queen and brood, via a mechanism that requires physical contact.

Worker honey bee pheromone regulation of foraging ontogeny.

The evolution of sociality has configured communication chemicals, called primer pheromones, which play key roles in regulating the organization of social life. Primer pheromones exert relatively slow effects that fundamentally alter developmental, physiological, and neural systems. Here, I demonstrate how substances extracted from the surface of foraging and young pre-foraging worker bees regulated age at onset of foraging, a developmental process. Hexane-extractable compounds washed from foraging workers increased foraging age compared with controls, whereas extracts of young pre-foraging workers decreased foraging age. This represents the first known direct demonstration of primer pheromone activity derived from adult worker bees.

The hive bee to forager transition in honeybee colonies: the double repressor hypothesis

In summer, the honeybee ( Apis mellifera) worker population consists of two temporal castes, a hive bee group performing a multitude of tasks including nursing inside the nest, and a forager group specialized on collecting nectar, pollen, water and propolis. Elucidation of the regulatory mechanisms responsible for the hive bee to forager transition holds a prominent position within present day sociobiology. Here we suggest a new explanation dubbed the “double repressor hypothesis” aimed to account for the substantial amount of empirical data in this field. This is the first time where both the regular transition and starvation-induced precocious transition are explained within the same regulatory framework. We suggest that the transition is under regulatory control by an internal and an external repressor of the allatoregulatory central nervous system, where these two repressors modulate a positive regulatory feedback loop involving juvenile hormone (JH) and the lipoprotein vitellogenin. The concepts of age-neutrality, fixed and variable response thresholds and reinforcement are integral parts of our explanation, and in addition they are given explicit physiological content. The hypothesis is represented by a differential equations model at the level of the individual bee, and by a discrete individual-based colony model. The two models generate predictions in accordance with empirical data concerning the cumulative probability of becoming a forager, mean age at onset of foraging, reversal of foragers, time window of reversal, relationship between JH titre and onset of foraging, relative representations of genotypic groups, and effects of forager depletion and confinement.