Comb Wax Salvage by the Red Dwarf Honeybee, <Emphasis Type="Italic">Apis florea</Emphasis> F.

Cannibalizing wax from a deserted nest and reusing it in construction of a new nest is only known for absconding colonies of red dwarf honeybee, Apis florea. We tested whether A. florea would preferentially choose to salvage wax from their own, original natal comb over that of other conspecific combs (test 1) and whether they would salvage wax from comb facsimiles of A. florea combs (test 2) fashioned from the combs of A. cerana, A. dorsata, and A. mellifera. In test 1, preferences for natal comb were significantly greater than for non-natal combs. In test 2, no wax was collected from heterospecific combs. It is evident that wax discrimination is context-dependent and that there is considerable genetic variation for the wax-salvaging trait.     

Hearing in the Asian honeybeesApis dorsata andApis florea

Summary In the dance language of the western honeybee,Apis mellifera, airborne near field sound signals and a sense of hearing are used to communicate the locations of food sources. In the Asian honeybeeApis dorsata similar acoustical signals have been found recently, whereasApis florea does not emit dance sounds to transfer information about the location of food sources. The aim of the present study was to investigate the sense of hearing in these two species. Operant conditioning experiments reveal that both species are able to detect such near field sounds. The results support the hypothesis of acoustical communication inApis dorsata. The auditory sense ofApis florea, which does not use acoustical signals in the dance language, is discussed as a preadaptation for the evolution of an acoustical dance communication in ancestral honeybees.     

Stop-Signaling Reduces Split Decisions without Impairing Accuracy in the Honeybee Nest-Site Selection Process

In the honeybee swarm nest-site selection process, individual bees gather information about available candidate sites and communicate the information to other bees. The swarm makes an agreement for a candidate site when the number of bees that supports the site reaches a threshold. This threshold is usually referred to as the quorum threshold and it is shown by many studies as a key parameter that is a compromise between the accuracy and speed of decisions. In the present work, we use a model of the honeybee Apis mellifera nest-site selection process to study how the quorum threshold and discovery time of candidate sites have major impact on two unfavorable situations in selecting a nest site: decision deadlock and decision split. We show that cross-inhibitory stop-signaling, delivered among bees supporting different sites, enables swarms to avoid the decision split problem in addition to avoiding the decision deadlock problem that has been previously proposed. We also show that stop-signaling improves decision speed, but compromises decision accuracy in swarms using high quorum thresholds by causing the swarms to be trapped in local optima (e.g., choosing a sub-optimal option that is encountered first). On the other hand, we demonstrate that stop-signaling can reduce split decisions without compromising decision accuracy in swarms using low quorum thresholds when it is compared to the accuracy of swarms using the same threshold values but not exhibiting stop-signaling. Based on our simulations, we suggest that swarms using low quorum thresholds (as well as swarms with large population sizes) would benefit more from exhibiting the stop-signaling activity than not exhibiting it.     

Infections of Nosema ceranae in four different honeybee species

The microsporidium Nosema ceranae is detected in honeybees in Thailand for the first time. This endoparasite has recently been reported to infect most Apis mellifera honeybee colonies in Europe, the US, and parts of Asia, and is suspected to have displaced the endemic endoparasite species, Nosema apis, from the western A. mellifera. We collected and identified species of microsporidia from the European honeybee (A. mellifera), the cavity nesting Asian honeybee (Apis cerana), the dwarf Asian honeybee (Apis florea) and the giant Asian honeybee (Apis dorsata) from colonies in Northern Thailand. We used multiplex PCR technique with two pairs of primers to differentiate N. ceranae from N. apis. From 80 A. mellifera samples, 62 (77.5%) were positively identified for the presence of the N. ceranae. Amongst 46 feral colonies of Asian honeybees (A. cerana, A. florea and A. dorsata) examined for Nosema infections, only N. ceranae could be detected. No N. apis was found in our samples. N. ceranae is found to be the only microsporidium infesting honeybees in Thailand. Moreover, we found the frequencies of N. ceranae infection in native bees to be less than that of A. mellifera.     

Phylogenetic analysis of Nosema ceranae isolated from European and Asian honeybees in Northern Thailand

Nosema ceranae was found to infect four different host species including the European honeybee (A. mellifera) and the Asian honeybees (Apis florea, A. cerana and Apis dorsata) collected from apiaries and forests in Northern Thailand. Significant sequence variation in the polar tube protein (PTP1) gene of N. ceranae was observed with N. ceranae isolates from A. mellifera and A. cerana, they clustered into the same phylogenetic lineage. N. ceranae isolates from A. dorsata and A. florea were grouped into two other distinct clades. This study provides the first elucidation of a genetic relationship among N. ceranae strains isolated from different host species and demonstrates that the N. ceranae PTP gene was shown to be a suitable and reliable marker in revealing genetic relationships within species.     

Making good choices with variable information: a stochastic model for nest-site selection by honeybees

A density-dependent Markov process model is constructed for information transfer among scouts during nest-site selection by honeybees (Apis mellifera). The effects of site quality, competition between sites and delays in site discovery are investigated. The model predicts that bees choose the better of two sites more reliably when both sites are of low quality than when both sites are of high quality and that delay in finding a second site has most effect on the final choice when both sites are of high quality. The model suggests that stochastic effects in honeybee nest-site selection confer no advantage on the swarm.     

Are nest sites actively chosen? Testing a common assumption for three non-resource limited birds

Many widely-accepted ecological concepts are simplified assumptions about complex situations that remain largely untested. One example is the assumption that nest-building species choose nest sites actively when they are not resource limited. This assumption has seen little direct empirical testing: most studies on nest-site selection simply assume that sites are chosen actively (and seek explanations for such behaviour) without considering that sites may be selected randomly. We used 15 years of data from a nestbox scheme in the UK to test the assumption of active nest-site choice in three cavity-nesting bird species that differ in breeding and migratory strategy: blue tit (Cyanistes caeruleus), great tit (Parus major) and pied flycatcher (Ficedula hypoleuca). Nest-site selection was non-random (implying active nest-site choice) for blue and great tits, but not for pied flycatchers. We also considered the relative importance of year-specific and site-specific factors in determining occupation of nest sites. Site-specific factors were more important than year-specific factors for the tit species, while the reverse was true for pied flycatchers. Our results show that nest-site selection, in birds at least, is not always the result of active choice, such that choice should not be assumed automatically in studies of nesting behaviour. We use this example to highlight the need to test key ecological assumptions empirically, and the importance of doing so across taxa rather than for single “model” species.     

csd alleles in the red dwarf honey bee (Apis florea,Hymenoptera: Apidae) show exceptionally high nucleotide diversity

Abstract The single locus complementary sex determination (sl‐csd) gene is the primary gene determining the gender of honey bees (Apis spp.). While the csd gene has been well studied in the Western honey bee (Apis mellifera), and comparable data exist in both the Eastern honey bee (Apis cerana) and the giant honey bee (Apis dorsata), no studies have been conducted in the red dwarf honey bee, Apis florea. In this study we cloned the genomic region 3 of the A. florea csd gene from 60 workers, and identified 12 csd alleles. Analysis showed that similar to A. mellifera, region 3 of the csd gene contains a RS domain at the N terminal, a proline‐rich domain at the C terminal, and a hypervariable region in the middle. However, the A. florea csd gene possessed a much higher level of nucleotide diversity, compared to A. mellifera, A. cerana and Apis dorsata. We also show that similar to the other three Apis species, in A. florea, nonsynonymous mutations in the csd gene are selectively favored in young alleles.     

Ant repellent resins of honeybees and stingless bees

We measured the repellent effects of plant resins against the weaver ants, Oecophylla smaragdina. The resins were the sticky bands of the dwarf honeybees, Apis florea and A. andreniformis, propolis of the Western honeybee, A. mellifera and the nest entrance tubes of the stingless bees, Tetrigona apicalis, Lepidotrigona terminata, and Tetragonula collina. A bioassay was developed for testing the effects of these resins in field experiments by placing them along natural foraging pathways of ants’ nests. A repellency index was generated to quantify this bioactivity. The sticky bands of dwarf honeybees and propolis of A. mellifera were significantly more repellent against O. smaragdina than were the entrance tube resins of the stingless bees. Nonetheless, the diverse, viscid and adhesive resins employed by these bees constitute a generally effective first-line of defense against depredations of a formidable adversary, the weaver ants.     

Economics of comb wax salvage by the red dwarf honeybee, <Emphasis Type="Italic">Apis florea</Emphasis>

Colonies of Apis florea, which only abscond a short distance, usually return to salvage old nest wax; but, those colonies, and all other honeybee species which go considerably further, do not. Wax salvage would clearly be counter-productive unless the energy input/energy yield threshold was a profitable one. There are two possible trade-offs in this scenario, the trade-off between the energy expended to recover the wax (recovering hypothesis) as against that of replacing the wax by new secretion (replacing hypothesis). In order to compare the two hypotheses, the fuel costs involved in salvaging wax on one return trip, the average flower handling time, flight time and relative values for substituting the salvaged wax with nectar were calculated. Moreover, the energy value of the wax was determined. Net energy gains for salvaged wax were calculated. The energy value of the salvaged wax was 42.7 J/mg, thus too high to be the limiting factor since salvaging costs are only 642.76 mJ/mg (recovering hypothesis). The recovery costs (642.76 mJ/mg) only fall below the replacement costs for absconding distance below 115 m thus supporting the replacing hypothesis. This energetic trade-off between replacing and recycling plus the small absconding range of A. florea might explain why A. florea is probably the only honeybee species known to salvage wax and it parsimoniously explains the underlying reasons why A. florea only salvages wax from the old nest if the new nesting site is less than 100–200 m away—energetically, it pays off to recycle.     

Development ofEuvarroa sinhai (Acarina: Mesostigmata), a parasitic mite ofApis florea,onA. mellifera worker brood

The development ofEuvarroa sinhai Delfinado and Baker, a parasite ofApis florea F., onA. mellifera worker brood was demonstrated for the first time. The mite fed, lived and reproduced onA. mellifera worker brood as a new host in addition toA. florea. Fertile females used once in the experiment produced 1–8 offspring (x 4.30±1.7) per cell. The actual and potential reproduction rates ofEuvarroa in honeybee worker brood cells were 3.62 and 3.95, respectively. Developmental period from egg to adult was 5 and 6–7 days for males and females, respectively. The female commences to mate soon after her deutonymph/adult moult. Copulation was observed in 18 cases.     

Independence and interdependence in collective decision making: an agent-based model of nest-site choice by honeybee swarms

Condorcet''s jury theorem shows that when the members of a group have noisy but independent information about what is best for the group as a whole, majority decisions tend to outperform dictatorial ones. When voting is supplemented by communication, however, the resulting interdependencies between decision makers can strengthen or undermine this effect: they can facilitate information pooling, but also amplify errors. We consider an intriguing non-human case of independent information pooling combined with communication: the case of nest-site choice by honeybee (Apis mellifera) swarms. It is empirically well documented that when there are different nest sites that vary in quality, the bees usually choose the best one. We develop a new agent-based model of the bees'' decision process and show that its remarkable reliability stems from a particular interplay of independence and interdependence between the bees.     

Experimental test of nest-site limitation in mature mixed forests of central British Columbia,Canada

Nest-site availability limits cavity-using populations in many harvested forests; however, little is known about the extent of nest-site limitation in mature forests with a full complement of excavator species and intact processes of cavity creation and loss. To examine the role of nest-site availability in limiting cavity-using populations in mature mixed conifer forests in central British Columbia, Canada, we conducted an 11-year before-after control-impact experiment in which we increased nest-site availability via nest box addition. Our 7 sites (3 treatments, 4 controls) had low cavity densities (<2/ha) prior to treatment and cavity occupation rates were also low (<10%/yr), which is a relationship often cited in the literature as evidence of non-limitation in cavity-nesting populations. Following nest box addition at our treatment sites, which tripled the availability of cavities, total density of bird and mammal nests more than tripled. Density of mountain chickadee (Poecile gambeli) nests increased 9-fold on treatment sites and returned to pre-treatment levels following box removal, suggesting that chickadee populations were limited by cavity availability at our study sites. Density of red squirrel (Tamiasciurus hudsonicus) and northern flying squirrel (Glaucomys sabrinus) nests and roosts also increased significantly at treatment sites following box addition and declined following box removal. We noted little change in chickadee or squirrel nest density at control sites monitored concurrently. Squirrels preferred large-sized over small-sized boxes, and significantly enlarged the entrance areas of small boxes by chewing, suggesting that there may have been a shortage of suitable nest and roost sites for them in our study area. We contend that low cavity occupancy rates may not accurately reflect nest-site availability for cavity nesters in mature forests, and that cavity size may influence the true availability of cavities on the landscape. © 2011 The Wildlife Society.     

Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens)

Here we explored the potential for host shift from honeybee, Apis mellifera, colonies to bumblebee, Bombus impatiens, colonies by the small hive beetle, a nest parasite/scavenger native to sub-Saharan Africa. We investigated small hive beetle host choice, bumblebee colony defence as well as individual defensive behaviour of honeybee and bumblebee workers. Our findings show that in its new range in North America, bumblebees are potential alternate hosts for the small hive beetle. We found that small hive beetles do invade bumblebee colonies and readily oviposit there. Honeybee colonies are not preferred over bumblebee colonies. But even though bumblebees lack a co-evolutionary history with the small hive beetle, they are able to defend their colonies against this nest intruder by removal of beetle eggs and larvae and stinging of the latter. Hence, the observed behavioural mechanisms must be part of a generalistic defence system suitable for defence against multiple attackers. Nevertheless, there are quantitative (worker force) and qualitative differences (hygienic behaviour) between A. mellifera and B. impatiens. Received 16 July 2007; revised 16 January 2008; accepted 17 January 2008.     

Waggle dances in absconding colonies of the red dwarf honeybee, Apis florea

The directional information encoded in the waggle dances of absconding colonies of Apis florea shows how different sites are advertised during decision-making. Colonies of A. florea were observed from the inception of absconding until the swarm settled at a new nest site. The number of waggle dancers at the beginning of the absconding sequence was low, gradually increased and then declined shortly before liftoff. During the last 2 to 0.5?h before liftoff, the dances still indicated different directions. This significantly decreased in the last 0.5?h until only one or two dance directions were being advertised. All colonies reached a near consensus in the last 20 dances before liftoff. The swarm flight path is meandering so the actual distance flown is about twice that indicated by the dances. During the last 3?min the waggle dance in most colonies showed nest target angles that were closely clustered indicating that the final directions advertised were close to the chosen target site. In all absconding/migratory species of honeybees thus far studied, there is a special dance associated with absconding that appears not to select specific destinations but rather a particular direction in search of a new nesting area.     

The role of body size in nest-site selection by secondary cavity-nesting birds in a subtropical Chaco forest

Most bird species that nest in tree cavities globally occur in diverse assemblages in little-studied tropical and subtropical forests which have high rates of habitat loss. Conservation of these communities will require an understanding of how species traits, such as body size, influence nest-site selection. We examined patterns of nest-site selection of secondary cavity-nesting birds at the nest patch, tree and cavity scale, and investigated how these patterns are influenced by body size. Using conditional logistic regression, we compared characteristics of 155 nest tree cavities paired with 155 unused tree cavities in quebracho Schinopsis balansae forests in Chaco National Park, Argentina (2016–2018). The odds of a cavity being used for nesting increased with its depth and height above ground, decreased with entrance size, and were greater for dead trees than live. Small-bodied (13–90 g) species used floor diameters in proportion to availability, but medium- (150–200 g) and large-bodied (400–700 g) species selected cavities with larger floors. Model selection indicated that characteristics at the nest patch scale (canopy cover, tree density) had little effect on nest-site selection when cavity-scale variables were included. Cavity floor diameter, entrance size, cavity height and tree diameter (but not cavity depth) increased with body mass, and larger bird species more often used live trees. Two tree species proved to be key for the community: large and medium-sized birds used almost exclusively large live Schinopsis balansae, whereas small birds used live and dead Prosopis spp. in a proportion greater than its availability. Small birds could be differentiated according to species-specific cavity characteristics, but medium and large species overlapped considerably with one another. Although body mass explained much of the overall variation in tree and cavity characteristics between small and medium/large species, several small-bodied species consistently used cavities outside of the expected characteristics for their body size, suggesting that other natural history traits may play important roles in nest-site selection by small-bodied birds. To retain the full suite of secondary cavity-nesters in species-rich tropical and subtropical forests, it is necessary to conserve a diversity of trees and cavities that meet the full range of nesting requirements of these trait-diverse communities.     

The role of genetic diversity in nest cooling in a wild honey bee, Apis florea

Simulation studies of the task threshold model for task allocation in social insect colonies suggest that nest temperature homeostasis is enhanced if workers have slightly different thresholds for engaging in tasks related to nest thermoregulation. Genetic variance in task thresholds is one way a distribution of task thresholds can be generated. Apis mellifera colonies with large genetic diversity are able to maintain more stable brood nest temperatures than colonies that are genetically uniform. If this phenomenon is generalizable to other species, we would predict that patrilines should vary in the threshold in which they engage in thermoregulatory tasks. We exposed A. florea colonies to different temperatures experimentally, and retrieved fanning workers at these different temperatures. In many cases we found statistically significant differences in the proportion of fanning workers of different patrilines at different experimental temperatures. This suggests that genetically different workers have different thresholds for performing the thermoregulatory task of fanning. We suggest, therefore, that genetically based variance in task threshold is a widespread phenomenon in the genus Apis.     

A Design Pattern for Decentralised Decision Making

The engineering of large-scale decentralised systems requires sound methodologies to guarantee the attainment of the desired macroscopic system-level behaviour given the microscopic individual-level implementation. While a general-purpose methodology is currently out of reach, specific solutions can be given to broad classes of problems by means of well-conceived design patterns. We propose a design pattern for collective decision making grounded on experimental/theoretical studies of the nest-site selection behaviour observed in honeybee swarms (Apis mellifera). The way in which honeybee swarms arrive at consensus is fairly well-understood at the macroscopic level. We provide formal guidelines for the microscopic implementation of collective decisions to quantitatively match the macroscopic predictions. We discuss implementation strategies based on both homogeneous and heterogeneous multiagent systems, and we provide means to deal with spatial and topological factors that have a bearing on the micro-macro link. Finally, we exploit the design pattern in two case studies that showcase the viability of the approach. Besides engineering, such a design pattern can prove useful for a deeper understanding of decision making in natural systems thanks to the inclusion of individual heterogeneities and spatial factors, which are often disregarded in theoretical modelling.     

Traditional versus non-traditional nest-site choice: alternative decision strategies for nest-site selection

In order to understand habitat selection, it is important to consider the way individual animals assess the suitability of a future reproductive site. One way of investigating mechanisms (such as those involved in nest site selection) is to examine breeding success and habitat characteristics in terms of animals returning to a place where they have already reproduced and using the same location over successive years or searching for new alternatives. This approach seems especially suitable for testing recent hypotheses suggesting that nest site selection is an integrative process that includes the use of social information (e.g. past breeding success of conspecifics). Determining the factors that elicit conservative or innovative behaviour regarding nest-site selection could be important for improving our understanding of habitat selection decisions in animals. More than half of the nests of the long-distance migratory lesser grey shrike Lanius minor, are built in the same or neighbouring trees. We found no evidence that habitat characteristics influence nest-site tradition. On the contrary, social information in terms of the presence of conspecifics and past reproductive success in terms of complete nest failures due to nest predation (but not detailed information such as variation in fledgling number) influenced nest-site tradition. Hence, social information and past reproductive success may play a role in nest-site choice in this species. Our results further demonstrate that previous experience with a nest site does not appear to be beneficial.     

Transcriptome differences in the hypopharyngeal gland between Western Honeybees (Apis mellifera) and Eastern Honeybees (Apis cerana)

Background

Apis mellifera and Apis cerana are two sibling species of Apidae. Apis cerana is adept at collecting sporadic nectar in mountain and forest region and exhibits stiffer hardiness and acarid resistance as a result of natural selection, whereas Apis mellifera has the advantage of producing royal jelly. To identify differentially expressed genes (DEGs) that affect the development of hypopharyngeal gland (HG) and/or the secretion of royal jelly between these two honeybee species, we performed a digital gene expression (DGE) analysis of the HGs of these two species at three developmental stages (newly emerged worker, nurse and forager).

Results

Twelve DGE-tag libraries were constructed and sequenced using the total RNA extracted from the HGs of newly emerged workers, nurses, and foragers of Apis mellifera and Apis cerana. Finally, a total of 1482 genes in Apis mellifera and 1313 in Apis cerana were found to exhibit an expression difference among the three developmental stages. A total of 1417 DEGs were identified between these two species. Of these, 623, 1072, and 462 genes showed an expression difference at the newly emerged worker, nurse, and forager stages, respectively. The nurse stage exhibited the highest number of DEGs between these two species and most of these were found to be up-regulated in Apis mellifera. These results suggest that the higher yield of royal jelly in Apis mellifera may be due to the higher expression level of these DEGs.

Conclusions

In this study, we investigated the DEGs between the HGs of two sibling honeybee species (Apis mellifera and Apis cerana). Our results indicated that the gene expression difference was associated with the difference in the royal jelly yield between these two species. These results provide an important clue for clarifying the mechanisms underlying hypopharyngeal gland development and the production of royal jelly.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-744) contains supplementary material, which is available to authorized users.