Memory and sun compensation by honey bees

Summary Experiments with two species of honey bees (Apis mellifera andA. cerana) have revealed that bees form a detailed memory of the spatial and temporal pattern of the sun's azimuthal movement, using local landmarks as a reference for the learning. These experiments were performed on overcast days, and consisted of removing a hive from one site in which bees had been trained to find food by flying along a prominent landmark, and displacing it to a similar site in which the landmark was aligned in a different compass direction. On overcast days, bees which flew along the landmark in the new site oriented their waggle dances in the hive as if they had actually flown in the training site. Thus, they confused the two sets of landmarks and set their dance angles according to a memory of the sun's position relative to the original landmarks. Furthermore, the dances changed in correspondence with the sun's azimuthal shift over several hours, even reflecting (approximately) the regular temporal variations in the rate of shift; such features of the sun's course must therefore be stored in memory. The primary mechanism underlying the learning of this pattern is probably similar to that proposed by New and New (1962): bees store in memory several time-linked solar azimuthal positions relative to features of the landscape, and refer to this stored array when they need to determine an unknown azimuth intermediate between two known positions.During the cloudy-day displacement experiments, celestial cues often appeared to bees in the new site, contradicting the stored information on which they had been basing their dances. Although most bees quickly adopted the dance angle reflecting their actual direction of flight relative to the sun, some later reverted to the original dance angle, indicating that the information on which it was based had remained in memory when the new information was being expressed; other bees performed bimodal dances which expressed both sets of information in alternate waggle runs. The separation in memory implied by these behaviors may reflect a neural strategy for updating a previously stored relationship between celestial and terrestrial references with new information presented by seasonal changes in the sun's course or by newly learned landmarks.     

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.     

A comparison of the dance language in<Emphasis Type="Italic"> Apis mellifera carnica</Emphasis> and<Emphasis Type="Italic"> Apis florea</Emphasis> reveals striking similarities

Honeybees have a dance language by which successful foragers inform nestmates about attractive food patches. The classical concept of dialects in the dance language of honeybees points to two differences in the dances by different species and races, firstly in the flight distance at which the dancers start performing waggle dances instead of round dances, and secondly in the circuit duration of the waggle dance performed for a given flight distance. However, recent findings have indicated that the dance language is influenced and affected by a number of parameters, both genetic and environmental. The current study was carried out to see whether the distance at which dancers change from round dances to waggle dances is statistically different in two different species, Apis mellifera carnica and A. florea and to develop a set of definitions for such comparative studies. Results show that the two species do not differ in the relative proportion of waggle dances and round dances performed at a given distance. Thus, this study points to the need of addressing the dialect question again.     

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.     

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.     

Working against gravity: horizontal honeybee waggle runs have greater angular scatter than vertical waggle runs

The presence of noise in a communication system may be adaptive or may reflect unavoidable constraints. One communication system where these alternatives are debated is the honeybee (Apis mellifera) waggle dance. Successful foragers communicate resource locations to nest-mates by a dance comprising repeated units (waggle runs), which repetitively transmit the same distance and direction vector from the nest. Intra-dance waggle run variation occurs and has been hypothesized as a colony-level adaptation to direct recruits over an area rather than a single location. Alternatively, variation may simply be due to constraints on bees' abilities to orient waggle runs. Here, we ask whether the angle at which the bee dances on vertical comb influences waggle run variation. In particular, we determine whether horizontal dances, where gravity is not aligned with the waggle run orientation, are more variable in their directional component. We analysed 198 dances from foragers visiting natural resources and found support for our prediction. More horizontal dances have greater angular variation than dances performed close to vertical. However, there is no effect of waggle run angle on variation in the duration of waggle runs, which communicates distance. Our results weaken the hypothesis that variation is adaptive and provide novel support for the constraint hypothesis.     

Crossfostered drones ofApis cerana (Fabricius, 1793) andApis koschevnikovi (Buttel-Reepen, 1906) fly at their species specific mating times

Summary Reciprocal transfer of sealed drone brood between colonies ofApis cerana andApis koschevnikovi was successful and resulted in four colonies (two of each species) with a mixed drone population. Flights ofApis cerana drones occurred between 14.00 and 16.15 regardless whether they were in a conspecific or alien colony.Apis koschevnikovi drones also flew at their species specific time from 16.45 to 18.30. A variance estimation revealed that 99.4% of the total variance depended on the species of the drone. In contrast to theApis drone's general biological dependence upon the colony, crossfostered drones ofApis cerana andApis koschevnikovi showed an unexpected autonomy in chosing their mating flight time.     

Polarized skylight orientation in the desert antCataglyphis

Summary The desert antCataglyphis bicolor is able to use the pattern of polarized light in the sky as compass. By confronting the ant to single spots of artificially and naturally polarized light it is shown howCataglyphis uses the polarization pattern.When exposed to a horizontal e-vector,Cataglyphis was always oriented correctly. Orientation errors occurred, however, when other e-vector directions were presented. This indicates that the e-vector positions assumed by the ant do not coincide with the e-vector positions actually realized in the sky. From this it is concluded thatCataglyphis has no detailed knowledge of the actual azimuthal positions of the e-vectors. Instead, it is relying on a simplified celestial map of the polarization patterns in the sky (Fig. 7).Usually, the ant did not confuse celestial spots with identical e-vector directions. Even at sunset when the polarization pattern is completely ambiguous, correct orientation occurred. This suggests that the ant uses additional celestial cues such as the degree of polarization, the color or the intensity to find its way home when the sun is obscured.     

Proboscis behavioral response of four honey bee Apis species towards different concentrations of sucrose,glucose, and fructose

Honey bees forage for pollen and nectar. Sugar is an important stimulus for foraging and a major source of energy for honey bees. Any differential response of bees to different concentrations of sugary nectar can affect their foraging. The sugar responsiveness of Apis species (Apis dorsata, Apis florea, and Apis cerana) was determined in comparison to that of Apis mellifera by evaluating the proboscis extension response (PER) with eight serial concentrations (0.00001, 0.0001, 0.001, 0.01, 0.1, 0.5, 1.0, and 1.5 M) of sucrose, glucose and fructose. Nectar foragers of bee species (A. dorsata, A. florea, A. cerana, and A. mellifera) exhibited an equal response for sucrose, glucose, and fructose, with no significant differences in their PER at all tested concentrations of these sugars within the same species. The inter-species comparison between Apis species revealed the differential responsiveness to the different concentrations of sugars, and the lowest concentration at which a response occurs was considered as the response threshold of these bee species for sugar solutions. A. mellifera presented significantly higher responsiveness than A. dorsata to low concentrations (0.00001, 0.0001, 0.001, 0.01, and 0.1 M) of sucrose, glucose and fructose. A. mellifera displayed a significantly higher response to water than A. dorsata. A. florea and A. mellifera presented no significant difference in their responsiveness to sucrose, glucose, and fructose at all tested concentrations, and their water responsiveness was also significantly at par but relatively higher in A. mellifera than in A. florea. Likewise, the responsiveness of A. cerana and A. mellifera to different concentrations of sucrose, glucose and fructose was significantly at par with no difference in their water responsiveness. This study represents preliminary research comparing the response of different honey bee species to three sugar types at different concentrations. The results imply that the native species are all better adapted than A. mellifera under local climate conditions.     

Mechanisms of gravity processing by leg and abdominal gravity receptors in bees

In Apis florea, the strength of the geotactic turning tendency depends on the inclination γ of the walking plane, from γ = 15° to γ = 90° (vertical). In contrast to Bombus terrestris, pedal proprioreceptors are not involved in gravity reception in A. florea, whereas the petiole organ, as in Bombus, is a gravity receptor. Stimulation of this sense organ, by loading the abdomen of the bee, causes a decrease of the standard deviation of the walking directions from the negative and positive geotactic basic direction.The processing of gravity in Apis cerana is similar to that in Apis mellifera. The metageotactic reaction is controlled by bristle fields of the petiole and by pedal proprioreceptors. Loading the thorax, as well as eliminating the petiole organ, alters the type of geotactic reaction. On the contrary, a simultaneous change of stimulus for the leg organs and the petiolus organ by loading the abdomen does not affect the metageotactic reaction.     

Polarotaxis and scototaxis in the supratidal amphipod Platorchestia platensis

Talitrid amphipods use many cues for orientation during forays between temporary burrows and feeding areas, and for locating beaches when submerged, with visual cues being particularly important. Little evidence exists for polarized light among these visual cues despite extensive orientation by celestial and underwater polarized light in other crustaceans and in insects. We used electroretinography to assess spectral sensitivity in the eye of the beach flea Platorchestia platensis, and behavioral studies to test whether linearly polarized light serves as an orientation cue. Two spectral classes were present in the P. platensis eye with maxima at 431 and 520 nm. Non-uniform orientation of amphipods in the laboratory arena required either light/dark or polarized cues. Scototactic movements depended on arena conditions (day/night, wet/dry), while orientation under linearly polarized light was wavelength-dependent and parallel to the e-vector. Subsequent tests presented conflicting and additive scototactic and polarotactic cues to differentiate among these responses. In dry conditions, orientation parallel to the polarization e-vector overcame a dominant negative scototaxis, confirming that polarotaxis and scototaxis are separate orientation responses in this species. These behavioral results demonstrate talitrid amphipods can perceive and orient to linearly polarized light, and may use it to orient toward preferred zones on beaches.     

Similar but not the same: insights into the evolutionary history of paralogous sex-determining genes of the dwarf honey bee Apis florea

Studying the fate of duplicated genes provides informative insight into the evolutionary plasticity of biological pathways to which they belong. In the paralogous sex-determining genes complementary sex determiner (csd) and feminizer (fem) of honey bee species (genus Apis), only heterozygous csd initiates female development. Here, the full-length coding sequences of the genes csd and fem of the phylogenetically basal dwarf honey bee Apis florea are characterized. Compared with other Apis species, remarkable evolutionary changes in the formation and localization of a protein-interacting (coiled-coil) motif and in the amino acids coding for the csd characteristic hypervariable region (HVR) are observed. Furthermore, functionally different csd alleles were isolated as genomic fragments from a random population sample. In the predicted potential specifying domain (PSD), a high ratio of π_N/π_S=1.6 indicated positive selection, whereas signs of balancing selection, commonly found in other Apis species, are missing. Low nucleotide diversity on synonymous and genome-wide, non-coding sites as well as site frequency analyses indicated a strong impact of genetic drift in A. florea, likely linked to its biology. Along the evolutionary trajectory of ~30 million years of csd evolution, episodic diversifying selection seems to have acted differently among distinct Apis branches. Consistently low amino-acid differences within the PSD among pairs of functional heterozygous csd alleles indicate that the HVR is the most important region for determining allele specificity. We propose that in the early history of the lineage-specific fem duplication giving rise to csd in Apis, A. florea csd stands as a remarkable example for the plasticity of initial sex-determining signals.     

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.     

Celestial orientation in the marbled newt (Triturus marmoratus)

Orientation toward breeding ponds plays an important role in the seasonal movements of amphibians. In this study, adult marbled newts were tested in a circular arena to determine sensory cues used to locate breeding ponds. Animals were collected from a temporary pond situated in northern Spain, taken to the experimental site 340 m distant, and tested for orientation under a variety of conditions (i.e., orientation under a clear night sky, orientation under an overcast night sky, and orientation under a clear night sky in the presence of an altered geomagnetic field). These investigations have demonstrated that the marbled newt is able to orient using celestial cues. Animals chose a compass course in the direction of their breeding pond only when celestial cues were available. Conversely, the ambient geomagnetic field does not seem to be relevant to orientation of marbled newts since they were unable to orient themselves using the ambient geomagnetic field in the absence of celestial cues. Electronic Publication     

Memory and chemical communication in the orientation of two mass-recruiting ant species

Summary The relative contribution of visual and chemical components in the orientation ofLasius niger andIridomyrmex humilis (Argentine ant) workers during mass recruitment to newly discovered food sources is analyzed over short time intervals. While both species orient in response to the trail pheromone, a large number ofL. niger foragers rapidly switch to a more individual orientation, based on their memory of environmental cues.I. humilis workers, on the other hand, predominantly use collective chemical cues. The effect of the number of reinforcements on visual learning and its interference with chemical communication show that olfactory cues always prevail in the Argentine ant. InL. niger, the proportion of ants orienting to visual cues is independent of the trail concentration. Detailed observations of the trail-laying behavior of individually marked foragers show that nearly all theI. humilis workers initially lay a trail, whereas only half theL. niger foragers do so. This proportion decreases considerably with the number of trips performed byL. niger workers, while remaining constant for the Argentine ants. These results are interpreted with respect to the species' behavioral ecology.     

Hierarchy of sun,beach slope,and landmarks as cues for Y-axis orientation of the supratidal amphipod Talorchestia longicornis (Say)

The semi-terrestrial amphipod Talorchestia longicornis (Say) undergoes Y-axis orientation and has a hierarchy among orientation cues. A previous study found that they used sun compass orientation and moved in the onshore direction of the home beach in both air and water. The present study determined whether this species could also use local landmarks and beach slope as orientation cues. They oriented upslope in simulated darkness in the laboratory on both dry and wet sand with threshold slopes of 2° and 4°, respectively. When tested outside in an arena in air on wet sand, they were disoriented when sun, slope, and landmarks were absent as cues. If presented with single cues, they moved upslope, toward landmarks and in the up-beach direction of the home beach during sun compass orientation. Using paired cues, sun was dominant over slope and landmarks, while slope was dominant over landmarks. In the presence of all three cues, amphipods displayed sun compass orientation in all test combinations except when slope and landmarks were paired together against the sun, which evoked a bimodal response. Thus, the hierarchy of cues for up-beach movement of T. longicornis during Y-axis orientation is the sun, then the slope, and finally the landmarks.     

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.     

A comprehensive hypothesis on the migration of European glass eels (Anguilla anguilla)

The European eel (Anguilla anguilla) is a catadromous fish that spawns in the Sargasso Sea. As larvae, eels cross the Atlantic Ocean and reach the continental slope of Europe, where they metamorphose into post‐larval glass eels. These reach the continent, where some enter fresh water, some remain in marine waters, and others move between fresh and marine waters. After 5–25 years, as adult silver eels, they migrate back from fresh water to the Sargasso Sea to spawn and die. The glass eel stage is a critical step during which the eels cross the continental shelf and recruit to estuaries, where they facultatively transition to fresh water. Extensive research has been conducted to understand the behavioural mechanisms and environmental cues that aid and guide glass eels' migration. Glass eels follow odours and salinity gradients, they avoid light, and they change orientation and depth according to the tides. Recent work revealed that European glass eels also use Earth's magnetic field and lunar cues to orient. However, while we understand many aspects of their orientation behaviour, a unifying theory describing how glass eels migrate from the continental slope to fresh water is lacking. The goal of this review is to develop a comprehensive hypothesis on the migration of European glass eels, integrating previous knowledge on their orientation behaviour with recent findings on magnetic and celestial orientation. This review follows the journey of a hypothetical glass eel, describing the nature and the role of orientation cues involved at each step. I propose that, although glass eels have the sensory capacity to use multiple cues at any given time, their migration is based on a hierarchical succession of orientation mechanisms dictated by the physical properties of the environments that they occupy: (i) lunar and magnetic cues in pelagic water; (ii) chemical and magnetic cues in coastal areas; and (iii) odours, salinity, water current and magnetic cues in estuaries.     

Some observations on the concurrent parasitization ofApis florea byTropilaelaps clareae andEuvarroa sinhai

Adult bees, worker brood cells and drone brood cells ofApis florea were examined for the presence of mites by stereo microscope and by washing with soap. Tropilaelaps clareae was only found on adult bees;Euvarroa sinhai on adult bees and drone brood. The level ofT. clareae infestation is always very low, generally not exceeding 0.1%; that ofE. sinhai is somewhat higher. The mites were never found together on a single bee.