Temporal dynamics of facultative social parasitism in bumble bees (Hymenoptera: Apidae)

Parasitical behaviour is thought to play an important, yet so far largely unknown role in the evolution and maintenance of insect sociality. In this study, the influence of interspecific, facultative social parasitism upon bumble bee, Bombus, nesting biology was explored. Queens of B. affinis were introduced into 38 various-sized laboratory colonies of B. terricola. Foreign queens were very successful at killing the resident queen and usurping pre-worker nests (77% wins), although usurpation success decreased to 30% in colonies that contained workers. In addition, B. affinis queens were unable to suppress ovarian development in B. terricola workers that emerged prior to nest usurpation, resulting in the eventual death or expulsion of the foreign queen. In contrast, ovarian development was supporessed in workers that eclosed in the presence of a foreign queen, and in workers that were less than 5 h old when confined in small experimental boxes with a B. affinis queen. Foreign queens that usurped a nest prior to worker emergence were assisted by B. terricola workers, and achieved similar reproductive success when compared to a cohort of 22 B. affinis queens that initiated their own nests in the laboratory. These results suggest that there are periods in the ontogeny of Bombus nest defence, recognition and dominance during which bees are sensitive to the effects of nest parasitism. In bumble bees, and in other social insects, individuals of some species may exploit these weaknesses for their own reproductive benefit.     

Suppression of queen rearing in European and Africanized honey beesApis mellifera L. by synthetic queen mandibular gland pheromone

Summary Queen rearing is suppressed in honey bees (Apis mellifera L.) by pheromones, particularly the queen's mandibular gland pheromone. In this study we compared this pheromonally-based inhibition between temperate and tropically-evolved honey bees. Colonies of European and Africanized bees were exposed to synthetic queen mandibular gland pheromone (QMP) for ten days following removal of resident queens, and their queen rearing responses were examined. Queen rearing was suppressed similarly in both European and Africanized honey bees with the addition of synthetic QMP, indicating that QMP acts on workers of both races in a comparable fashion. QMP completely suppressed queen cell production for two days, but by day six, cells containing queen larvae were present in all treated colonies, indicating that other signals play a role in the suppression of queen rearing. In queenless control colonies not treated with QMP, Africanized bees reared 30% fewer queens than Europeans, possibly due to racial differences in response to feedback from developing queens and/or their cells. Queen development rate was faster in Africanized colonies, or they selected older larvae to initiate cells, as only 1 % of queen cells were unsealed after 10 days compared with 12% unsealed cells in European colonies.     

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.     

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

Summary. 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.Received 24 November 2003; revised 27 March 2004; accepted 21 April 2004.     

Social parasitism of <Emphasis Type="Italic">Polistes dominulus</Emphasis> by <Emphasis Type="Italic">Polistes nimphus</Emphasis> (Hymenoptera,Vespidae)

Summary Interspecific facultative social parasitism is well known in ants and in bumble-bees, but it is rarer in wasps. This form of parasitism is traditionally considered to be an intermediate stage in the evolution of obligate interspecific parasitism, where the parasites are no longer able to nest alone. We report field and experimental observations of a newly discovered facultative parasitic relationship between two closely related free-living Polistes species: P. nimphus and P. dominulus. P. nimphus foundresses sometimes usurp the nests of the larger P. dominulus before worker emergence. The invading queen takes over the nest with abundant abdomen stroking on the nest surface and is accepted by workers if they emerge 6 or more days after usurpation. Morphometric comparisons show that the usurper species, though smaller than its victims, has morphological adaptations consisting of larger heads, mandibles and front femora relative to their body size that may give it an advantage during nest invasion. This strategy is likely to be taken only after the foundress loses her original nest because invading P. nimphus queens have lower reproductive success than they would have had on their own nest. Overall, we found that P. nimphus usurpers use strategies of invasion similar to those of two obligate parasites, suggesting that this may be an example of one of the pathways by which social parasitism evolved.Received 4 April 2003; revised 8 August 2003; accepted 14 September 2003.     

Intergenerational reproductive parasitism in a stingless bee

Insect colonies have been traditionally regarded as closed societies comprised of completely sterile workers ruled over by a single once-mated queen. However, over the past 15 years, microsatellite studies of parentage have revealed that this perception is far from the truth ( Beekman & Oldroyd 2008 ). First, we learned that honey bee queens are far more promiscuous than we had previously imagined ( Estoup et al. 1994 ), with one Apis dorsata queen clocked at over 100 mates ( Wattanachaiyingcharoen et al. 2003 ). Then Oldroyd et al. (1994) reported a honey bee colony from Queensland, where virtually all the males were sons of a single patriline of workers – a clear case of a cheater mutant that promoted intra-colonial reproductive parasitism. Then we learned that both bumble bee colonies ( Lopez-Vaamonde et al. 2004 ) and queenless honey bee colonies ( Nanork et al. 2005, 2007 ) are routinely parasitized by workers from other nests that fly in and lay male-producing eggs that are then reared by the victim colony. There is even evidence that in a thelytokous honey bee population, workers lay female-destined eggs directly into queen cells, thus reincarnating themselves as a queen ( Jordan et al. 2008 ). And let us not forget ants, where microsatellite studies have revealed equally bizarre and totally unexpected phenomena (e.g. Cahan & Keller 2003 ; Pearcy et al. 2004 ; Fournier et al. 2005 ). Now, in this issue, Alves et al. (2009) use microsatellites to provide yet another shocking and completely unexpected revelation about the nefarious goings-on in insect colonies: intergenerational reproductive parasitism by stingless bee workers.     

Anarchistic queen honey bees have normal queen mandibular pheromones

Summary. Anarchistic honey bees are a line developed by recurrent selection in which workers frequently lay eggs. In unselected colonies, workers refrain from reproduction in response to pheromonal signals that indicate the presence of brood and a queen. We show that queen type (anarchistic or wild type) has no effect on rates of ovary activation of anarchistic or wild type workers. In addition, we show that an important component of the queens signalling system, the queen mandibular gland pheromone, is similar in wild type and anarchistic queens. Anarchistic larvae do not inhibit worker ovary development to the same degree as wild type larvae, however all colonies in this experiment contained only wild type larvae. Anarchistic workers had greater rates of ovary activation than wild type workers in colonies headed by either queen type. We therefore conclude that there must be differences in the transmission or reception of queen pheromones, or worker sensitivity to these compounds. These results clearly demonstrate that anarchy is a complex syndrome, not simply the result of reduced pheromone production by anarchist queens and larvae.Received 23 December 2003; revised 14 May 2004; accepted 1 June 2004.     

Quantitative trait loci for honey bee stinging behavior and body size.

A study was conducted to identify quantitative trait loci (QTLs) that affect colony-level stinging behavior and individual body size of honey bees. An F1 queen was produced from a cross between a queen of European origin and a drone descended from an African subspecies. Haploid drones from the hybrid queen were individually backcrossed to sister European queens to produce 172 colonies with backcross workers that were evaluated for tendency to sting. Random amplified polymorphic DNA markers were scored from the haploid drone fathers of these colonies. Wings of workers and drones were used as a measure of body size because Africanized bees in the Americas are smaller than European bees. Standard interval mapping and multiple QTL models were used to analyze data. One possible QTL was identified with a significant effect on tendency to sting (LOD 3.57). Four other suggestive QTLs were also observed (about LOD 1.5). Possible QTLs also were identified that affect body size and were unlinked to defensive-behavior QTLs. Two of these were significant (LOD 3.54 and 5.15).     

Old comb for nesting site recognition by <Emphasis Type="Italic">Apis dorsata?</Emphasis> Field experiments in China

The Asian giant honey bee, Apis dorsata, often conducts seasonal, long-distance migrations in southern China, between a preferred tree (having more than one nest) and alternate sites. Although worker bees cannot make a round-trip journey, colonies re-utilize preferred trees after an absence of several months. We performed comb experiments in which bases and all abandoned combs were entirely scraped off trees and their sites covered with plastic, or comb was moved to trees of the same species. Swarms of giant honey bees investigated trees where combs were removed and continued to nest on the same trees. In contrast, placing combs in nets on previously used trees, or on nearby trees of the same species, did not attract more swarms. The same number of colonies that left them returned to previously occupied trees. Our findings suggest that direct olfactory or sensory contact with old comb bases might regulate nest establishment, but individual trees, lacking normal visual or chemical cues of old nests, are relocated using behavioral devices that remain to be elucidated. Received 12 February 2007; revised 5 June 2007; accepted 13 September 2007.     

Nest Defense Behavior in Colonies from Crosses Between Africanized and European Honey Bees (Apis mellifera L.) (Hymenoptera: Apidae)

Honey bee (Apis mellifera L.) colonies with either European or Africanized queens mated to European or Africanized drones alone or in combination were tested for defensive behavior using a breath test. The most defensive colonies were those with European or Africanized queens mated to Africanized drones. In colonies where both European and Africanized patrilines existed, most of the workers participating in nest defense behavior for the first 30 s after a disturbance were of African patrilines. Nest defense behavior appears to be genetically dominant in honey bees.     

Origin and rearing season of honeybee queens affect some of their physiological and reproductive characteristics

Queen honeybees of Apis mellifera ligustica and Apis mellifera syriaca were raised to investigate physiological and reproductive characteristics and to determine the most suitable time for queen rearing under semi‐arid conditions in Jordan. The queen rearing season as well as the origin of the queens affected the queens’ weight, acceptance, preoviposition period, volume of the spermatheca, and quantity and quality of sperm in the spermatheca. Italian bees were heavier than Syrian bees at emergence. The introduced queen acceptance rate appeared to be a genetic influence of the queen: A. m. ligustica virgin queens were accepted at a higher rate than were A. m. syriaca queens. There were large seasonal variations in the acceptance rate. Experimental bee colonies accepted their virgin queens during spring with good honey flows at a higher rate compared to the other rearing periods. The greatest mating success was achieved in May and the smallest was during July and August. The preoviposition period was shorter in the Syrian than in the Italian queens, and was longer during summer for both honeybee subspecies. The volume of the spermatheca was smaller in Syrian bees and the spermatheca had lower numbers of spermatozoa compared with Italian bees. Thus, under semi‐arid Mediterranean region conditions, it is highly recommended to raise virgin queens in the spring months only to obtain their highest quality.     

Higher vitellogenin concentrations in honey bee workers may be an adaptation to life in temperate climates

The honey bee originated in tropical Africa and later dispersed to northern Europe. It has been suggested that a higher hemolymph storage capacity for the glycolipoprotein vitellogenin evolved in temperate regions, and that the trait constitutes an adaptation to a strongly seasonal environment. We have investigated whether the relative vitellogenin levels of European and African honey bees are in accordance with this hypothesis. Our data indicate that European workers have a higher set-point concentration for vitellogenin compared to their African origin. Considered together with available life history information and physiological data, the results lend support to the view that “winter bees”, a longlived honey bee worker caste that survives winter in temperate regions, evolved through an increase in the worker bees’ capacity for vitellogenin accumulation. Received 20 September 2004; revised 25 March 2005; accepted 13 April 2005.     

Behaviour in usurpers and late joiners ofPolistes biglumis bimaculatus (Hymenoptera,Vespidae)

Summary During the late pre-emergence phase, a foundress of the paper waspPolistes biglumis bimaculatus may be expelled by a conspecific female from her own nest (usurpation) or, less frequently, joined by another female of the same species (late association). The behaviour of femalePolistes biglumis bimaculatus, when usurping a conspecific colony or joining another foundress, is compared with that of foundresses on non-usurped colonies. The most conspicous difference is the intense abdomen stroking behaviour the usurper performs over the comb surface on the first days after usurpation. As observed in otherPolistes species, once usurpers and joiners arrive on a strange nest they will destroy most of the immature brood of the previous nest owner. Although host workers are not aggressive towards the intruder females, reproductive success of usurpers and joiners is low compared with that of legitimate foundresses. The same behaviours observed on usurped colonies are found in the obligate social parasites ofPolistes. These behaviours are therefore discussed in the context of the evolution of intra- and inter-specific parasitism.     

Attraction and Repellence of Workers by the Honeybee Queen (Apis mellifera L.)

The spatial distribution of worker honeybees in colonies of two African subspecies ( Apis mellifera capensis and Apis mellifera scutellata ), as well as their natural hybrids, was determined in five observation colonies, each containing one frame. The queens were allowed to roam freely throughout the hive during the initial phase of the experiment, and were observed on both sides of the frame in all colonies. In the second phase of the experiment the queen was caged on one side of the frame in three of the observation colonies, the other two colonies serving as controls. Queen caging significantly affected the distribution of worker bees, with more A. m. scutellata workers being attracted to the queen and more A. m. capensis worker bees being repelled by the presence of the queen. The hybrid workers were also repelled, but to a lesser extent. Queens thus not only attract workers to form a retinue or during swarming but also repel workers in the nest. Evasion of the reproductive suppression by the queen pheromones may be a typical behavior for workers with a high reproductive potential.     

Seasonal patterns of foraging activity in colonies of the African honey bee,Apis mellifera scutellata,in Africa

Summary Seasonal foraging patterns were investigated using six observation colonies maintained in the Okavango Delta, Botswana. Pollen collection, flight from the hive, and recruitment for pollen and nectar sources occurred throughout the 11 months of the study. However, the distribution of foraging activity throughout the day changed seasonally. Colonies emphasized recruitment for pollen sites throughout most of the year. Brood production occurred in all months except May, and there was a significant, positive correlation between the proportion of recruitment activity devoted to pollen sources and the amount of brood comb in the colonies. The seasonal foraging patterns ofscutellata in the Okavango were similar to those of Africanized honey bees in the neotropics. The extended foraging season and emphasis on pollen collection may be associated with the high swarming rates and migrational movements of tropical honey bees.     

Colony structure and sex allocation ratios in the ant <Emphasis Type="Italic">Temnothorax crassispinus</Emphasis>

Summary. We analyzed the impact of ecological parameters, such as nest density and nest site availability, on colony organization and investment patterns in two populations of the ant Temnothorax crassispinus, a parapatric sibling species of the well-studied T. nylanderi (Temnothorax was until recently referred to as Leptothorax (Myrafant); Bolton, 1993). As in T. nylanderi, sex allocation ratios were strongly associated with total sexual reproduction, i. e., nests with large sexual investment produced mainly female sexuals. Furthermore, nest site quality affected sex allocation ratios, with colonies from ephemeral nest sites producing a more male-biased sex allocation ratio than colonies from sturdy nest sites. In contrast to T. nylanderi, workers in colonies of T. crassispinus were mostly fullsisters both in a dense and a sparsely populated area, suggesting that colony fusion and colony usurpation are rare in this species. In addition, the presence of a queen in a local nest unit strongly influenced sex ratio decisions, in that these nests raised a more male biased allocation ratio compared to queenless nests. This also suggests that colony structure is more stable in T. crassispinus than in T. nylanderi. We conclude that sibling species, though often very similar in their morphology and ecological requirements, may nevertheless react very differently to ecological variation.Received 11 December 2003; revised 4 March 2004; accepted 19 April 2004.     

Biology of the stingless beePlebeia remota (Holmberg): observations and evolutionary implications

Summary The genusPlebeia has a special significance for the study of social evolution of stingless bees: morphologically primitive, its species display a wealth of behavioural evolution, especially with respect to the oviposition process. We comparePlebeia remota with the few other members of the genus studied so far.Related to its subtropical geographical range, brood production is seasonal (there is no brood in the colony in colder months), and adult workers occur as summer and winter bees. The nest is in tree cavities, and the involucrum is absent or restricted to the winter period. Brood cells are arranged in horizontal combs, and new cells are built completely synchronously. Each series consists of up to 50 cells, their number being mainly dependent on colony size. Construction speed is remarkably constant, allowing 4–6 batches per 24 hours. Cell building and provisioning are activities of a small group of specialized workers.The oviposition cycle follows the classical subdivisions for stingless bees. During the patrolling phase a worker may offer a trophic egg in a most remarkable way: while retreating backward from the queen she bends the abdomen under thorax and head, and lays an egg on the comb. This egg is eaten by the queen or a worker.The provisioning, oviposition and operculation of all cells occur simultaneously, each cell is provisioned by 4–9 workers. Localization of a cell by the queen may be facilitated by its characteristic guard, which defends the cell against the approaching queen. The degree of synchronization within a batch is very high: the duration per cell lasts 420–950 sec, the batch of up till 50 cells needs only 557–1160 sec. Operculation is done by a worker that was not involved in the previous steps.Males are generally produced by the queen. Several male producing cycles per year occur. In orphan colonies laying workers give rise to males, and in queenright colonies workers may occasionally reproduce as well.Division of labour follows the general pattern for stingless bees; however, cell building and provisioning are activities of a specialized group of workers.     

Population dynamics of a stingless bee community in the seasonal dry lowlands of Costa Rica

This study examines the dynamics of a population of stingless bee colonies in the seasonal tropics of Guanacaste, Costa Rica. The community in a forest remnant was compared with that in surrounding deforested areas. During this 4-year study, a total of 192 wild stingless bee colonies were recorded, belonging to 14 species. Population dynamics were highly seasonal. Colony mortality peaked at the end of the wet season (October–November) while colony reproduction was most frequent during the dry season (December to April). Colony survival was not lower in founder colonies compared to established colonies. The most common species, T. angustula, had a much lower probability of annual survivorship in the forest (P = 0.74) than in deforested areas (P = 0.92). This results in an estimated colony life span for T. angustula of 3.8 years in the forest and 12.5 years in deforested areas. T. angustula should swarm once every two years to maintain its forest population, but only once every 12.5 years to maintain its population in the deforested areas. Survivorship of all other stingless bees was similar in the forest and deforested areas and did not significantly differ among the species. The average annual survivorship probability of these species was as high as 0.96, resulting in an estimated colony life span of 23.3 years. On average only one swarm per 20 years is needed to maintain their populations. Life history of the sympatric Africanised honey bee clearly differed from that of the stingless bees, with much lower annual survivorship probabilities for both founder (none survived) and established colonies (P = 0.33). These figures support the general idea that stingless bees invest more in colony survival rather than reproduction, but also show that life history is affected by both species and location. Received 27 October 2004; revised 8 March and 15 June 2005; accepted 5 July 2005.     

Variation in worker response to honey bee (Apis mellifera L.) queen mandibular pheromone (Hymenoptera: Apidae)

Genetic and environmental influences on the worker honey bee retinue response to queen mandibular gland pheromone (QMP) were investigated. Worker progeny were reared from queens originating from four sources: Australia, New Zealand, and two locations in British Columbia, Canada (Simon Fraser University and Vancouver Island). Progeny from New Zealand queens responded significantly higher (P < 0.05) than progeny from Australia in a QMP retinue bioassay. Retinue response was not related to queen production of pheromone or colony environment, and the strain-dependent differences in retinue bioassay responses were maintained over a wide range of dosages. Selected high- and low-responding colonies were bioassayed over the course of 1 year. High-responding colonies contacted QMP lures more frequently than low-responding colonies (P < 0.05) throughout the year except in late summer. We conclude that there is a strong genetic component to QMP response by worker honey bees, as well as a seasonal effect on response.     

Factors influencing seasonal absconding in colonies of the African honey bee,Apis mellifera scutellata

Summary This study investigated the effects of colony growth and development, food storage, foraging activity and weather on the migration behavior of African honey bees in the Okavango River Delta, Botswana. Four observation colonies were studied during the honey bee migration season (November–May), at which time the availability of blooming species was reduced. Two of the colonies (colonies 1 & 2) migrated during the study period, while the remaining two (colonies 3 & 4) did not. During the 4–6 weeks preceding the onset of migration preparations, colonies 1 & 2 exhibited increasing population sizes, high levels of brood production with low brood mortality, relatively large stores of food, and increasing mass. In contrast, the populations of colonies 3 & 4 did not increase, brood-rearing activity was erratic and lower, brood mortality was higher, food stores became depleted and colony mass declined. Both colonies 3 & 4 ceased rearing brood, and colony 3 died of starvation. Colony foraging activity was examined by monitoring waggle-dance activity 2–3 days each week. For 4–6 weeks before the onset of migration in colonies 1 & 2, daily foraging areas and mean daily foraging distances became increasingly large and variable. Colonies 3 & 4 exhibited foraging patterns similar to those observed for colonies 1 & 2 preceding migration. There was no clear association between 7 weather parameters examined and migration behavior. These data suggest that migration is influenced by an interaction of intra-colony demographics, food reserves and foraging patterns. Migration may be feasible only for those colonies that possess (1) a population of appropriate size and age structure to compensate for the natural attrition of older workers during the emigration process, and (2) sufficient food reserves for long-distance travel and the establishment of a new nest. Changing foraging patterns may reflect a deteriorating foraging environment, which may trigger the onset of migration preparations, provided that colony demographics and food reserves are conducive. Colonies that show decreased brood production, higher brood mortality and reduced food stores may be incapable of migrating, even when experiencing deteriorating foraging conditions. Rather, such colonies may have a greater chance of survival if they attempt to persist in a given area.