Responses to novelty in wild insular birds: comparing breeding populations in ecologically contrasting habitats.

Islands have always provided ideal natural laboratories for assessing ecological parameters influencing behaviour. One hypothesis that lends itself well to testing in island habitats suggests that animals frequenting highly variable environments should be motivated to approach and interact with (i.e. explore) novelty. Intra-species comparisons of populations living in ecologically different island habitats may, thus, help reveal the factors that modulate animals' responses to novelty. In this study, we presented novel objects to two geographically isolated breeding populations of the black-faced sheathbill (Chionis minor), a sedentary land-based bird that frequents remote sub-Antarctic islands. In the first population (Chionis minor ssp. crozettensis), the "Crozet group" (Baie du Marin, Ile de la Possession, Crozet Islands), breeding pairs inhabit a variable habitat close to penguin (Aptenodytes patagonicus) colonies. In the second population (Chionis minor ssp. minor), the "Kerguelen group" (île Verte, Morbihan gulf, Kerguelen Islands) breeding pairs live in penguin-free territories. In this latter population, the environment is less variable due to the presence of a broad intertidal zone which ensures year-round food availability. At both Kerguelen and Crozet, at least one breeding partner in all pairs approached at least one of the novel objects, and we found no significant differences in the latency of approach between the two populations. However, sheathbills at Crozet touched objects significantly more than birds at Kerguelen, and were also faster to touch them. We discuss how environmental variability, along with other potential influencing factors, may favour exploration of novelty in this wild insular bird.

Remote islands as natural laboratories: human-food association increases attraction to humans and novelty exploration in a seabird.

Increased attraction to humans and their objects often arises after repeated and positive human-wildlife encounters (e.g. food provided in tourist settings). The causes of this 'over-attraction', which may result from a learned association between humans and food, are still poorly studied in wild animals. Understanding the influence of humans on animals' responses is yet crucial to prevent negative effects (e.g. aggression). We presented three novel objects to two groups of free-ranging brown skuas (Catharacta antarctica ssp. lonnbergi) in the remote sub-Antarctic, where their habitats show no or minimal human disturbance. Skuas in one group (Verte) had previously participated in repeated food-rewarded behavioural and cognitive tasks with a human experimenter; skuas in the other group (Ratmanoff) had never done so. Objects consisted of (i) one natural-food-resembling object (plastic fish), (ii) one anthropogenic food object (real cake slice), and (iii) one anthropogenic non-food object (yellow glove). Verte group skuas approached the human experimenter and pecked significantly more and sooner at novel objects. Human-food association may have thus resulted in increased attraction to humans and novelty exploration in previously naive brown skuas, making this species a useful model for investigating the consequences of experience with humans on wildlife behaviour.

Wild skuas can follow human-given behavioural cues when objects resemble natural food.

The capacity to follow human cues provides animals with information about the environment and can hence offer obvious adaptive benefits. Most studies carried out so far, however, have been on captive animals with previous experience with humans. Further comparative investigation is needed to properly assess the factors driving the emergence of this capacity under natural conditions, especially in species that do not have longstanding interactions with humans. Wild brown skuas (Catharacta antarctica ssp. lonnbergi) are non-neophobic seabirds that live in human-free habitats. In test 1, we assessed this species' capacity to use human behavioural cues (i.e., pecking at the same object previously picked up and lifted by a human experimenter) when the items presented were food objects: anthropogenic objects (wrapped muffins) and natural-food-resembling objects (plaster eggs). In test 2, we examined the response of another skua population towards non-food objects (sponges). Although all skuas in test 1 pecked at the objects, they pecked significantly more at the same previously handled items when they resembled natural food (plaster eggs). Most skuas in test 2, however, did not approach or peck at the non-food objects presented. Our results lead us to suggest that the use of human behavioural cues may be influenced by skuas' foraging ecology, which paves the way to further field studies assessing whether this capacity is directed specifically towards food objects and/or develops after previous interaction with humans.

Evidence of tool use in a seabird.

Documenting novel cases of tool use in wild animals can inform our understanding of the evolutionary drivers of the behavior's emergence in the natural world. We describe a previously unknown tool-use behavior for wild birds, so far only documented in the wild in primates and elephants. We observed 2 Atlantic puffins at their breeding colonies, one in Wales and the other in Iceland (the latter captured on camera), spontaneously using a small wooden stick to scratch their bodies. The importance of these observations is 3-fold. First, while to date only a single form of body-care-related tool use has been recorded in wild birds (anting), our finding shows that the wild avian tool-use repertoire is wider than previously thought and extends to contexts other than food extraction. Second, we expand the taxonomic breadth of tool use to include another group of birds, seabirds, and a different suborder (Lari). Third, our independent observations span a distance of more than 1,700 km, suggesting that occasional tool use may be widespread in this group, and that seabirds' physical cognition may have been underestimated.

Birds invest wingbeats to keep a steady head and reap the ultimate benefits of flying together.

Flapping flight is the most energetically demanding form of sustained forwards locomotion that vertebrates perform. Flock dynamics therefore have significant implications for energy expenditure. Despite this, no studies have quantified the biomechanical consequences of flying in a cluster flock or pair relative to flying solo. Here, we compared the flight characteristics of homing pigeons (Columba livia) flying solo and in pairs released from a site 7 km from home, using high-precision 5 Hz global positioning system (GPS) and 200 Hz tri-axial accelerometer bio-loggers. As expected, paired individuals benefitted from improved homing route accuracy, which reduced flight distance by 7% and time by 9%. However, realising these navigational gains involved substantial changes in flight kinematics and energetics. Both individuals in a pair increased their wingbeat frequency by 18% by decreasing the duration of their upstroke. This sharp increase in wingbeat frequency caused just a 3% increase in airspeed but reduced the oscillatory displacement of the body by 22%, which we hypothesise relates to an increased requirement for visual stability and manoeuvrability when flying in a flock or pair. The combination of the increase in airspeed and a higher wingbeat frequency would result in a minimum 2.2% increase in the total aerodynamic power requirements if the wingbeats were fully optimised. Overall, the enhanced navigational performance will offset any additional energetic costs as long as the metabolic power requirements are not increased above 9%. Our results demonstrate that the increases in wingbeat frequency when flying together have previously been underestimated by an order of magnitude and force reinterpretation of their mechanistic origin. We show that, for pigeons flying in pairs, two heads are better than one but keeping a steady head necessitates energetically costly kinematics.

Wild skuas can use acoustic cues to locate hidden food.

Among animals, the visual acuity of several predatory bird species is probably the most outstanding. This, and the ease with which visually based tasks are administered, has led researchers to predominantly use the visual modality when studying avian cognition. Some wild skua populations routinely use acoustic cues emitted by their prey during foraging. In this study, we thus assessed whether this species was able to locate hidden food using acoustic cues alone (training phase). During the subsequent test phase, we investigated the capacity of successful individuals to choose the correct baited container in four conditions: (i) baited (shaking the baited container), (ii) full information (shaking both containers), (iii) exclusion (shaking the empty container), and (iv) control (shaking neither container). Four out of ten subjects succeeded in locating the baited container in the training phase. During the test phase, most subjects chose the baited container significantly more than the empty container in the baited and full information condition, while their performance was at chance level in the control condition. When no sound emanated from the empty container in the exclusion condition, one out of four skuas chose the baited container with more accuracy than predicted by chance. As this bird chose correctly on the first trial and during the first five trials, its performance is unlikely due to learning processes (learning to exclude the empty container). Although further tests are necessary to draw firm conclusions, our results open the way for assessing further this species' reasoning abilities in the wild.

Pigeons retain partial memories of homing paths years after learning them individually, collectively or culturally.

Memory of past experience is central to many animal decisions, but how long specific memories can influence behaviour is poorly understood. Few studies have reported memories retrieved after several years in non-human animals, especially for spatial tasks, and whether the social context during learning could affect long-term memory retention. We investigated homing pigeons' spatial memory by GPS-recording their homing paths from a site 9 km from their loft. We compared solo flights of naive pigeons with those of pigeons that had last homed from this site 3-4 years earlier, having learnt a homing route either alone (individual learning), together with a naive partner (collective learning) or within cultural transmission chains (cultural learning). We used as a control a second release site unfamiliar to all pigeons. Pigeons from all learning treatments outperformed naive birds at the familiar (but not the unfamiliar) site, but the idiosyncratic routes they formerly used several years before were now partially forgotten. Our results show that non-human animals can use their memory to solve a spatial task years after they last performed it, irrespective of the social context during learning. They also suggest that without reinforcement, landmarks and culturally acquired 'route traditions' are gradually forgotten.

A missing piece of the Papio puzzle: Gorongosa baboon phenostructure and intrageneric relationships.

Most authors recognize six baboon species: hamadryas (Papio hamadryas), Guinea (Papio papio), olive (Papio anubis), yellow (Papio cynocephalus), chacma (Papio ursinus), and Kinda (Papio kindae). However, there is still debate regarding the taxonomic status, phylogenetic relationships, and the amount of gene flow occurring between species. Here, we present ongoing research on baboon morphological diversity in Gorongosa National Park (GNP), located in central Mozambique, south of the Zambezi River, at the southern end of the East African Rift System. The park exhibits outstanding ecological diversity and hosts more than 200 baboon troops. Gorongosa National Park baboons have previously been classified as chacma baboons (P. ursinus). In accordance with this, two mtDNA samples from the park have been placed in the same mtDNA clade as the northern chacma baboons. However, GNP baboons exhibit morphological features common in yellow baboons (e.g., yellow fur color), suggesting that parapatric gene flow between chacma and yellow baboons might have occurred in the past or could be ongoing. We investigated the phenostructure of the Gorongosa baboons using two approaches: 1) description of external phenotypic features, such as coloration and body size, and 2) 3D geometric morphometric analysis of 43 craniofacial landmarks on 11 specimens from Gorongosa compared to a pan-African sample of 352 baboons. The results show that Gorongosa baboons exhibit a mosaic of features shared with southern P. cynocephalus and P. ursinus griseipes. The GNP baboon phenotype fits within a geographic clinal pattern of replacing allotaxa. We put forward the hypothesis of either past and/or ongoing hybridization between the gray-footed chacma and southern yellow baboons in Gorongosa or an isolation-by-distance scenario in which the GNP baboons are geographically and morphologically intermediate. These two scenarios are not mutually exclusive. We highlight the potential of baboons as a useful model to understand speciation and hybridization in early human evolution.

Head-mounted sensors reveal visual attention of free-flying homing pigeons.

Gaze behavior offers valuable insights into attention and cognition. However, technological limitations have prevented the examination of animals' gaze behavior in natural, information-rich contexts; for example, during navigation through complex environments. Therefore, we developed a lightweight custom-made logger equipped with an inertial measurement unit (IMU) and GPS to simultaneously track the head movements and flight trajectories of free-flying homing pigeons. Pigeons have a limited range of eye movement, and their eye moves in coordination with their head in a saccadic manner (similar to primate eye saccades). This allows head movement to act as a proxy for visual scanning behavior. Our IMU sensor recorded the 3D movement of the birds' heads in high resolution, allowing us to reliably detect distinct saccade signals. The birds moved their head far more than necessary for maneuvering flight, suggesting that they actively scanned the environment. This movement was predominantly horizontal (yaw) and sideways (roll), allowing them to scan the environment with their lateral visual field. They decreased their head movement when they flew solo over prominent landmarks (major roads and a railway line) and also when they flew in pairs (especially when flying side by side, with the partner maintained in their lateral visual field). Thus, a decrease in head movement indicates a change in birds' focus of attention. We conclude that pigeons use their head gaze in a task-related manner and that tracking flying birds' head movement is a promising method for examining their visual attention during natural tasks.

Wild birds respond to flockmate loss by increasing their social network associations to others.

Understanding the consequences of losing individuals from wild populations is a current and pressing issue, yet how such loss influences the social behaviour of the remaining animals is largely unexplored. Through combining the automated tracking of winter flocks of over 500 wild great tits (Parus major) with removal experiments, we assessed how individuals' social network positions responded to the loss of their social associates. We found that the extent of flockmate loss that individuals experienced correlated positively with subsequent increases in the number of their social associations, the average strength of their bonds and their overall connectedness within the social network (defined as summed edge weights). Increased social connectivity was not driven by general disturbance or changes in foraging behaviour, but by modifications to fine-scale social network connections in response to losing their associates. Therefore, the reduction in social connectedness expected by individual loss may be mitigated by increases in social associations between remaining individuals. Given that these findings demonstrate rapid adjustment of social network associations in response to the loss of previous social ties, future research should examine the generality of the compensatory adjustment of social relations in ways that maintain the structure of social organization.

Homing pigeons (Columba livia) modulate wingbeat characteristics as a function of route familiarity.

Mechanisms of avian navigation have received considerable attention, but whether different navigational strategies are accompanied by different flight characteristics is unknown. Managing energy expenditure is critical for survival; therefore, understanding how flight characteristics, and hence energy allocation, potentially change with birds' familiarity with a navigational task could provide key insights into the costs of orientation. We addressed this question by examining changes in the wingbeat characteristics and airspeed of homing pigeons (Columba livia) as they learned a homing task. Twenty-one pigeons were released 20 times individually either 3.85 or 7.06 km from home. Birds were equipped with 5 Hz GPS trackers and 200 Hz tri-axial accelerometers. We found that, as the birds' route efficiency increased during the first six releases, their median peak-to-peak dorsal body (DB) acceleration and median DB amplitude also increased. This, in turn, led to higher airspeeds, suggesting that birds fly slower when traversing unfamiliar terrain. By contrast, after route efficiency stabilised, birds exhibited increasing wingbeat frequencies, which did not result in further increases in speed. Overall, higher wind support was also associated with lower wingbeat frequencies and increased DB amplitude. Our study suggests that the cost of early flights from an unfamiliar location may be higher than subsequent flights because of both inefficient routes (increased distance) and lower airspeeds (increased time). Furthermore, the results indicate, for the first time, that birds modulate their wingbeat characteristics as a function of navigational knowledge, and suggest that flight characteristics may be used as 'signatures' of birds' route familiarity.

Misinformed leaders lose influence over pigeon flocks.

In animal groups where certain individuals have disproportionate influence over collective decisions, the whole group's performance may suffer if these individuals possess inaccurate information. Whether in such situations leaders can be replaced in their roles by better-informed group mates represents an important question in understanding the adaptive consequences of collective decision-making. Here, we use a clock-shifting procedure to predictably manipulate the directional error in navigational information possessed by established leaders within hierarchically structured flocks of homing pigeons (Columba livia). We demonstrate that in the majority of cases when leaders hold inaccurate information they lose their influence over the flock. In these cases, inaccurate information is filtered out through the rearrangement of hierarchical positions, preventing errors by former leaders from propagating down the hierarchy. Our study demonstrates that flexible decision-making structures can be valuable in situations where 'bad' information is introduced by otherwise influential individuals.

Hierarchical group dynamics in pigeon flocks.

Animals that travel together in groups display a variety of fascinating motion patterns thought to be the result of delicate local interactions among group members. Although the most informative way of investigating and interpreting collective movement phenomena would be afforded by the collection of high-resolution spatiotemporal data from moving individuals, such data are scarce and are virtually non-existent for long-distance group motion within a natural setting because of the associated technological difficulties. Here we present results of experiments in which track logs of homing pigeons flying in flocks of up to 10 individuals have been obtained by high-resolution lightweight GPS devices and analysed using a variety of correlation functions inspired by approaches common in statistical physics. We find a well-defined hierarchy among flock members from data concerning leading roles in pairwise interactions, defined on the basis of characteristic delay times between birds' directional choices. The average spatial position of a pigeon within the flock strongly correlates with its place in the hierarchy, and birds respond more quickly to conspecifics perceived primarily through the left eye-both results revealing differential roles for birds that assume different positions with respect to flock-mates. From an evolutionary perspective, our results suggest that hierarchical organization of group flight may be more efficient than an egalitarian one, at least for those flock sizes that permit regular pairwise interactions among group members, during which leader-follower relationships are consistently manifested.

Context-dependent hierarchies in pigeons.

Hierarchical organization is widespread in the societies of humans and other animals, both in social structure and in decision-making contexts. In the case of collective motion, the majority of case studies report that dominant individuals lead group movements, in agreement with the common conflation of the terms "dominance" and "leadership." From a theoretical perspective, if social relationships influence interactions during collective motion, then social structure could also affect leadership in large, swarm-like groups, such as fish shoals and bird flocks. Here we use computer-vision-based methods and miniature GPS tracking to study, respectively, social dominance and in-flight leader-follower relations in pigeons. In both types of behavior we find hierarchically structured networks of directed interactions. However, instead of being conflated, dominance and leadership hierarchies are completely independent of each other. Although dominance is an important aspect of variation among pigeons, correlated with aggression and access to food, our results imply that the stable leadership hierarchies in the air must be based on a different set of individual competences. In addition to confirming the existence of independent and context-specific hierarchies in pigeons, we succeed in setting out a robust, scalable method for the automated analysis of dominance relationships, and thus of social structure, applicable to many species. Our results, as well as our methods, will help to incorporate the broader context of animal social organization into the study of collective behavior.

Asymmetric visual input and route recapitulation in homing pigeons.

Pigeons (Columba livia) display reliable homing behaviour, but their homing routes from familiar release points are individually idiosyncratic and tightly recapitulated, suggesting that learning plays a role in route establishment. In light of the fact that routes are learned, and that both ascending and descending visual pathways share visual inputs from each eye asymmetrically to the brain hemispheres, we investigated how information from each eye contributes to route establishment, and how information input is shared between left and right neural systems. Using on-board global positioning system loggers, we tested 12 pigeons' route fidelity when switching from learning a route with one eye to homing with the other, and back, in an A-B-A design. Two groups of birds, trained first with the left or first with the right eye, formed new idiosyncratic routes after switching eyes, but those that flew first with the left eye formed these routes nearer to their original routes. This confirms that vision plays a major role in homing from familiar sites and exposes a behavioural consequence of neuroanatomical asymmetry whose ontogeny is better understood than its functional significance.

Route following and the pigeon's familiar area map.

Homing pigeons (Columba livia) have been the central model of avian navigation research for many decades, but only more recently has research extended into understanding their mechanisms of orientation in the familiar area. The discovery (facilitated by GPS tracking) that pigeons gradually acquire with experience individually idiosyncratic routes home to which they remain faithful on repeated releases, even if displaced off-route, has helped uncover the fundamental role of familiar visual landmarks in the avian familiar area map. We evaluate the robustness and generality of the route-following phenomenon by examining extant studies in depth, including the single published counter-example, providing a detailed comparison of route efficiencies, flight corridor widths and fidelity. We combine this analysis with a review of inferences that can be drawn from other experimental approaches to understanding the nature of familiar area orientation in pigeons, including experiments on landmark recognition, and response to clock-shift, to build the first detailed picture of how bird orientation develops with experience of the familiar area. We articulate alternative hypotheses for how guidance might be controlled during route following, concluding that although much remains unknown, the details of route following strongly support a pilotage interpretation. Predictable patterns of efficiency increase, but limited to the local route, typical corridor widths of 100-200 m, high-fidelity pinch-points on route, attraction to landscape edges, and a robustness to clock-shift procedures, all demonstrate that birds can associatively acquire a map of their familiar area guided (at least partially) by direct visual control from memorised local landscape features.

Learning multiple routes in homing pigeons.

The aerial lifestyle of central-place foraging birds allows wide-ranging movements, raising fundamental questions about their remarkable navigation and memory systems. For example, we know that pigeons (Columba livia), long-standing models for avian navigation, rely on individually distinct routes when homing from familiar sites. But it remains unknown how they cope with the task of learning several routes in parallel. Here, we examined how learning multiple routes influences homing in pigeons. We subjected groups of pigeons to different training protocols, defined by the sequence in which they were repeatedly released from three different sites, either sequentially, in rotation or randomly. We observed that pigeons from all groups successfully developed and applied memories of the different release sites (RSs), irrespective of the training protocol, and that learning several routes in parallel did not impair their capacity to quickly improve their homing efficiency over multiple releases. Our data also indicated that they coped with increasing RS uncertainty by adjusting both their initial behaviour upon release and subsequent homing efficiency. The results of our study broaden our understanding of avian route following and open new possibilities for studying learning and memory in free-flying animals.

Landscape complexity influences route-memory formation in navigating pigeons.

Observations of the flight paths of pigeons navigating from familiar locations have shown that these birds are able to learn and subsequently follow habitual routes home. It has been suggested that navigation along these routes is based on the recognition of memorized visual landmarks. Previous research has identified the effect of landmarks on flight path structure, and thus the locations of potentially salient sites. Pigeons have also been observed to be particularly attracted to strong linear features in the landscape, such as roads and rivers. However, a more general understanding of the specific characteristics of the landscape that facilitate route learning has remained out of reach. In this study, we identify landscape complexity as a key predictor of the fidelity to the habitual route, and thus conclude that pigeons form route memories most strongly in regions where the landscape complexity is neither too great nor too low. Our results imply that pigeons process their visual environment on a characteristic spatial scale while navigating and can explain the different degrees of success in reproducing route learning in different geographical locations.

The Arena System: a novel shared touch-panel apparatus for the study of chimpanzee social interaction and cognition.

We report on the development of a novel shared touch-panel apparatus for examining a diverse range of topics in great ape social cognition and interaction. Our apparatus-named the Arena System-is composed of a single multitouch monitor that spans across two separate testing booths, so that individuals situated in each booth have tactile access to half of the monitor and visual access to the whole monitor. Additional components of the system include a smart-film barrier able to restrict visual access between the booths, as well as two automated feeding devices that dispense food rewards to the subjects. The touch-panel, smart-film, and feeders are controlled by a PC that is also responsible for running the experimental tasks. We present data from a pilot behavioral game theory study with two chimpanzees in order to illustrate the efficacy of our method, and we suggest applications for a range of topics including animal social learning, coordination, and behavioral economics. The system enables fully automated experimental procedures, which means that no human participation is needed to run the tasks. The novel use of a touch-panel in a social setting allows for a finer degree of data resolution than do the traditional experimental apparatuses used in prior studies on great ape social interaction.