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Dora Biro

    Dora Biro

    University of Oxford, Zoology, Department Member
    The field of collective animal behaviour examines how relatively simple, local interactions between individuals in groups combine to produce global-level outcomes. Existing mathematical models and empirical work have identified candidate... more
    The field of collective animal behaviour examines how relatively simple, local interactions between individuals in groups combine to produce global-level outcomes. Existing mathematical models and empirical work have identified candidate mechanisms for numerous collective phenomena but have typically focused on one-off or short-term performance. We argue that feedback between collective performance and learning – giving the former the capacity to become an adaptive, and potentially cumulative, process – is a currently poorly explored but crucial mechanism in understanding collective systems. We synthesise material ranging from swarm intelligence in social insects through collective movements in vertebrates to collective decision making in animal and human groups, to propose avenues for future research to identify the potential for changes in these systems to accumulate over time. What Are Collective Behaviours and How Do They Arise? Some of the most impressive biological phenomena emerge out of interactions among members of animal groups. Bird flocks, fish schools, and insect swarms perform highly coordinated collective movements that can encompass thousands of individuals, producing complex group-level patterns that are difficult to predict from the behaviour of isolated individuals only. Animal groups are also able to solve problems that are beyond the capacities of single individuals [1]; ant colonies, for example, tackle certain types of optimisation problems so effectively that they have inspired an entire field of computer science [2]. Despite the appearance of synchronised organisation, it is increasingly well understood that no central control acts on the collective as a whole; instead, the global patterns result from simple, local interactions among the group's neighbouring members – a form of biological self-organisation [3] (see Glossary). Recent years have seen a proliferation of both empirical and theoretical work on the mechanistic underpinnings of collective animal behaviour [4], with self-organisation emerging as a major principle in various contexts including collective motion [5], decision making [6] and construction [7], activity synchronisation [8], and the spontaneous emergence of leader–follower relations [9]. Nonetheless, a rigorous adaptive framework is yet to be applied to collective animal behaviour; little is known about the nature of the selective forces that act at the level of the individual behavioural rules to shape pattern formation at group level. Over shorter timescales, and crucially for this review, no major synthesis has yet examined collective behaviour from a time–depth perspective; we do not know: (i) what changes group-level organisation might undergo over the course of repeated executions of collective tasks; (ii) to what extent solutions arrived at collectively are retained (learned), either at the individual or at the collective level, with the potential to influence future interactions; or (iii) what effect changes in group composition, due to natural demographic processes, have on whether solutions are 'inherited' from previous generations.
    Research Interests:
    The recognition of familiar areas by homing pigeons, Columba livia, is now known to depend at least in part on visual cues. Birds allowed a 5-min preview of the surrounding landscape prior to release home faster than those denied access... more
    The recognition of familiar areas by homing pigeons, Columba livia, is now known to depend at least in part on visual cues. Birds allowed a 5-min preview of the surrounding landscape prior to release home faster than those denied access to such cues, suggesting that ...
    Research Interests:
    Recent etho-archaeological studies of stone-tool use by wild chimpanzees have contributed valuable data towards elucidating the variables that influenced the emergence and development of the first lithic industries among Plio-Pleistocene... more
    Recent etho-archaeological studies of stone-tool use by wild chimpanzees have contributed valuable data towards elucidating the variables that influenced the emergence and development of the first lithic industries among Plio-Pleistocene hominins. Such data help to identify potential behaviours entailed in the first percussive technologies that are invisible in archaeological records. The long-term research site of Bossou in Guinea features a unique chimpanzee community whose members systematically use portable stones as hammers and anvils to crack open nuts in natural as well as in field experimental settings. Here we present the first analysis of repeated reuse of the same tool-composites in wild chimpanzees. Data collected over 5 years of experimental nut-cracking sessions at an “outdoor laboratory” site were assessed for the existence of systematic patterns in the selection of tool-composites, at group and at individual levels. Chimpanzees combined certain stones as hammer and anvil more often than expected by chance, even when taking into account preferences for individual stones by themselves. This may reflect an ability to recognise the nut-cracker as a single tool (composed of two elements, but functional only as a whole), as well as discrimination of tool quality-effectiveness. Through repeatedly combining the same pairs of stones—whether due to preferences for particular composites or for the two elements independently—tool-users may amplify use-wear traces and increase the likelihood of fracturing the stones, and thus of detaching pieces by battering.
    Field experiments can provide compelling demonstrations of social learning in wild populations. Social learning has been experimentally demonstrated in at least 23 field experiments, in 20 species, covering a range of contexts, such as... more
    Field experiments can provide compelling demonstrations of social learning in wild populations. Social learning has been experimentally demonstrated in at least 23 field experiments, in 20 species, covering a range of contexts, such as foraging preferences and techniques, habitat choice, and predator avoidance. We review experimental approaches taken in the field and with wild animals brought into captivity and note how these approaches can be extended. Relocating individuals, introducing trained individual demonstrators or novel behaviors into a population, or providing demonstrator-manipulated artifacts can establish whether and how a particular act can be socially transmitted in the wild and can help elucidate the benefits of social learning. The type, strength, and consistency of presented social information can be varied, and the provision of conditions favoring the performance of an act can both establish individual discovery rates and help determine whether social information is needed for acquisition. By blocking particular avenues of social transmission or removing key individuals, routes of transmission in wild populations can be investigated. Manipulation of conditions proposed to favor social learning can test mathematical models of the evolution of social learning. We illustrate how field experiments are a viable, vital, and informative approach to the study of social learning.
    Social animals have much to gain from observing and responding appropriately to the actions of their conspecific group members. This can in turn lead to the learning of novel behavior patterns (social learning) or to foraging, ranging, or... more
    Social animals have much to gain from observing and responding appropriately to the actions of their conspecific group members. This can in turn lead to the learning of novel behavior patterns (social learning) or to foraging, ranging, or social behavioral choices copied from fellow group members, which do not necessarily result in long-term learning, but at the time represent adaptive responses to environmental cues (public information use). In the current study, we developed a novel system for the study of public information use under fully automated conditions. We modified a classic single-subject laboratory paradigm—matching-to-sample (MTS)—and examined chimpanzees’ ability to interpret and utilize cues provided by the behavior of a conspecific to solve the task. In Experiment 1, two subjects took turns on an identity MTS task, with one subject (the model) performing the first half of the trial and the other subject (the observer) completing the trial using the model’s actions as discriminative cues. Both subjects performed above chance from the first session onwards. In Experiment 2, the subjects were tested on a symbolic version of the same MTS task, with one subject showing spontaneous transfer. Our study establishes a novel method for examining public information use within a highly controlled and automated setting.
    Chimpanzees (Pan troglodytes) are the most proficient and versatile users of tools in the wild. How such skills become integrated into the behavioural repertoire of wild chimpanzee communities is investigated here by drawing together... more
    Chimpanzees (Pan troglodytes) are the most proficient and versatile users of tools in the wild. How such skills become integrated into the behavioural repertoire of wild chimpanzee communities is investigated here by drawing together evidence from three complementary approaches in a group of oil-palm nut- (Elaeis guineensis) cracking chimpanzees at Bossou, Guinea. First, extensive surveys of communities adjacent to Bossou have shown that population-specific details of tool use, such as the selection of species of nuts as targets for cracking, cannot be explained purely on the basis of ecological differences. Second, a 16-year longitudinal record tracing the development of nut-cracking in individual chimpanzees has highlighted the importance of a critical period for learning (3–5 years of age), while the similar learning contexts experienced by siblings have been found to result in near-perfect (13 out of 14 dyads) inter-sibling correspondence in laterality. Third, novel data from field experiments involving the introduction of unfamiliar species of nuts to the Bossou group illuminates key aspects of both cultural innovation and transmission. We show that responses of individuals toward the novel items differ markedly with age, with juveniles being the most likely to explore. Furthermore, subjects are highly specific in their selection of conspecifics as models for observation, attending to the nut-cracking activities of individuals in the same age group or older, but not younger than themselves. Together with the phenomenon of inter-community migration, these results demonstrate a mechanism for the emergence of culture in wild chimpanzees.
    This chapter describes a series offield experiments aimed at investigating aspects ofemergence of cultural traditions in wild chimpanzee communities. Long-term research at a number ofsites in Africa has revealed that each community... more
    This chapter describes a series offield experiments aimed at investigating aspects ofemergence of cultural traditions in wild chimpanzee communities. Long-term research at a number ofsites in Africa has revealed that each community ofchim-panzees has developed its unique set ...
    An adult female chimpanzee with previous training in the use of Arabic numerals 1–9 was introduced to the meaning of "zero" in the context of three different numerical tasks. The first two were cardinal tasks where the subject was... more
    An adult female chimpanzee with previous training in the use of Arabic numerals 1–9 was introduced to the meaning of "zero" in the context of three different numerical tasks. The first two were cardinal tasks where the subject was required either to select numerals corresponding to the number of items presented on a computer screen (productive use of numerals) or to match sets of the appropriate size to numerals presented as samples (receptive use). The third task addressed the ordinal meaning of the same symbols where the subject was required to respond to numerals sequentially, arranging them into an ascending series. The subject mastered the recognition of the meaning of zero in all three tasks. However, details of her usage of the symbol revealed that transfer of the meaning between different kinds of tasks was incomplete, suggesting that the level of abstraction characteristic of human numerical ability was not attained in the chimpanzee. Over the course of acquisition leading to the high levels of accuracy eventually observed, the newly introduced zero appeared to shift along the length of a continuous numerical scale toward the lower end, while confusions with 1 remained the most frequently encountered mistakes. Such patterns of error thus suggest that Ai's understanding of the meaning of zero in relation to the rest of the number symbols was not consistent with an "absence of items versus presence of items" scheme.
    The recognition of familiar areas by homing pigeons, Columba livia, is now known to depend at least in part on visual cues. Birds allowed a 5-min preview of the surrounding landscape prior to release home faster than those denied access... more
    The recognition of familiar areas by homing pigeons, Columba livia, is now known to depend at least in part on visual cues. Birds allowed a 5-min preview of the surrounding landscape prior to release home faster than those denied access to such cues, suggesting that ...
    Experiments with robins wearing frosted goggles have revealed a tantalising relationship between object vision and magnetoreception, shedding further light on the close interconnection between the two senses in migratory birds.
    During group navigation the information shared by group members may be complex, het-erogeneous and may vary over time. Nevertheless, modelling approaches have demonstrated that even relatively simple interactions between individuals can... more
    During group navigation the information shared by group members may be complex, het-erogeneous and may vary over time. Nevertheless, modelling approaches have demonstrated that even relatively simple interactions between individuals can produce complex collective outcomes. In ...
    Chimpanzees (Pan troglodytes) are known to make and use a variety of tools, activities which require them to employ their hands in a skilful manner. The learning process underlying the acquisition of tool-using skills, and the degree of... more
    Chimpanzees (Pan troglodytes) are known to make and use a variety of tools, activities which require them to employ their hands in a skilful manner. The learning process underlying the acquisition of tool-using skills, and the degree of laterality evident in both immature and mature performers are investigated here focusing on the use of leaves for drinking water by members of the Bossou chimpanzee community in Guinea, West Africa. In addition, comparisons are drawn between the present findings and our previous data on the cracking of oil-palm nuts (Elaeis guineensis) using stone tools by members of the same community. The use of leaves for drinking water emerges approximately 2 years earlier than nut cracking, at around the age of 1.5 years, although the manufacture of leaf tools begins only at 3.5 years of age. In addition, in clear contrast with nut cracking, the majority of chimpanzees are ambidextrous in their use of leaves, with only certain individuals showing a bias for one hand. We discuss possible explanations for the earlier emergence and increased ambidextrousness that characterises leaf-tool use in comparison with other forms of tool use by wild chimpanzees. In summary, our results provide the first detailed description of the acquisition process underlying leaf-tool use along with the accompanying patterns of handedness, while also being the first to provide comparisons of the development of different forms of tool use within the same wild chimpanzee population.
    We report the first successful use of miniature Global Positioning System loggers to track the ocean-going behaviour of a c. 400 g seabird, the Manx Shearwater Puffinus puffinus. Breeding birds were tracked over three field seasons during... more
    We report the first successful use of miniature Global Positioning System loggers to track the ocean-going behaviour of a c. 400 g seabird, the Manx Shearwater Puffinus puffinus. Breeding birds were tracked over three field seasons during the incubation and chick-rearing periods on their foraging excursions from the large colony on Skomer Island, Pembrokeshire, UK. Foraging effort was concentrated in the Irish Sea. Likely foraging areas were identified to the north, and more diffusely to the west of the colony. No foraging excursions were recorded significantly to the south of the colony, conflicting with the conclusions of earlier studies based on ringing recoveries and observations. We discuss several explanations including the hypothesis that foraging may have shifted substantially northwards in recent decades. We found no obvious relationship between birds’ positions and water depth, although there was a suggestion that observations at night were in shallower water than those during the day. We also found that, despite the fact that Shearwaters can be observed rafting off-shore from their colonies in the hours prior to making landfall at night, breeding birds are usually located much further from the colony in the last 8 h before arrival, a finding that has significance for the likely effectiveness of marine protection areas if they are only local to the colony. Short sequences of precise second-by-second fixes showed that movement speeds were bimodal, corresponding to sitting on the water (most common at night and around midday) and flying (most common in the morning and evening), with flight behaviour separable into erratic (indicative of searching for food) and directional (indicative of travelling). We also provide a first direct measurement of mean flight speed during directional flight (c. 40 km/h), slower than a Shearwater's predicted maximum range velocity, suggesting that birds are exploiting wave or dynamic soaring during long-distance travel.
    We utilised precision Global Positioning System (GPS) tracking to examine the homing paths of pigeons (Columba livia) released 20 times consecutively 25 km from the loft. By the end of the training phase, birds had developed highly... more
    We utilised precision Global Positioning System (GPS) tracking to examine the homing paths of pigeons (Columba livia) released 20 times consecutively 25 km from the loft. By the end of the training phase, birds had developed highly stereotyped yet individually distinct routes ...
    Perceptual and cognitive processes underlying the skill of ordering numerals were assessed in a female chimpanzee (Pan troglodytes) with previous experience i n computer-assisted numerical competence tasks. The subject was required to... more
    Perceptual and cognitive processes underlying the skill of ordering numerals were assessed in a female chimpanzee (Pan troglodytes) with previous experience i n computer-assisted numerical competence tasks. The subject was required to order 3 numerals from the range of 0-9 into an ascending series, with occasional probe trials (referred to as switch trials) in which the positions of the 2nd