Ground-nesting bees determine the location of their nest relative to a landmark by other than angular size cues

Bees and wasps acquire a visual representation of their nest's environment and use it to locate their nest when they return from foraging trips. This representation contains among other features cues to the distance of near-by landmarks. We worked with two species of ground-nesting bees, Lasioglossum malachurum (Hymenoptera: Halictidae), Dasypoda hirtipes (Hymenoptera: Melittidae) and asked which cues to landmark distance they use during homing. Bees learned to associate a single cylindrical landmark with their nest's location. We subsequently tested returning bees with landmarks of different sizes and thus introduced large discrepancies between the angular size of the landmark as seen from the nest during training and its distance from the nest. The bees' search behaviour and their choice of dummy nest entrances show that both species of ground-nesting bees consistently search for their nest at the learned distance from landmarks. The influence of the apparent size of landmarks on the bees' search and choice behaviour is comparatively weak. We suggest that the bees exploit cues derived from the apparent speed of the landmark's image at their retina for distance evaluation.     

Sex-inducing effect of a hydrophilic fraction on reproductive switching in the planarian Dugesia ryukyuensis (Seriata, Tricladida)

Background

Insects are known to rely on terrestrial landmarks for navigation. Landmarks are used to chart a route or pinpoint a goal. The distant panorama, however, is often thought not to guide navigation directly during a familiar journey, but to act as a contextual cue that primes the correct memory of the landmarks.

Results

We provided Melophorus bagoti ants with a huge artificial landmark located right near the nest entrance to find out whether navigating ants focus on such a prominent visual landmark for homing guidance. When the landmark was displaced by small or large distances, ant routes were affected differently. Certain behaviours appeared inconsistent with the hypothesis that guidance was based on the landmark only. Instead, comparisons of panoramic images recorded on the field, encompassing both landmark and distal panorama, could explain most aspects of the ant behaviours.

Conclusion

Ants navigating along a familiar route do not focus on obvious landmarks or filter out distal panoramic cues, but appear to be guided by cues covering a large area of their panoramic visual field, including both landmarks and distal panorama. Using panoramic views seems an appropriate strategy to cope with the complexity of natural scenes and the poor resolution of insects' eyes. The ability to isolate landmarks from the rest of a scene may be beyond the capacity of animals that do not possess a dedicated object-perception visual stream like primates.     

The significance of visual landmarks for navigation of the giant tropical ant,Paraponera clavata (Formicidae,Ponerinae)

Summary Workers of the giant tropical ant,Paraponera clavata, use trail pheromones for orientation and recruitment of nestmates. However, chemical markings may not always be sufficient for successful navigation in complex three-dimensional terrain, and additional orientation cues may be required. Behavioral field experiments were performed to investigate the significance of visual landmarks for homing foragers. Animals which were prevented from seeing the canopy were unable to navigate back to the nest, even though trail pheromones were still present. In contrast, foragers found their way back to the nest after their trail pheromones had been abolished but their visual scenes remained unchanged. This emphasizes the important role of visual landmarks during spatial orientation in homingP. clavata foragers. Individually foraging scouts were discovered in the understory of the forest floor up to 30 m away from their nest. They were rewarded, and displaced between 0.8 m and 13.6 m. Fifteen out of 16 animals had no difficulties in finding the nest entrance despite the altered appearance of local and distant landmarks at the release site. Apparently the scouts were able to recognize the visual scenes at the release site, and used them for reference to locate the nest entrance. In contrast, ants displaced from their nest to sites around 4 m away had more difficulties to re-find the nest.     

Landmark cues can change the motivational state of desert ant foragers

Desert ants of the genus Cataglyphis rely on path integration vectors to return to the nest (inbound runs) and back to frequently visited feeding sites (outbound runs). If disturbed, e.g., experimentally displaced on their inbound runs, they continue to run off their home-bound vector, but if disturbed in the same way on their outbound runs, they do not continue their feeder-based vector, but immediately switch on the home-bound state of their path integration vector and return to the nest. Here we show that familiar landmarks encountered by the ants during their run towards the feeder can change the ants’ motivational state insofar that the ants even if disturbed continue to run in the nest-to-feeder direction rather than reverse their courses, as they do in landmark-free situations. Hence, landmark cues can cause the ants to change their motivational state from homing to foraging.     

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.     

Long-distance Homing Ability in Dasypoda altercator (Hymenoptera,Melittidae)

Homing rates and initial orientations after release from different directions were investigated in the solitary bee Dasypoda altercator. Homing rates and the proportion of individuals returning on the day of release declined with distance, implying that homing from greater distances is not based solely on the use of landmarks. A long duration of return (often not on the same day) and high efficiency of homing (four bees out of 10 returned from a 4 km distance over the lake), as well as an increase in average return speed ? 10 m/min) with distance of bees homing on the same day suggest that homing is also not based upon radial scatter as the sole tactic. This is supported by the observation that the initial orientations of the bees were not equally probable. Departures towards the sun greatly exceeded those away from the sun and the bees also tended to depart in cardinal geographical (or geomagnetic) directions, preferring meridional directions (especially southward) to parallel ones (of which east was preferred). Departure directions did not depend on wind direction but did depend, to some extent, on the landscape features of release sites. However, bees neither tended to depart in the direction of the nest, nor did homing success correlate with the direction of departure in relation to that of the nest.     

Individual scent marking of the nest entrance as a mechanism for nest recognition inXylocopa pubescens (Hymenoptera: Anthophoridae)

The mechanism by which female Xylocopa pubescenslocate their nest in a nesting aggregation was investigated. The bees were induced to nest in canes to which uniform nest entrances were attached. The results of nest displacement experiments revealed that the bees use visual cues for proximate orientation,but at very close range they also use olfactory cues. This conclusion was corroborated by the results of experiments in which the nest entrances were either removed or exchanged for alien nest entrances. Moreover, habituation experiments strongly indicated that the bees impart their individual marking at the nest entrance and that they can learn and memorize the individual odors of the neighboring bees.     

Relationship between body size and homing ability in the genus Osmia (Hymenoptera; Megachilidae)

Abstract 1. The maximum homing ability of female bees, that is, their capacity to return to the nest after being displaced a certain distance, is considered to be an estimate of their maximum foraging distance. 2. The present study provides data on homing ability and body weight for Osmia lignaria and combines them with data for five other congenerics, O. rufa, O. cornuta, O. pedicornis, O. cornifrons, and O. emarginata for analysis. These species are important pollinators of spring‐flowering plants, and some have been developed as commercial crop pollinators. 3. It is shown that homing ability is positively and linearly related to body weight (r² = 0.81; P = 0.01). 4. These results should be of use in selecting Osmia species as potential crop pollinators and establishing adequate buffer distances around genetically modified crops.     

Large scale homing in honeybees

Honeybee foragers frequently fly several kilometres to and from vital resources, and communicate those locations to their nest mates by a symbolic dance language. Research has shown that they achieve this feat by memorizing landmarks and the skyline panorama, using the sun and polarized skylight as compasses and by integrating their outbound flight paths. In order to investigate the capacity of the honeybees' homing abilities, we artificially displaced foragers to novel release spots at various distances up to 13 km in the four cardinal directions. Returning bees were individually registered by a radio frequency identification (RFID) system at the hive entrance. We found that homing rate, homing speed and the maximum homing distance depend on the release direction. Bees released in the east were more likely to find their way back home, and returned faster than bees released in any other direction, due to the familiarity of global landmarks seen from the hive. Our findings suggest that such large scale homing is facilitated by global landmarks acting as beacons, and possibly the entire skyline panorama.     

Visual marks learned by the solitary bee Megachile rotundata for localizing its nest

We studied homing behaviour of leaf-cutter bees, Megachile rotundata, by using artificial landmarks. We evaluated their nest-searching behaviour in different test situations to elucidate the nature of the visual marks they used in this task. When we modified or removed geometrical figures surrounding the nest, the bees searched for longer, showing that they noticed the introduced changes. However, these manipulations never prevented bees from finding their nest, suggesting that other visual cues were crucial in the task. Manipulations of the edges provided by the boundaries of the device (nest block, metal sheet on which the block was mounted) strongly impaired the homing performance. The further away the edges that were left intact, the stronger was the impairment of the homing behaviour. These results suggest that bees learn the distances of the various edges from the goal and that edges have a hierarchical significance according to their distance from the nest. The most distant edges provide vague information, which suffices to guide the insect towards the next edge in the sequence, until it recognizes the final, precise location of the nest. The results support the conclusion that information on distances is acquired using cues derived from motion parallax generated by the insect's self-motion. Recognition of edge parameters such as position and orientation might be achieved by an image-matching mechanism based on dynamic processes. Thus, in the homing task, there is no clear discrepancy between the eidetic and the parametric hypotheses of spatial representation.     

Can the antCataglyphis cursor (Hymenoptera: Formicidae) encode global landmark-landmark relationships in addition to isolated landmark-goal relationships?

The antCataglyphis cursor was tested for its landmark-based homing in a laboratory setting. Workers were induced to go down a tube at the center of an arena to forage. On the periphery of the arena were four different black shapes serving as the only distinguishing visual landmarks, i.e., a cross, a circle, a triangle, and a square. The purpose was to show that the spatial memory of ants represents something of the overall arrangement of landmarks. When first released into the arena, the ants were not oriented toward home in their navigation. After 2 days of free access in the usual landmark setup, the ants learned to orient rapidly significantly goalward. When landmarks were all removed, they did not orient in any direction significantly. When the landmarks were rotated by 90°, their compass positions were changed but their relative positions maintained, and the ants rotated their heading by a similar amount. This rotated homing direction implies that the array of landmarks was used as the only source of directional determination. When the landmark nearest their home was absent, but the other three were in their usual places, the ants were slightly homeward oriented at one-quarter of the way, but not at one-half of the way when the other landmarks were behind them. When the landmarks were randomly permuted, both their compass positions and their overall spatial relationships were altered, and the ants were not significantly oriented in any direction. These results indicate that spatial memory in the antC. cursor encodes global landmark-landmark relations. Thus, ants can abstract certain topological properties of their environment.     

Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera)

Bees and wasps are known to use a visual representation of the nest environment to guide the final approach to their nest. It is also known that they acquire this representation during an orientation flight performed on departure.A detailed film analysis shows that orientation flights in solitary wasps of the genus Cerceris consist of a systematic behavioural sequence: after lift-off from the nest entrance, wasps fly in ever increasing arcs around the nest. They fly along these arcs obliquely to their long axis and turn so that the nest entrance is held in the left or right visual field at retinal positions between 30° and 70° from the midline. Horizontal distance from the nest and height above ground increase throughout an orientation flight so that the nest is kept at retinal elevations between 45° and 60° below the horizon. The wasps' rate of turning is constant at between 100°/s and 200°/s independent of their distance from the nest and their ground velocity increases with distance. The consequence of this is that throughout the flight wasps circle at a constant angular velocity around the nest.Orientation flights are strongly influenced by landmark lay-out. Wasps adjust their flight-path and their orientation in a way that allows them to fixate the nest entrance and to hold the closest landmark in their frontal visual field.The orientation flight generates a specific topography of motion parallax across the visual field. This could be used by wasps to acquire a series of snapshots that all contain the nest position, to acquire snapshots of close landmarks only (distance filtering), to exclude shadow contours from their visual representation (figure-ground discrimination) or to gain information on the distance of landmarks relative to the nest.     

Target-directed Orientation in Displaced Honeybees

Under sunny weather conditions, displaced honeybees (Apis mellifera) usually fly into the celestial compass direction and thus may be misled from their goal, or they are disorientated. Under cloudy conditions, they may determine the celestial compass direction from prominent landmarks. They may also fly directly toward their goal from a release site. In two experiments, we investigated the orientation of displaced bees when a landmark (target) was close to the goal under different weather conditions. It is shown that in sunny conditions, the celestial compass will override target orientation under most conditions. Under 100% cloud cover, the celestial compass direction retrieved from landmarks modulates target-orientated behaviour but is not by itself a primary orientation factor. The bees will fly toward a previously encountered landmark that signals the target, and in case of several similar landmarks which are visible to the bees, they will choose the one in the direction nearest the celestial compass direction. The results indicate that honeybee orientation is the result of a set of context-specific interdependent orientation mechanisms.     

A stingless bee (Melipona seminigra) uses optic flow to estimate flight distances

Foragers of a stingless bee, Melipona seminigra, are able to use the optic flow experienced en route to estimate flight distance. After training the bees to collect food inside a flight tunnel with black-and-white stripes covering the side walls and the floor, their search behavior was observed in tunnels lacking a reward. Like honeybees, the bees accurately estimated the distance to the previously offered food source as seen from the sections of the tunnel where they turned around in search of the food. Changing the visual flow by decreasing the width of the flight tunnel resulted in the underestimation of the distance flown. The removal of image motion cues either in the ventral or lateral field of view reduced the bees' ability to gauge distances. When the feeder inside the tunnel was displaced together with the bees feeding on it while preventing the bee from seeing any image motion during the displacement the bees experienced different distances on their way to the food source and during their return to the nest. In the subsequent test the bees searched for the food predominantly at the distance associated with their return flight.     

Use of Landmarks in Three Species of Food-storing Corvids

The use of landmarks by Clark's nutcrackers (Nucifraga columbiana), pinyon jays (Gymnorbinus cyanocepbalus), and Western scrub jays (Apbelocoma coerulescens) was investigated in three experiments. In the first experiment, birds were trained to find a hidden food reward beneath wood chips near a plastic landmark located 20 cm from one edge of a stationary tray. During unrewarded test trials, all species displaced their searching in response to movement of the landmark in both parallel and perpendicular directions; however, searching was displaced significantly more in the parallel direction. In a second experiment, the landmark was removed with the tray stationary or shifted. When the tray was shifted, all species responded by searching relative to the shifted tray. This indicates that the global (room) cues were not being used as salient landmarks. In the third experiment, the tray was placed in different positions for each trial, making global cues unreliable. As in experiment 1, all species displaced their searching in response to parallel and perpendicular movement of the landmark, with movement being similar in both directions. These results indicate no species differences on this landmark-use task.     

Orientation and Communication in the Neotropical Ant Odontomachus bauri Emery (Hymenoptera,Formicidae, Ponerinae)

The Neotropical species Odontomachus bauri employs canopy orientation during foraging and homing. An artificial canopy pattern above the ants is much more effective as an orientation cue than horizontal landmarks or chemical marks. However, both horizontal visual cues and chemical marks on the ground can serve in localizing the nest entrance. Successful O. bauri foragers recruit nestmates to leave the nest and search for food. However, the recruitment signals do not contain directional information. Antennation bouts and pheromones from the pygidial gland most likely serve as stimulating recruitment signals. Secretions from the mandibular and poison gland elicit alarm and attack behavior.     

Path integration controls nest-plume following in desert ants

The desert ant Cataglyphis fortis is equipped with sophisticated navigational skills for returning to its nest after foraging. The ant's primary means for long-distance navigation is path integration, which provides a continuous readout of the ant's approximate distance and direction from the nest. The nest is pinpointed with the aid of visual and olfactory landmarks. Similar landmark cues help ants locate familiar food sites. Ants on their outward trip will position themselves so that they can move upwind using odor cues to find food. Here we show that homing ants also move upwind along nest-derived odor plumes to approach their nest. The ants only respond to odor plumes if the state of their path integrator tells them that they are near the nest. This influence of path integration is important because we could experimentally provoke ants to follow odor plumes from a foreign, conspecific nest and enter that nest. We identified CO(2) as one nest-plume component that can by itself induce plume following in homing ants. Taken together, the results suggest that path-integration information enables ants to avoid entering the wrong nest, where they would inevitably be killed by resident ants.     

Use of local cues in the night-time navigation of the wandering desert spider <Emphasis Type="Italic">Leucorchestris arenicola</Emphasis> (Araneae,Sparassidae)

Adult male Leucorchestris arenicola can walk round-trips of several tens of meters in search of females. Most excursions end with the spiders returning to their burrow. For small animals homing over distances of several meters is theoretically impossible without the aid of external cues. It was investigated, whether the spiders use local cues or they rely solely on global cues. Individually marked male spiders were captured during their excursions and displaced several meters inside an opaque box. Ten out of twelve displaced spiders returned to their burrows. This shows that the male L. arenicola are using local cues during their homing, as the comparatively small displacement distances could not be detected by means of global, e.g. celestial cues. In order to test whether the spiders could be using olfactory guidance, the burrows were displaced by 2 m while the spiders were out on their journeys. In 12 out of 15 experiments, the spiders did not find their burrows. These results show that the burrows do not function as olfactory beacons for the homing spiders.     

Homing in the swimming crab Thalamita crenata: a mechanism based on underwater landmark memory

We investigated whether Thalamita crenata, a swimming crab found on the East African intertidal flats, uses landmarks to locate its refuges. We modified the visual panorama of an intertidal flat, using conspicuous movable objects, and conducted homing trials with the local population of swimming crabs. In the first set of trials, after being moved away from their dens, the crabs were immediately able to find other known dens, using direct shortcut paths. In the second set of trials we moved all the artificial landmarks surrounding a crab's den 5 m away and then displaced the crab itself. The crabs made initial navigational errors in accordance with the new position of the landmarks; this shows that they oriented themselves by remembering the landmarks. We then repositioned the landmarks and released the crabs far from the familiar area, on a similar flat. This time the crabs could rely only on the artificial landmarks; they used this information and reached the point where home should have been according to the landmarks. Thus, T. crenata showed good spatial knowledge, based on the storage of landmark memories. This orienting mechanism is much more flexible and complex than those of other crabs and is comparable to the route-based memory of honeybees, Apis mellifera. Copyright 2000 The Association for the Study of Animal Behaviour.