Size is relative: use of relational concepts by wild hummingbirds.

Rufous hummingbirds (Selasphorus rufus) will readily learn the location and the colour of rewarded flowers within their territory. But if these birds could apply a relational concept such as 'the larger flowers have more nectar', they could forego learning the locations of hundreds of individual flowers. Here, we investigated whether wild male territorial rufous hummingbirds might use 'larger than' and 'smaller than' relational rules and apply them to flowers of different sizes. Subjects were trained to feed consistently from one of two flowers. Although the flowers differed only in size, the reward was always contained in the same-size flower. The birds were then tested on a choice of two empty flowers: one of the familiar size and the other a novel size. Hummingbirds applied relational rules by choosing the flower that was of the correct relational size rather than visiting the flower of the size rewarded during training. The choices made by the hummingbirds were not consistent with alternative mechanisms such as peak shift or associative learning. We suggest that while hummingbirds are very good at remembering the spatial locations of rewarding flowers, they would be able to use relative rules when foraging in new and changing environments.

Hummingbirds modify their routes to avoid a poor location.

Traplining, when animals repeat the order in which they visit a number of locations, is taxonomically widespread, but little is known about which factors influence the routes that animals follow. For example, as the quality of rewarding locations changes over time, foragers are expected to update their traplines, either to prioritize locations where the reward increases or to avoid locations that have ceased to be profitable. Here, we tested how traplining wild hummingbirds responded to increases or to decreases in the sucrose concentration of one of the flowers on their trapline. Hummingbirds did not change their trapline to visit the flower with the increased reward first, but by changing the order in which they visited flowers, they avoided a flower that contained a decreased reward. Depending on where along the trapline the reduced-content flower occurred, hummingbirds either changed the origin of their trapline or changed the direction in which they flew around their trapline. It may be that this asymmetric modification of foraging traplines is especially noticeable in risk-averse foragers, such as these territorial hummingbirds.

Estimating on the fly: The approximate number system in rufous hummingbirds (Selasphorus rufus).

When presented with resources that differ in quantity, many animals use a numerosity system to discriminate between them. One taxonomically widespread system is the approximate number system. This is a numerosity system that allows the rapid evaluation of the number of objects in a group and which is regulated by Weber's Law. Here we investigated whether wild, free-living rufous hummingbirds (Selasphorus rufus) possess an approximate number system. The hummingbirds were presented with two experiments. In the first we investigated whether hummingbirds spontaneously chose an array containing more flowers than an alternate array. In the second we asked whether the hummingbirds could learn to use numerosity as a cue to which of two arrays contained the better reward. The birds did not spontaneously prefer an array containing more flowers. After minimal training, however, they learned to choose the more numerous array and could differentiate between arrays of five and seven flowers. These data support the presence of an approximate number system in the rufous hummingbird. It seems plausible that having such a system would enable much more efficient foraging in this species.

Numerical ordinality in a wild nectarivore.

Ordinality is a numerical property that nectarivores may use to remember the specific order in which to visit a sequence of flowers, a foraging strategy also known as traplining. In this experiment, we tested whether wild, free-living rufous hummingbirds (Selasphorus rufus) could use ordinality to visit a rewarded flower. Birds were presented with a series of linear arrays of 10 artificial flowers; only one flower in each array was rewarded with sucrose solution. During training, birds learned to locate the correct flower independent of absolute spatial location. The birds' accuracy was independent of the rewarded ordinal position (1st, 2nd, 3rd or 4th), which suggests that they used an object-indexing mechanism of numerical processing, rather than a magnitude-based system. When distance cues between flowers were made irrelevant during test trials, birds could still locate the correct flower. The distribution of errors during both training and testing indicates that the birds may have used a so-called working up strategy to locate the correct ordinal position. These results provide the first demonstration of numerical ordinal abilities in a wild vertebrate and suggest that such abilities could be used during foraging in the wild.

Effects of landmark distance and stability on accuracy of reward relocation.

Although small-scale navigation is well studied in a wide range of species, much of what is known about landmark use by vertebrates is based on laboratory experiments. To investigate how vertebrates in the wild use landmarks, we trained wild male rufous hummingbirds to feed from a flower that was placed in a constant spatial relationship with two artificial landmarks. In the first experiment, the landmarks and flower were 0.25, 0.5 or 1 m apart and we always moved them 3-4 m after each visit by the bird. In the second experiment, the landmarks and flower were always 0.25 m apart and we moved them either 1 or 0.25 m between trials. In tests, in which we removed the flower, the hummingbirds stopped closer to the predicted flower location when the landmarks had been closer to the flower during training. However, while the distance that the birds stopped from the landmarks and predicted flower location was unaffected by the distance that the landmarks moved between trials, the birds directed their search nearer to the predicted direction of the flower, relative to the landmarks, when the landmarks and flower were more stable in the environment. In the field, then, landmarks alone were sufficient for the birds to determine the distance of a reward but not its direction.

Three-dimensional space: locomotory style explains memory differences in rats and hummingbirds.

While most animals live in a three-dimensional world, they move through it to different extents depending on their mode of locomotion: terrestrial animals move vertically less than do swimming and flying animals. As nearly everything we know about how animals learn and remember locations in space comes from two-dimensional experiments in the horizontal plane, here we determined whether the use of three-dimensional space by a terrestrial and a flying animal was correlated with memory for a rewarded location. In the cubic mazes in which we trained and tested rats and hummingbirds, rats moved more vertically than horizontally, whereas hummingbirds moved equally in the three dimensions. Consistent with their movement preferences, rats were more accurate in relocating the horizontal component of a rewarded location than they were in the vertical component. Hummingbirds, however, were more accurate in the vertical dimension than they were in the horizontal, a result that cannot be explained by their use of space. Either as a result of evolution or ontogeny, it appears that birds and rats prioritize horizontal versus vertical components differently when they remember three-dimensional space.

Wild hummingbirds rely on landmarks not geometry when learning an array of flowers.

Rats, birds or fish trained to find a reward in one corner of a small enclosure tend to learn the location of the reward using both nearby visual features and the geometric relationships of corners and walls. Because these studies are conducted under laboratory and thereby unnatural conditions, we sought to determine whether wild, free-living rufous hummingbirds (Selasphorus rufus) learning a single reward location within a rectangular array of flowers would similarly employ both nearby visual landmarks and the geometric relationships of the array. Once subjects had learned the location of the reward, we used test probes in which one or two experimental landmarks were moved or removed in order to reveal how the birds remembered the reward location. The hummingbirds showed no evidence that they used the geometry of the rectangular array of flowers to remember the reward. Rather, they used our experimental landmarks, and possibly nearby, natural landmarks, to orient and navigate to the reward. We believe this to be the first test of the use of rectangular geometry by wild animals, and we recommend further studies be conducted in ecologically relevant conditions in order to help determine how and when animals form complex geometric representations of their local environments.

The function of episodic memory in animals.

The best-known example of episodic memory in animals came from food-storing birds. One of the beauties of the food-storing system was that inherent in the behaviour were the elements that (at the time) made up episodic memory: what, where and when. While there were then already plenty of data on animals' ability to put together what and where, the addition of the time element in animals' memory and its testing was one that was both new and experimentally challenging. It has, however, led to an increasing variety of examples showing that animals can put together all three informational components. If episodic memories can be described as those memories that make any one of us who we are, why should non-human animals have such memories? Here, we argue that episodic memories play a significant functional role in the lives of real animals, in particular, enabling them to make decisions about how they might or should act in their future. We support our argument with data from a range of examples, focussing on data from the field.This article is part of the theme issue 'Elements of episodic memory: lessons from 40 years of research'.

What, where and when: deconstructing memory.

The ability of animals to remember the what, where and when of a unique past event is used as an animal equivalent to human episodic memory. We currently view episodic memory as reconstructive, with an event being remembered in the context in which it took place. Importantly, this means that the components of a what, where, when memory task should be dissociable (e.g. what would be remembered to a different degree than when). We tested this hypothesis by training hummingbirds to a memory task, where the location of a reward was specified according to colour (what), location (where), and order and time of day (when). Although hummingbirds remembered these three pieces of information together more often than expected, there was a hierarchy as to how they were remembered. When seemed to be the hardest to remember, while errors relating to what were more easily corrected. Furthermore, when appears to have been encoded as a combination of time of day and sequence information. As hummingbirds solved this task using reconstruction of different memory components (what, where and when), we suggest that similar deconstructive approaches may offer a useful way to compare episodic and episodic-like memories.

One-trial spatial learning: wild hummingbirds relocate a reward after a single visit.

Beaconing to rewarded locations is typically achieved by visual recognition of the actual goal. Spatial recognition, on the other hand, can occur in the absence of the goal itself, relying instead on the landmarks surrounding the goal location. Although the duration or frequency of experiences that an animal needs to learn the landmarks surrounding a goal have been extensively studied with a variety of laboratory tasks, little is known about the way in which wild vertebrates use them in their natural environment. Here, we allowed hummingbirds to feed once only from a rewarding flower (goal) before it was removed. When we presented a similar flower at a different height in another location, birds frequently returned to the location the flower had previously occupied (spatial recognition) before flying to the flower itself (beaconing). After experiencing three rewarded flowers, each in a different location, they were more likely to beacon to the current visible flower than they were to return to previously rewarded locations (without a visible flower). These data show that hummingbirds can encode a rewarded location on the basis of the surrounding landmarks after a single visit. After multiple goal location manipulations, however, the birds changed their strategy to beaconing presumably because they had learned that the flower itself reliably signalled reward.

Do rufous hummingbirds (Selasphorus rufus) use visual beacons?

Animals are often assumed to use highly conspicuous features of a goal to head directly to that goal ('beaconing'). In the field it is generally assumed that flowers serve as beacons to guide pollinators. Artificial hummingbird feeders are coloured red to serve a similar function. However, anecdotal reports suggest that hummingbirds return to feeder locations in the absence of the feeder (and thus the beacon). Here we test these reports for the first time in the field, using the natural territories of hummingbirds and manipulating flowers on a scale that is ecologically relevant to the birds. We compared the predictions from two distinct hypotheses as to how hummingbirds might use the visual features of rewards: the distant beacon hypothesis and the local cue hypothesis. In two field experiments, we found no evidence that rufous hummingbirds used a distant visual beacon to guide them to a rewarded location. In no case did birds abandon their approach to the goal location from a distance; rather they demonstrated remarkable accuracy of navigation by approaching to within about 70 cm of a rewarded flower's original location. Proximity varied depending on the size of the training flower: birds flew closer to a previously rewarded location if it had been previously signalled with a small beacon. Additionally, when provided with a beacon at a new location, birds did not fly directly to the new beacon. Taken together, we believe these data demonstrate that these hummingbirds depend little on visual characteristics to beacon to rewarded locations, but rather that they encode surrounding landmarks in order to reach the goal and then use the visual features of the goal as confirmation that they have arrived at the correct location.

Timing in free-living rufous hummingbirds, Selasphorus rufus.

Animals organize their lives around circannual and circadian rhythms, but little is known of their use of much shorter intervals. In the laboratory, some animals can learn the specific duration (seconds or minutes) between periods of food access. It has been supposed that wild nectarivores, such as hummingbirds, might also learn short time intervals so as to avoid revisiting emptied flowers until the nectar has been replenished. We provided free-living, territorial rufous hummingbirds each with eight artificial flowers containing sucrose solution. Four flowers were refilled 10 min after the bird emptied them, and the other four were refilled 20 min after being emptied. Throughout the day, birds revisited the 10 min flowers significantly sooner than they revisited the 20 min flowers, and return visits to the flowers matched their refill schedules. Hummingbirds remembered the locations and timing of eight rewards, updating this information throughout the day. Not only is this the first time that this degree of timing ability has been shown in wild animals, but these hummingbirds also exhibit two of the fundamental aspects of episodic-like memory (where and when), the kind of memory for specific events often thought to be exclusive to humans.

Wild hummingbirds can use the geometry of a flower array.

Animals use cues from their environment to orient in space and to navigate their surroundings. Geometry is a cue whose informational content may originate from the metric properties of a given environment, and its use has been demonstrated in the laboratory in nearly every species of animal tested. However, it is not clear whether geometric information, used by animals typically tested in small, rectangular boxes, is directly relevant to animals in their natural environment. Here we present the first data that confirm the use of geometric cues by a free-living animal in the wild. We trained rufous hummingbirds to visit a rectangular array of four artificial flowers, one of which was rewarded. In some trials a conspicuous landmark cued the reward. Following array translocation and rotation, we presented hummingbirds with three tests. When trained and tested with the landmark, or when trained and tested without it, hummingbirds failed to show geometric learning. However, when trained with a landmark but tested without it, hummingbirds produced the classic geometric response, showing that they had learned the geometric relationships (distance and direction) of several non-reward visual elements of the environment. While it remains that the use of geometry to relocate a reward may be an experimental artefact, its use is not confined to the laboratory.

Why study cognition in the wild (and how to test it)?

An animal's behavior is affected by its cognitive abilities, which are, in turn, a consequence of the environment in which an animal has evolved and developed. Although behavioral ecologists have been studying animals in their natural environment for several decades, over much the same period animal cognition has been studied almost exclusively in the laboratory. Traditionally, the study of animal cognition has been based on well-established paradigms used to investigate well-defined cognitive processes. This allows identification of what animals can do, but may not, however, always reflect what animals actually do in the wild. As both ecologists and some psychologists increasingly try to explain behaviors observable only in wild animals, we review the different motivations and methodologies used to study cognition in the wild and identify some of the challenges that accompany the combination of a naturalistic approach together with typical psychological testing paradigms. We think that studying animal cognition in the wild is likely to be most productive when the questions addressed correspond to the species' ecology and when laboratory cognitive tests are appropriately adapted for use in the field. Furthermore, recent methodological and technological advances will likely allow significant expansion of the species and questions that can be addressed in the wild.

Assessment of health in human faces is context-dependent.

When making decisions between options, humans are expected to choose the option that returns the highest benefit. In practice, however, adding inferior alternatives to the choice set can alter these decisions. Here we investigated whether decisions over the facial features that people find healthy looking can also be affected by the context in which they see those faces. To do this we examined the effect of choice set on the perception of health of images of faces of light-skinned Caucasian females. We manipulated apparent facial health by changing yellowness of the skin: the healthy faces were moderately yellow and the less healthy faces were either much more yellow or much less yellow. In each experiment, two healthy faces were presented along with a third, less healthy face. When the third face was much more yellow, participants chose the more yellow of the two healthy faces more often as the most healthy. However, when the third face was the least yellow, participants chose the less yellow of the two healthy faces more often. A further experiment confirmed that this result is not due to a generalised preference for an intermediate option. These results extend our understanding of context-dependent decision-making in humans, and suggest that comparative evaluation may be a common feature across many different kinds of choices that humans have to make.

Context-dependent foraging decisions in rufous hummingbirds.

A core assumption implicit in economic models of animal choice is that subjects assign absolute utilities to options that are independent of the type and number of alternatives available. Humans sometimes appear to violate this assumption and employ relative, as opposed to absolute, currencies when making choices. Recent evidence suggests that animals too might sometimes employ relative choice mechanisms. We tested this idea by measuring the foraging preferences of rufous hummingbirds (Selasphorus rufus) faced with choices analogous to those in which human use of relative currencies is evident. The birds experienced three treatments: a binary choice between two artificial flower types designated concentration (20 microl, 40% sucrose solution) and volume (40 microl, 20%), and two trinary treatments in which a third decoy option (either concentration decoy: 10 microl, 30% or volume decoy: 30 microl, 10%) was added to the set. The birds' preferences differed significantly across the three treatments. In the trinary treatments, the effect of the decoy options was to increase the preference for the option that dominated the decoy. These results are similar to those reported in the human choice literature, and are compatible with the hummingbirds using a relative evaluation mechanism in decision making.

Cue learning by rufous hummingbirds (Selasphorus rufus).

The authors investigated the use by wild-living rufous hummingbirds (Selasphorus rufus) of flower color pattern and flower position for remembering rewarded flowers. Birds were presented with arrays of artificial flowers, a proportion of which was rewarded. Once the locations were learned by the birds, the array was moved 2 m, and flower color pattern and/or rewarded positions were manipulated. The birds' ability to learn which were the rewarded flowers in this 2nd array was much more strongly affected by whether the rewarded flowers occupied the same positions as in the 1st array than by their color patterns.

Colour cues facilitate learning flower refill schedules in wild hummingbirds.

Free-living hummingbirds can learn the refill schedules of individual experimental flowers but little is known about what information they use to do this. Colour cues, in particular, may be important to hummingbirds when learning about rewarded flower properties. We investigated, therefore, whether colour cues facilitated the learning of flower refill schedules in wild, free-living rufous hummingbirds (Selasphorus rufus). In the Cued condition, we presented birds with an array of six flowers, three of one colour, each of which were refilled 10min after being emptied by the bird and three of a different colour, which were refilled 20min after being emptied. In the Uncued condition we presented birds with six flowers of the same colour, three of which were refilled after 10min and three of which were refilled after 20min as for the birds in the Cued condition. In the second part of the experiment, we moved the array 2m and changed the shape of the array. Across both phases, birds in the Cued condition learned to discriminate between 10 and 20-min flowers more quickly than did the birds in the Uncued condition. The Cued birds were also better at discriminating between the two distinct refill intervals. Colour cues can, therefore, facilitate learning the refill schedules of experimental flowers in these birds. This article is part of a Special Issue entitled: Cognition in the wild.

Individual differences in decision making by foraging hummingbirds.

For both humans and animals preference for one option over others can be influenced by the context in which the options occur. In animals, changes in preference could be due to comparative decision-making or to changes in the energy state of the animal when making decisions. We investigated which of these possibilities better explained the response of wild hummingbirds to the addition of a decoy option to a set of two options by presenting Rufous hummingbirds (Selasphorus rufus) with a foraging experiment with two treatments. In each treatment the birds were presented with a binary choice between two options and a trinary choice with three options. In treatment one the binary choice was between a volume option and a concentration option, whereas in treatment two the same volume option was presented alongside an alternative concentration option. In the trinary choice, birds were presented with the same options as in the binary choice plus one of two inferior options. Birds changed their preferences when a poorer option was added to the choice set: birds increased their preference for the same option when in the presence of either decoy. Which option differed across individuals and the changes in preference were not readily explained by either energy maximisation or the decoy effect. The consistency in response within individuals, however, would suggest that the individual itself brings an extra dimension to context-dependent decision-making. This article is part of a Special Issue entitled: Cognition in the wild.