All third-party funded projects

A. Thomas Bugnyar as PI

SOCIAL KNOWLEDGE AND COMPETENCE IN RAVENS
FWF P33960-B: 2020-2024, stand-alone project, together with Dr. Palmyre Boucherie, PhD candidate: Awani Bapat

Abstract of proposal

Studies on children and ‘smart’ non-human animals like primates indicate a link between complexity in social life and the development of intelligence. Individuals differ substantially in their ability to adjust and optimize the expression of social behaviour, resulting in fitness consequences. Early-life social experience has been identified as a key factor for this variation in individual social competence. However, the role of interaction partners other than the mother on the development of social competence is little understood. Furthermore, the long-term effects of early-life experience have been hardly investigated under dynamic field-like conditions, where individuals can choose whom to join and whom to avoid.

Ravens, Corvus corax, are large-brained birds that show sophisticated, ‘primate-like’ socio-cognitive skills. Raven non-breeders form groups that are structured by different types of social relationships, creating a system of dependent ranks and alliances. Yet, individuals differ substantially in how many conspecifics they interact with and how well they form and maintain relationships. The aim of this project is to investigate how early-life social experience shapes the development of ravens’ social competence and mediates the expression of their social behaviour in later stages of life. Specifically, we will test the hypothesis that the number of siblings and the patterns of social interactions among siblings and parents will affect individuals’ opportunities to develop their social competences, resulting in i) different social profiles (diversity of social repertoire, quantity and quality of social relationships), ii) differences in social performance (responsiveness to social cues) and iii) differences in social integration and competitiveness in non-breeder groups. We will experimentally manipulate the brood size of our captive breeding pairs in subsequent years, varying the number of chicks raised by parents per year; depending on the manipulation, the offspring will have the opportunity to grow up with few or many siblings. Per year, we will follow the young ravens’ development i) during the entire family period, ii) during the formation of the first non-breeder group with same-aged peers in captivity, and iii) during the integration in wild non-breeder groups after transition into free-flight. This integrative approach promises important new perspectives for studying the causes and consequences of inter-individual variation in social behaviour and cognition.

FISSION-FUSION DYNAMICS AND SOCIAL COGNITION IN WILD RAVENS
FWF P29705-B29: 2016-2020, stand-alone project, together with Dr. Matthias Loretto,
PhD candidate: Mario Gallego Abenza

Abstract of final report

Complexity in social life has been suggested as one of the main driving forces for the development of higher cognitive abilities in humans and non-human animals. A key aspect of complexity is the formation of social relationships, which become difficult to keep track of when groups increase in size or when individuals vary in spatial cohesion and group membership over time, i.e. they show a high degree of fission-fusion dynamics. Until recently, little attention has been paid to such dynamics, even though highly stable groups are the exception rather than the rule in many social systems outside primates. Hence, the interplay between fission-fusion dynamics, social relationships and cognition is still little understood. Ravens Corvus corax combine features of both, high social complexity and high fission-fusion dynamics. Raven non-breeders form groups that are structured by different types of social relationships, creating a system of dependent ranks and alliances. Yet, these groups are also characterized by high inter-individual variation in fission-fusion dynamics, with some birds staying at a foraging site over long time periods and others for a few days only.

The aim of this project was to investigate i) the pronounced individual differences in fission-fusion dynamics of raven non-breeders and ii) how these differences in dynamics affect the birds’ foraging skills and knowledge about relationships. We conducted behavioural studies and acoustical playback experiments on our unique study population of wild ravens in the Austrian Alps, out of which >400 birds are marked individually and >80 birds got tagged with GPS loggers for tracking their movements. While our behavioural observations confirmed a high and consistent interindividual variation in using foraging sites, we could find hardly any effects of these differences on the ravens’ foraging skills (showing/avoiding kleptoparasitism, food caching); we did, however, find effects on their vocal behaviour, with locals ravens being more active than vagrants, and ravens generally paying much attention to the callers’ identity, age and/or social class. The latter was confirmed with playback studies under controlled conditions on temporarily captive ravens. These findings suggest that ravens are capable of telling group members apart. What remains still unclear is how much the fission-fusion dynamics affect the ravens’ personal knowledge about group members, as we could not find the predicted link between the birds’ responses to playback and their degree of fission-fusion dynamics so far. Future studies will reveal whether our results were constrained by methodological or analytical short-comings or whether ravens could potentially handle much more social information as originally thought. The project thus laid the basis for exciting further work. Notably, it kick-started a long-term monitoring of GPS-tagged ravens at our study site in the Alps and a similar project in Yellowstone National Park.

WHAT DO CROWS IN VIENNA ZOO?
FWF TCS67: 2020-2021, Top Citizen Science project together with Dr. Palmyre Boucherie and Dr. Didone Frigerio

Abstract of final report

Ravens and crows are renowned for using anthropogenic food sources. Although their foraging groups have a fluid character, with individuals coming and going, recent studies indicate that these groups are not entirely anonymous crowds. Some individuals meet regularly, possibly because they develop individual preferences for specific locations or for social constellations. What makes individuals join groups has been studied in ravens on a large geographical scale, across the Alps (P29705-B29, see above). We here use crows to study group choices on a small scale, as crows exploit various food sources in cities. The Zoo Vienna not only offers a variety of foraging opportunities for crows but also attracts thousands of visitors per day. We thus applied a Citizen Science (CS) approach to examine effects of foraging sites (enclosures with different zoo animals) on crows’ group formation. Furthermore, we used the CS approach to focus on rare events like interactions between crows and zoo animals and to learn about the lay persons’ ability to distinguish between different corvid species. Despite of severe restrictions due to Covid-19 pandemic, including four lockdowns in the course of a 2-year frame, the CS approach worked exceptionally well: zoo visitors got involved in data collection via the newly developed App “KraMobil”, resulting in more than 17.000 entries over the summer period in 2020 and 21. While the analysis of this substantial data set is still ongoing, preliminary findings indicate that the foraging groups of crows are rather small, which fits well to previous studies on crows in Vienna zoo. We can also confirm the strength of the CS approach in detecting rare events: in comparison to the impressive number of 1042 sightings on inter-specific interactions collected via crowdsourcing in this project, two master students could previously only observe 19 of such cases within a 6-months observation period. Finally, a comparison between the species-detection data and the answers provided in a verbal survey among 230 people showed that participants were able to identify the crow species much better as they thought they would. Taken together, these findings reveal the attractiveness and appropriateness of the CS approach on behavioral studies in an urban setting like the Zoo Vienna. Follow-up studies are already in preparation.

RAVEN POLITICS: Understanding and Use of Social Relationships
FWF Y366-B17: 2008-2014, START Prize
PhD candidates: Anna Braun, Markus Boeckle, Tina Gunhold, Georgine Szipl, Matthias Loretto

Abstract of final report

Corvids are renown for enlarged forebrains and cognitive abilities that rival those of primates. However, compared to primates, little is known about the factors that drive corvid brain evolution. One of the possibilities is life in complex social groups. Species like ravens Corvus corax have been reported to deceive others but also to cooperate with others for access to food. ‘Raven Politics’ aimed at empirically testing the hypotheses concerning social complexity and intelligence in corvids.

We first focused on what ravens understand about other individuals and their social relations. Applying methods from psychology and biology, we showed that ravens i) recognize individual variation in communication (i.e., who is who), ii) remember their relationship to former group members over years (whether they were friends or foes) and iii) respond to simulated rank changes as if they are aware of third-party relationships (who are the others’ friends and foes). We then focused on how ravens make use of their social knowledge in daily life, combining field and lab techniques. We found that i) ravens show a variety of third-party interactions, including social support in fights and post-conflict consolation, ii) bonded ravens rise in rank most likely because of mutual social support and iii) bonded ravens selectively intervene in others’ bonding attempts, probably to prevent those from becoming powerful themselves. Ravens are thus capable of showing a sophisticated level of social manipulation that resembles a form of ‘politics’ hitherto described only from chimpanzees. We finally addressed the question of how raven bonds could work in a system of high social fluidity. Using GPS technology, we revealed different levels of fission-fusion dynamics in non-breeders, with some ravens meeting each other on a daily basis, whereas others meet only once a month or even year. Such a layered social system with different forms of interdependencies resembles that of some mammals, including us humans. These findings have been largely confirmed by comparative studies on crows, indicating that pair-bond-like relationships and temporarily stable subgroups of non-breeders may be typical for corvids in general. Comparative work also involved species like parrots and primates and concerned cognitive aspects of the programme, like paying attention to and learning from others.

Taken together, ‘Raven Politics’ represents the first comprehensive study on the use of social knowledge in an avian model system. It confirms that ravens come to understand, and use, their social world in a similar way to some primates, despite of their radically different brain structures and evolutionary trajectories. The findings thus provide strong support for the idea of a convergent cognitive evolution between corvids and primates. The studies inspired several national and international collaborations, led to a number of follow-up projects, and strengthened the reputation of Austria as one of the main centres for animal cognition.

SOCIAL KNOWLEGDE IN RAVENS
FWF R31-B03: 2004-2007, Erwin-Schrödinger return fellowship
Co-supervision of PhD candidate: Christian Schloegl

Abstract of final report

The project aimed at investigating (i) how ravens Corvus corax make use of others’ visual behaviour and (ii) if they come to understand that others may see things differently than they do. We pursued these questions via four lines of research and with different experimental paradigms. We first investigated the development in following others’ gaze (= head and eye direction), showing that ravens are capable of visual co-orientation with conspecifics and human experimenters already shortly after fledging in May, whereas they come to track others’ gaze direction behind obstacles not before September/October. Interestingly, the two modes of gaze following also showed different habituation pattern, suggesting that they may be based on different underlying mechanism. In a second step, we performed two parallel series of experiments, exploring the birds’ ability to base their foraging decisions on others’ visual orientation that indicate the location of hidden food (using the object choice paradigm) and on others’ visual experience at the hiding of food (using a variant of the knower/guesser paradigm). Results indicate that ravens hardly pick up on the visual behaviour of others to find hidden food. In sharp contrast, ravens appear to be excellent in distinguishing who has and has not been visually present during the caching of food and selectively adjust their timing to pilfer caches and even the sequence of pilfering (which cache to take first) according to the ‘knowledge state’ of potential competitors. Follow-up experiments revealed that the ravens’ performance is affected by manipulation of the competitors’ view rather than by their mere visual presence, suggesting that birds indeed understand something about the others’ visual experience. These findings are strikingly similar to those obtained for apes and, in principal, can be interpreted as ravens being capable of showing an element of a human-like theory of mind (concept see). However, the findings are also consistent with a relatively complex non-mentalistic interpretation that rests on their ability to geometrically follow others’ gaze behind obstacles and their memory for past experiences with individuals that had the possibility to see the caching. Future studies are needed to distinguish between these alternatives. From an evolutionary perspective, it seems possible that corvids as a group may possess well-developed gaze-use skills that are not necessarily present in other birds, since rooks Corvus frugilegus and jackdaws Corvus monedula seem to geometrically follow others’ gaze behind obstacles whereas waldrapp ibises Geronticus eremita and keas Nestor notabilis do not.

Taken together, we found that ravens are capable of sophisticated forms of gaze following and judging the others’ visual perception, taking into account that visual barriers may block their own and/or other’s view. Hence, they show a level of understanding roughly comparable to that of 2-years-old children. Our results provide strong support for the recent idea of a convergent cognitive evolution between corvids and primates.

TACTICAL DECEPTION IN RAVENS
FWF J2064 and J2225: 2001-2003, Erwin-Schrödinger fellowship

Summary report

In the last two years, I have been working on social cognition in ravens in collaboration with Prof. Bernd Heinrich at the University of Vermont, USA.

Considering the neophobic nature of ravens, the main goal of the first year (J2064) was to obtain relatively tame ravens that cooperate during experimental testing. This was achieved by hand-raising birds from nestling to fledging and by habituating birds at a very young age to temporal separation from their group members in specifically designed experimental compartments. Experimental compartments are visually isolated but connected through windows that can be covered with opaque curtains. This set-up allows full control of what birds can and cannot see. A second object of hand-raising raven was to investigate the ontogeny of caching behaviour and the birds’ improvement in social manipulation. The basis of these studies was standardized observation during daily foraging bouts combined with tests on object permanence and social learning. We found that the birds’ stepwise progress in caching, from (a) partial hiding by sticking food next to structures to complete hiding by (b) sticking food into gaps and (c) covering the cache with surrounding substrate, correlated with the acquisition of Piagetian Stage 4 and 5 of object permanence. In addition, we found that young ravens avoided interactions with conspecifics during caching of food but initiated interactions during caching of small, non-edible objects. Repeated interactions over cached objects positively affected the birds’ skills to prevent others from raiding and to successfully raid the caches of others in the first two months post-fledging. Hence, improvement in caching behaviour seems to go along with (a) the development of cognitive capacities, such as object permanence and memory for the observed caches, and (b) competition with group members on the cached items.

The goal of the second year of the study (J2225) was to examine the ravens’ deceptive abilities during caching and raiding (i.e. Can birds tactically inhibit behaviour, withhold information and conceal intentions?). Experiments took place in the experimental compartments and involved manipulation of the (i) presence and (ii) view of conspecific competitors towards the cache makers. In a first step, ravens were allowed to cache either in private (no conspecifics present in adjacent compartments), in front of conspecifics that can see (“observers”; window to caching compartment uncovered) or cannot see (“non-observers”; window covered). Birds made fewer caches and more often refrained from caching with observers than in private and with non-observers. However, compared to in-private trials, the time to finish the caches was shorter with both observers and non-observers. This suggests that cache makers are aware of the presence of conspecifics but suppress caching only when their competitors have visual access.

In a second step, ravens got the chance to prevent others from seeing their caches by caching behind a visual barrier. Birds selectively cached outside view of observers, supporting the hypothesis that ravens are able to withhold information from conspecifics. However, cache makers did so only when observers were perched next to the observation windows and not when they were in the back or on the ground of the compartment. This raises the possibility that ravens may take into account the view of competitors for their deceptive maneuvers.

In a third step, cache makers were allowed to compete with conspecifics that are knowledgeable or naïve in respect to the location of their previous caches. Birds retrieved their caches more often when paired with knowledgeable than with naïve competitors, suggesting that cache makers can remember who has and has not observed them caching. Alternatively, cache makers may have based their decision on behavioural cues of the raiders (e.g. different patterns in approaching the caches). However, during the same experiment, we examined the behaviour of (knowledgeable and naïve) raiders in relation to the identity of their competitor, either the cacher or another conspecific. Compared to in-private raiding trials, knowledgeable raiders delayed their raiding attempts when paired with the cache maker but speeded up when paired with another competitor. This demonstrates that ravens selectively conceal their raiding intention from those individuals that could prevent their raiding attempts by retrieving the caches first. Furthermore, the results provide little support for the hypothesis that cache makers can use the behaviour of raiders to judge the likelihood of raiding attempts.

In a fourth step, we further examined the knowledge of raiders. Birds that had observed a previous caching event (knowledgeable raiders) were tested with competitors that had also seen that caching event (co-observers) or with competitors that were naïve in respect to the cache location (non-observers). Knowledgeable birds delayed their raiding attempts with naïve dominant non-observers (until those were foraging at another part of the aviary) but speeded up raiding with knowledgeable dominant co-observers. This further supports the idea that ravens can selectively withhold intentions and, more importantly, demonstrates that they base their raiding decision on what a competitor has and has not seen.

In summary, these results provide clear evidence for tactical deception in ravens. Moreover, they suggest that birds may take into account the visual perspective of others. This conclusion has been corroborated by an experiment on gaze following, carried out with the help of KLF Ph-D candidate M. Stöwe. Ravens followed the gaze direction of a human experimenter not only above them but also around a visual barrier, suggesting that, similar to chimpanzees and human infants of about 18 months of age, they can project a line of sight for the other person into distance. These experiments provide the basis of my application for the Schrödinger follow-up program. In addition to this extensive work on social manipulation during food caching, studies concerning (i) the conditions promoting cache raiding, (ii) the birds’ understanding of means-end properties and (iii) the effects of social context on neophobia and exploration were carried out in collaboration with B. Heinrich and M. Stöwe.

B. Collaborative Projects

COGNITION AND COMMUNICATION II
DK W1262-B29: Doctoral program, 2021-2024, speaker Tecumseh Fitch, Co-PIs Thomas Bugnyar, Leonida Fusani, Stefanie Höhl, Ludwig Huber, Sonia Kleindorfer, Claus Lamm, Friederike Range, Angela Stöger-Horwath, Sabine Tebbich, PhD candidate Thomas Bugnyar: Silvia Damini

2017-2021, speaker Tecumseh Fitch, Co-PIs Thomas Bugnyar, Leonida Fusani, Stefanie Höhl, Ludwig Huber, Sonia Kleindorfer, Claus Lamm, Friederike Range, Angela Stöger-Horwath, Sabine Tebbich, PhD candidate Thomas Bugnyar: Katharina Wenig

COGNITION AND COMMUNICATION I
DK W1234-B17: Doctoral program, 2011-2015, speaker Thomas Bugnyar, Co-PIs Tecumseh Fitch, Walter Hödl, Ludwig Huber, Kurt Kotrschal, PhD candidate Bugnyar: Alexandru Munteanu

Abstract of first application

The University of Vienna is rapidly becoming one of the leading centers for the study of cognition from an integrated biological viewpoint. In contrast to the currently-dominant approach of evolutionary psychologists, cognitive biology seeks to understand cognition, communication and behavior, in human and other animals, from both proximate (mechanistic and developmental) and ultimate (phylogenetic and adaptive) perspectives, with a strong emphasis on experimental comparisons of multiple species (the comparative method). Although already internationally recognized for research, and well established in teaching at the undergraduate and Masters levels, our group currently lacks a well-developed PhD training programme. The purpose of this DK Proposal is to integrate existing strengths in research and teaching and add new teaching and training opportunities, thus creating a world-class center for training the next generation of PhD students in cognitive biology. We will prepare our students to excel in this competitive and highly interdisciplinary research area by focusing on rigorous experimental research within a broad theoretical framework, focused on evolutionary theory and the comparative method. PhD students in our programme will be trained in both field and laboratory research, experimental design, and rigorous use of the comparative method to address focused questions concerning neural, endocrine and behavioral mechanisms and their ontogeny from an evolutionary perspective. Encompassed by the Center for Organismic and Systems Biology (School of Life Sciences, University of Vienna), and focused on the new Department of Cognitive Biology, the training programme will begin with five internationally recognized researchers but is expected to expand during the period of funding to about twice that number with the incorporation of new “rising stars” in the Vienna cognitive research scene. Strong connections already exist with other Viennese institutions (especially Zoo Vienna and University of Veterinary Medicine), and with other disciplines within the University of Vienna (e.g., philosophy, psychology and linguistics, via the cognitive science Masters). The DK proposal would round out an already vibrant and well-equipped research center, increase the international attractiveness of our group to the best and brightest young PhD students, and place Vienna at the center of this new biological and evolutionary approach to understanding cognition.

COBRA (Cognition and Brain of Ecological Invaders)
EU, FP7 PEOPLE Marie Curie Actions (international research staff exchange scheme), 2014-16, Coordinator: Thomas Bugnyar, Co-PIs: Onur Güntürkün (Bochum, D), Sue Healy (St Andrews, UK), Andrea Griffin (Newcastle, AUS)

Abstract of final report

The joint exchange program involved the movement of three experienced researchers between the Universities of Vienna, Austria, University of St Andrews, UK, Ruhr University in Bochum, Germany, and University of Newcastle, Australia. Specifically, a researcher from Newcastle spent 6 months in Europe, split between St Andrews, Vienna, and Bochum. Researchers from Bochum and Vienna visited Newcastle for 6 months. At both their home institution and during each secondment, exchange researchers have collected data towards a geographically global research project that aims to use a collection of avian species as model systems to understand: 1. The role of behavioural flexibility in species’ adaptation to urbanization, and 2. The extent to which behavioural flexibility is associated with changes in brain anatomy.

The program was structured along four work packages (WP1-4). While WP1 concerned the project management and coordination, WP2-4 concerned the empirical studies on Indian mynahs (WP2), European crows (WP3) and European songbirds like house sparrows and great tits (WP4). Birds were tested in the field with simple problem solving tasks for their behavioural flexibility along a rural to urban gradient. For instance, they had to remove a cork that was blocking the access to food at a known feeder. By examining several species, in several geographical locations, using several different measures of behavioural flexibility, and describing associated brain changes, we find support for the hypothesis that increasing behavioural flexibility in increasingly urbanized environments is a general effect. Specifically, urban birds tend to be more exploratory and more risk taking than rural birds, but they do not show any differences in innovativeness, sociality, or responses to predators. These findings clearly demonstrate what factors makes urban birds ‘special’ and provide hints for when to expect species differences. The results likely have implications for conservation attempts of declining species and the management of invasive species. They also highlight the importance of comparative studies at different places that could only be achieved by close collaboration between different researchers and their working groups.

Although some analyses are still ongoing, the project already resulted in 14 manuscripts for publication in international peer-reviewed journals and 16 presentations at conferences, workshops and seminars. Notably, the project resulted in the invitation to edit a special issue in the renowned journal Animal Cognition on one of the project’s main topics (the role of cognition in adapting to changing environments).

MODELLING SOCIAL TRANSMISSION: How Relationships, Group size and Group Structure influence Social Learning in Wild and Captive Corvids
WWTF CS 11-008: 2012-2015, PI: Christine Schwab, Co-applicant und host: Thomas Bugnyar
PhD candidate: Rachael Miller

Abstract of final report

Social learning is considered the crucial prerequisite of any cultural phenomena to emerge. However, social learning itself covers a wide range of theoretical approaches and assumptions, ranging from diverse learning mechanisms to similarly manifold learning strategies. In this project, we concentrated on the latter and investigated how social structure influences the transmission of social information through groups of carrion/hooded crows, Corvus corone/cornix, and ravens, Corvus corax. We chose these two corvid species because, similar to humans, they exhibit a social system comprising on one side long-term partnerships and on the other side (sub-)group formation with high degrees of fission-fusion dynamics. Notably, our unique setting in Vienna allowed us to combine (i) observations with (ii) mathematical modeling and (iii) empirical experimental tests under field and captive conditions. In captivity, we experimentally seeded innovations (by training a particular bird to acquire food at an ‘artificial carcass’ apparatus) and, based on the analysis of the birds’ social networks, tested the spreading patterns of social information through groups. Employing recently developed mathematical models, we could determine the type of social network that has the strongest influence on the transmission process (affiliation network) as well as the overall contribution of social learning to the transmission (60%). Despite of our initial success in catching and marking wild crows in the area of Vienna Zoo, the proportion of marked birds in the population remained too small to conduct similar transmission studies under field conditions. With an output of >12 publications and several international collaborations, the project successfully set the stage for future studies.

COOPERATION, COLLABORATION AND COGNITION IN RAVENS
FWF M1351-B17: 2012-2013, Lise Meitner fellow: Jorg Massen,
Co-applicant and host: Thomas Bugnyar

Abstract of proposal

Cooperation is a useful strategy to gain benefits that cannot be obtained alone, yet is characterized by risky investments. To deal with these uncertainties several mechanisms may have evolved. It has been argued that among group members or known individuals cooperation is unconsciously mediated by emotions. Yet, when dealing with unfamiliar individuals or strangers, human cooperation is governed by complex cognitive decisions involving the calculation of costs/benefits and the understanding of roles and intentions of collaborating individuals. Whether non-human animals also employ different decision rules for cooperation with either known or unknown individuals remains unknown. This study tests experimentally which behavioural decision rules ravens use in their cooperative behaviour with conspecifics of different familiarity. Ravens interact regularly with both familiar and unfamiliar conspecifics and are renowned for advanced socio-cognitive skills. The experiments aim to conceive whether ravens have a preference for cooperation with familiar individuals, whether they prefer an equal distribution of rewards for their cooperative act and whether ravens can calculate costs and benefits of their cooperation and act accordingly. Moreover, the experiments are complimented with an observational study on wild ravens, investigating the contingency of exchange patterns for different commodities in either familiar or unfamiliar dyads.

COOPERATION IN CORVIDS (COCOR)
FWF I105-G11: 2007-2010, PI Group Austria: Thomas Bugnyar
Part of ESF EUROCORES program TECT (The Evolution of Cooperation and Trading), Coordinator: Ronald Noe, Postdoc: Orlaith Fraser

Abstract of final report

This project was part of the international collaborative research program ‘Cooperation in Corvids’ that was conducted within the ESF-EUROCORES framework ‘The Evolution of Cooperation and Trading’. Our Group Austria aimed at investigating the role of social relationships in raven cooperative interactions. The concept was to focus on naturally occurring forms of cooperation, notably support in conflicts and sharing informing about food via calls. Concerning cooperation in conflict situations, we could show patterns that are strikingly similar to those reported in primates: ravens are highly selective in helping others in fights and/or in providing post-conflict behaviour such as reconciliation and consolation, with relationship quality being a main predictor for their choices. Comparative studies on related species were conducted by Groups France and Spain. Concerning communication, we found a high inter-individual variation in food calling, indicating that some ravens may be more or less reliable when it comes to informing others about feeding locations. Furthermore, we could demonstrate that ravens modulate their calls depending on their relationship to the receivers: if those are non-friends, they make themselves acoustically bigger. In a collaboration with Group Italy, we took detailed measures of the vocal tract to test if formants and their changes correlate with actual and perceived body size.

Finally, we tested some socio-cognitive skills underlying cooperation by adapting experimental paradigms used in primates, such as exchanging food for better food with a human experimenter, to corvids. We could show for the first time that birds can cope with delay of gratification and wait several minutes to exchange food for a more preferred reward. Moreover, when tested next to each other, they responded to inequity in reward structure and working effort (unfair treatments) and, under given conditions, they were even behaving prosocially, i.e. helping others at no costs but also without any immediate benefits.

Taken together, we found that corvids are highly selective in when and with whom they cooperate and that they show socio-cognitive skills that are comparable to those of primates. Our results provide support for the idea that sophisticated social strategies and cognitive skills may evolve independently of phylogeny in systems with a given degree of social complexity.

INCORE (Integrating Cooperation Research across Europe)
EU, FP6 043318, 2007-2010, Coordinator: David Skuse, 27 groups; PI Austria: Thomas Bugnyar WP 7: Building a network to understand economics and cooperation in corvids

Abstract of final report

The main objective of WP7 was to improve networking between European working groups on corvid social behaviour. This has been fully achieved. Working groups with background in behavioural ecology (Spain), comparative psychology (UK), behavioural biology/ethology (France, Austria) and veterinary medicine (Italy) have engaged in several lab-visits, discussion meetings and student exchanges. As a result, collaborations between groups have been initiated (e.g. Spain-Austria) and improved substantially (e.g. Austria-France, Austria-Italy). Joint papers and grant proposals are in progress and have already been submitted, respectively.

The second objective of WP7 was to integrate existing work on cooperation and its social and cognitive components into bigger international framework like GEBACO and TECT. The approach to corvid cooperation has indeed profited conceptually and methodologically from integration into these frameworks. Notably, the links to research on primates have been strengthened (almost half of contact meetings and one third of the student visits involved primatologists) and contacts to mathematicians, geneticists and economists have been established. One of the results has been an increased interest in the comparative approach, highlighting the possibility of a convergent evolution of cognitive traits. This increased interest is exemplified in exchange of PhD students and postdocs between primate and corvid labs (e.g. O. Fraser, E. Polizzi, E. Price, C, Scheid), new grant proposals and funded programmes.

C. Hosted Projects

PHYSIOLOGICAL BASES OF PROSOCIAL BEHAVIOR
Marie Skłodowska-Curie Postdoctoral Fellowship 2023-2025, Postdoc: Jelena Katic (DE), Okinawa Institute of Science and Technology (JP), host: Thomas Bugnyar

Abstract of proposal

DO SOCIAL RELATIONSHIPS AFFECT PRESCHOOLERS’ PROSOCIALITY?
FWF V863: 2021-2025, Elise-Richter senior postdoc fellow Lisa Horn-Peter (AT),
host: Thomas Bugnyar

Abstract of proposal

ACCELERATION TO FOOD
FWF Y1486: 2023-2028, START Prize Petra Sumasgutner (AT),
host of raven studies: Thomas Bugnyar

Abstract of proposal

In the Project “Acceleration to Food”, an international team led by Dr Petra Sumasgutner from the University of Vienna is researching how humans influence wild animals. With so-called accelerometers, sensors that are attached directly on the animal, behaviors such as searching for food, hunting and scavenging can be distinguished from one other, without relying on direct observations. Since these loggers are also equipped with a traditional GPS, feeding sites can be located and feeding times can be defined. We target endangered predators and scavengers, especially raptors, known to be sensitive to human influences. The more we know about spatial and temporal patterns, the better we can protect wildlife in anthropogenic landscapes.

Recent advances in remote wildlife monitoring include tri-axial acceleration sensors (accelerometers) that measure body posture (static acceleration) and body velocity (dynamic acceleration). The recorded patterns can be used to interpret which behavior is shown when and where, and to quantify the associated energy expenditure. These ‘passive sensors of change’ create extensive data sets that will be analyzed with machine learning. The developed algorithms will allow us to distinguish successful hunts from unsuccessful attempts and feeding on carcasses, so we can identify which anthropogenic structures or human activities influence raptor foraging behavior.

In ecology, it is often difficult to disentangle the influence of infrastructure (human footprint) from that of direct disturbance (human activity). During COVID-19 related lockdowns, these two factors were decoupled in a unique way and created an unprecedented research opportunity. For this reason, we launched the ‘Global Anthropause Raptor Research Network’ that continues to grow and is managed in collaboration with the Biologging Initiative and the Peregrine Fund. To date, over 500 raptor researchers from across the globe have indicated their interest in pooling global data sets to unravel mechanisms underlying the ongoing raptor decline. We will focus on the time surrounding the corona pandemic, to disentangle the different components of human impacts on raptors. Furthermore, we will underpin the global patterns with specifically designed supporting experiments. One involves common ravens – an important member of the scavenger group – to learn how animals find carcasses and how information about their location travels between individuals and across populations. A second relates to Galápagos short-eared owls – the only naturally occurring avian predator on Floreana Island – and how they cope with invasive mammals that were introduced by humans. Thus, we will learn about raptors as ‘active indicators for change’ and the role of scavengers and predators in stabilizing ecosystems. From these results, conservation strategies will be developed so we learn how to sustainably share our planet, in order to conserve our biodiversity through the era of the Anthropocene.

THE INTERPLAY BETWEEN COGNITION AND ECOLOGY IN EXTRACTIVE FORAGING BEHAVIORS
WWTF: 2023-2027, Vienna Research Group leader Barbara Klump (DE), Max-Planck Institute of Animal Behavior, host: Thomas Bugnyar

Abstract of proposal

Foraging successfully –and solving foraging problems– requires cognitive abilities across both ecological and social domains and is considered an important driver of enhanced cognitive skills. Extractive foraging – the extraction and processing of embedded or encased foods like arthropods, nuts and eggs – requires intensive object-manipulation. Animals have evolved both morphological (e.g. multi-purpose bill in parrots) and behavioural (tool use, prey-dropping) adaptations to access these otherwise inaccessible food items. Much attention has been given to the cognitive processes implicated in extractive foraging with tools (e.g. causal reasoning, planning, generalization) and the literature on the ecological significance of tool use is growing.

Extractive foraging without tools on the other hand –while likely implying the same complex cognition– is understudied and comparative work on extractive foraging with and without tools is missing. To fill this knowledge gap, I propose to study two large-brained, long-lived, and social species that engage in extractive foraging without tools – carrion crows (Corvus corone, henceforth crow) and Sulphur-crested cockatoos (Cacatua galerita, henceforth cockatoo). Corvids and parrots share many of the life history traits that have been identified as drivers for enhanced cognitive skills (e.g. large brains, long-lived, social) but differ in their morphology (especially their feet and bills). This makes them ideal systems to investigate the cognition and ecology of extractive foraging and object manipulation. Many bird species are known to drop hard-shelled items to break them open but the development and cognitive mechanisms involved in these behaviours remain unexplored. Crows open nuts by either pecking them open or dropping them on hard surfaces, while cockatoos use two different methods (splitting and nibbling) to open Jacaranda and other seed pods. Using a combination of experiments (in captivity and in the wild) and state-of-the-art tracking technology, I aim to investigate the ontogeny, underlying cognitive mechanisms and ecological significance of these behaviours. I will follow Tinbergen’s questions to gain a complete understanding of the behaviour by addressing it from multiple perspectives.

I propose to build my first research group to pursue an ambitious research project with five interrelated objectives. Objective 1 will investigate the ONTOGENY of nut-dropping behaviour in carrion crows. By raising juveniles in groups with ad libitum access to walnuts, I will map individual differences in uptake and performance of the behaviour and compare it to control groups who only get access to walnuts at specific points in time. Objective 2 will investigate the COGNITIVE MECHANISMS underlying nut-dropping behaviour in carrion crows using a cognitive test battery, with a focus on physical cognition (i.e. how an animal acquires and uses information about the physical world) and problem solving. New tasks will be designed to ensure that they are ecologically relevant and performance will then be compared to tasks which are well-established in the field but are not ecologically relevant for carrion crows. This enables a comprehensive assessment of how and why a species evolved the cognitive abilities it possesses.

Objective 3 will investigate the INDIVIDUAL VARIATION in seed- and nut-opening behaviour. A combination of field experiments (with cockatoos and crows), citizen science data collection (using a modified version of an existing mobile app for crows) and data from captive experiments from objective 1 (crows) will be used to address questions of the distribution and learning mechanisms of the different opening variants. Objective 4 will investigate the ECOLOGICAL SIGNIFICANCE of extractive foraging. Using field experiments with habituated wild cockatoos and newly developed ‘mini-tags’ which enable simultaneous tracking of crows and nuts, I will investigate how reliant individuals are on nuts, how the behaviour relates to local resource availability and how naïve and knowledgeable individuals interact when the resource is available. Objective 5 SYNTHESIZES the results from objectives 1-4 to investigate why species differ in their cognitive abilities and reliance on extractive foraging. Using a comparison between primates and birds, I will consolidate our knowledge on how complex cognitive traits develop within species over ontogeny and between species over evolutionary time.

DYNAMATES: DYNAMIC AUDITORY PREDICTIONS IN HUMAN AND NON HUMAN PRIMATES
FWF ZK..: 2021-2025, Young Independent Research Group (YIRG): Robert Baumgartner (AT), Ulrich Pomper (AT), Michelle Spierings (NL), host of M. Spierings: Thomas Bugnyar, Postdoc: Ruth Sonnweber, PhD candidate: Julia Grabner

Abstract of proposal

The human sensory information is often ambiguous, so that our brain generates generates several parallel interpretations and predictions and ultimately has to settle on one. Currently, most of our knowledge about these perceptual processes comes from studies of the sense of sight. Comparatively little is known about our our sense of hearing, which is equally central to our survival and social behavior. Dynamates aims to close these central gaps in our knowledge about auditory perception by testing the predictive mechanisms of closely related species in realistic but highly controllable virtual acoustic environments and and mapping them with computer models. In addition, Dynamates will use electroencephalography (EEG) in humans to investigate the neural basis of the underlying processes. The project is thus based on an interdisciplinary collaboration between experts from the field of computer modeling (Robert Baumgartner), neuroscience (Ulrich Pomper), and cognitive cognitive biology (Michelle Spierings).

The Evolution of Pro-Social Concern
FWF P26806: 2014-2017, PI: Jorg M. Massen, host: Thomas Bugnyar
Postdoc: Lisa Horn, PhD candidate: Martina Stocker

Abstract of proposal

In an attempt to better understand evolution of altruism, there has been a recent surge in studies on pro‐social behaviours like helping. Next to humans a variety of animals has been tested in experiments on pro‐sociality, with however, rather inconsistent results within and between species and across context. This raises questions about the evolutionary pressures (e.g. aspects of social life) and motivations behind pro‐social behaviour (e.g. need, sympathy). Therefore, the aim of the current proposal is two‐fold: The first aim is to test two main hypotheses about the evolution of pro‐social behaviour, namely the cooperative breeding hypothesis and the social bonding hypothesis, by making use of the comparative approach, including species with two distinct social features (cooperative breeding (CB) and social bonds (SB)). To control for effects of common ancestry, next to humans I will include two species per two phylogenetical different lineages (primates: common marmosets (CB) vs. long‐tailed macaques (SB); and corvids: Iberian magpies (CB) vs. common ravens (SB)). The second aim of the proposal is to test underlying motivation of prosocial behaviour, by confronting all five species with a series of experiments that vary across necessity and costs of pro‐social behaviour.

Abstract of final report

This project has shown that prosocial and cooperative behaviours have evolved independently in both primates and corvids, and that the degree of such behaviour in a species depends on the species’ social system and the specific context for which the behaviour is needed.

The aim of this project was to test two main hypotheses about the evolution of prosocial behaviour, namely the cooperative breeding hypothesis and the social bonding hypothesis, by testing humans and species that portray either cooperative breeding (CB) or strong social bonds (SB), while looking at two completely different animal classes: primates (common marmosets (CB) vs. long-tailed macaques (SB)), and corvids (Azure-winged magpies (CB) vs. common ravens (SB)). First, we could show that even in a very competitive environment humans are as prosocial as commonly believed. Moreover, in series of experiments, we showed that in a paradigm comparable to those used for animals, human children are prosocial too, even when at a cost to themselves, and already at an early age (3-5yrs). In contrast, ravens failed to show other-regard in two different paradigms, although they did provide at a moderate level in a group service paradigm. Nevertheless, the cooperatively breeding Azure-winged magpies provided at much higher levels in the same group service paradigm and in fact took any chance they got to provide to their group. Additional testing on a range of other corvid species revealed that species that have territorial pair-bonds or breed in colonies, where least prosocial, and those that are facultative cooperative breeders where somewhere in between, providing some first qualitative proof for the cooperative breeding hypothesis in corvids. Moreover, we noticed that the motivations behind being prosocial also differed per species, with azure-winged magpies providing indiscriminately, whereas for example the ravens only provided to higher-ranking individuals.

In contrast to their other regarding preferences, the ravens showed to be very proficient in a cooperation task, comparable to, for example chimpanzees. And both in the ravens, but also in kea, we found that particularly the social bond between two individuals predicts how well they will cooperate, and the ravens in fact choose to cooperate with their friends. In long- tailed macaques we could elucidate physiological mechanisms that may be responsible for such preferences; i.e., we could show that salivary cortisol levels of the macaques dropped when cooperating, yet only when cooperating with a friend, and thus cooperating with a friend may have a stress alleviating effect.

Finally, in common marmosets, we brought together the studies on prosociality and cooperation, and showed that prosocial individuals are also more cooperative.
In sum, by showing prosociality and its limits in different context in species ranging from primates to corvids, we have gained a better understanding of how prosociality evolved to the extraordinary levels we can witness in humans.

C. Infrastructure Projects

COMPUTATIONAL ETHOLOGY: Cutting-edge automation technology for the measurement and analysis of animal behavior and cognition
BMWFW, HRSM Ausschreibung 2016, funding period 2017-2021, University of Veterinary Medicine & University of Vienna: Thomas Bugnyar, Tecumseh Fitch, Leonida Fusani, Ludwig Huber

Abstract of final report

Computational ethology (CE) integrates methods from experimental animal physiology, taxonomic fieldwork, and comparative behavioral research, and seeks to build models for various types of experimental data on natural behavior (social networks, sequences, images, etc.) of biological systems. The underlying hypothesis of ethology is that uncovering the structure of behavior – how behavior in the natural environment is built from components and organized over time in response to ecologically relevant stimuli – provides insights into how behavior (largely self-motivated and without physical constraints) is generated.
To this end, methods from a variety of mathematical and computational fields (e.g., complexity theory, algorithms, machine learning, robotics, etc.) are used to answer the question: “How can I efficiently store, annotate, search, and compare information from biological measurements and observations?”

The goal of this project was to implement CE, which is the construction of automated systems for recognizing and analyzing individuals, behavior, and vocalizations of freely moving animals living in groups. A series of timed steps was required to build CE. Within 4 years, 3 individual measures (work packages/WP) were set and subsequently interconnected. These technologies were not commercially available as a complete system, but had to be developed and adapted on site. These subsystems were developed individually at focal species over the 4-year period and transferred into a CE complete system.

WP 1: Development of a biologger system to locate and record interactions of social animals in large enclosures or aviaries.
WP 2: Setup of a multi-camera recording and analysis system which allows targeted, automated extraction of video sequences as well as quantitative data analysis (3D position, distance to each other); synchronization of the video analysis with sensors (loggers) directly attached to the animals is possible. The planned system was modular, included 4 cameras each, software and storage systems and was adapted to different enclosures or species.
WP 3: Development of a portable bioacoustics measurement system, which can be used flexibly in the enclosure of different species. Consisting of several microphones and special cameras, it should allow high-resolution audio-video synchronization of high-speed recordings during vocalizations. The planned complete system included an X-ray device, software, storage and a transport device.

Impact on projects of the current performance agreement:
CE will expand the existing internationally competitive research field of cognitive biology in Vienna with the latest methods and IT developments. So far, these technologies are only established at very few locations (e.g. MPI Konstanz, Cambridge, Oxford). With this project, the research partners at the University of Veterinary Medicine Vienna (Vetmeduni Vienna) and the University of Vienna (UniVie) strengthen their leading position in the field of cognitive and behavioral biology, and can also actively develop the research field further.
The Messerli Research Institute of the Vetmeduni Vienna (WP1, research group L. Huber) is an interdisciplinary competence center for questions concerning the human-animal relationship, where animal welfare, ethics, biology and medicine in dealing with animals are considered in an interdisciplinary way. At the Konrad Lorenz Institute for Comparative Behavioral Research at Vetmeduni Vienna, researchers address questions of proximate mechanisms and evolution, mostly with animals in nature but also under semi-natural conditions and in the laboratory (WP2, L. Fusani).
The Department of Behavioral and Cognitive Biology of UniVie (WP2, research group T. Bugnyar, WP3, research group T. Fitch) is an important driving force in the Vienna Doctoral School CoBeNe. The development plan 2020 of the University of Vienna foresees a strengthening of the research areas Behavioral Biology and Neuroscience. With the award of the FWF’s third Doctoral College (DK) on “Cognition and Communication”, the next generation of researchers in the field of cognitive biology will be able to use the technologies developed in the project.
The project is another positive signal to increase international visibility by i) strengthening the research focus, ii) inter-university coordination/cooperation regarding acquisition/use of research equipment and networking, and iii) strengthening strategically important collaborations.

HAIDLHOF INFRASTRUCTURE
BMWFW, HRSM Ausschreibung 2013, funding period 2014-2018, University of Veterinary Medicine & University of Vienna: Thomas Bugnyar, Tecumseh Fitch, Ludwig Huber

Abstract of proposal

Cognitive biology has become a strong scientific focus in Vienna. The close collaboration between the University of Vienna and Vetmeduni Vienna has been instrumental in this development. A crucial component of the collaboration is the Haidlhof Research Station near Bad Vöslau, which has been jointly operated by the two universities since 2010 and for which a separate cooperation agreement has been signed for 10 years. The station is built and used by three renowned research groups around Professors Ludwig Huber (VetMeduni Vienna, Messerli Research Institute), Thomas Bugnyar and Tecumseh Fitch (both University of Vienna, Dept. of Cognitive Biology) together. For the construction of the facility, both universities invested the amount of 814.000,-, and from excellence third-party projects (ERC, START, FWF-DK) contributed about 150.000,- for the ongoing operation. The facility uniquely combines large flight aviaries and test rooms for corvids (ravens, crows) and keas (New Zealand mountain parrots), as well as a bioacoustics laboratory with video X-ray equipment for mammals and bird

The facility is also proving extremely attractive to international scientists and students. However, this has brought research groups to the limits of their capabilities (in terms of staff, experimental facilities, equipment, rooms, animal stock, and testing capabilities) more quickly than expected. Particularly aggravating is the extremely poor Internet connectivity. A sustainable increase in efficiency should be achieved by expanding and improving the personnel and spatial infrastructure at the research station.

In the area of administration, personnel is needed for the inter-university coordination of the expansion of the research station, including construction planning and construction supervision. This is to be achieved via the appointment of a Lab Manager (level IVa), limited to 3 years. A temporary project manager was also employed during the construction of the station and was critical for rapid and efficient implementation. For the implementation of a new, highly complex IT system including the creation of an e-government structure, an IT manager, limited to 3 years, is needed. Maintenance work beyond the term of the contract will be provided by the IT staff of the two universities or institutes. For the expansion and adaptation of the experimental laboratories (special test facilities), a technical specialist (level IIIa), limited to 3 years, is needed. Due to the planned expansion of the animal stock (development of the stock) in the direction of farm animals (pigs, chickens), the appointment of an additional animal keeper is indispensable for the project period in order to be able to guarantee species-appropriate animal husbandry and care.

In the area of infrastructure, new work and laboratory space has become indispensable due to the large number of project staff. The new rooms (a new office complex and two laboratories) are to be connected to the existing heating network/ring main. The test rooms (X-ray laboratory, sonic dead room) are also to be brought up to the latest technical standard. A high-performance Internet connection including a central server is particularly important.

The aim of the 3-year project is to implement a professional, sustainable structure in the area of administration (personnel), IT and infrastructure at the Haidlhof research station in order to be able to sustainably guarantee and expand already existing areas of excellence for both cooperation partners. An improvement of the technical infrastructure, such as high-performance internet connections, is indispensable in order to be able to survive in the scientific international competition. We expect an increased utilization of the research station of up to 50% in case of an expansion. This makes the establishment of an effective management structure indispensable. The construction work must be professionally supervised on site and the utilization and maintenance of the facility must be coordinated – independent of a university assignment. We assume that the measures taken will lead to an optimization of the facility within the specified period of 3 years and that no significant further follow-up costs will be incurred as a result.

Project to promote science education at the Haidlhof Research Station
Government of Lower Austria, Science ad Research, funding period 2015-2017, Thomas Bugnyar, Petra Pesak

Abstract of proposal

Cognitive biology has become a strong scientific focus in Austria. The close collaboration between the University of Vienna and the University of Veterinary Medicine Vienna has been instrumental in this development. A crucial component of this collaboration is the Haidlhof Research Station in the municipality of Bad Vöslau, which has been jointly operated by the two universities since 2010. The station is built and used by three renowned research groups of Ludwig Huber (VetMeduni Vienna, Messerli Research Institute), Thomas Bugnyar and Tecumseh Fitch (both University of Vienna, Department of Cognitive Biology).

Up to now, science education and science communication has only been carried out in an unstructured and incidental manner. Due to media interest and numerous requests from schools and private initiatives, this area is now to be raised to a professional level without burdening the ongoing scientific operations. It is the aim of a 3-year project to create a suitable visitor infrastructure and implementation of a professional science communication to strengthen the research location Haidlhof. Embedded in the association “Förderer des Haidlhofes”, which is currently being founded, it is necessary to create the necessary internal structures in the first year: Educational programs have to be worked out by pedagogues, employees have to be trained, information material has to be created. At the same time, it is necessary to initiate cooperations with scientific institutions (ornithological station, regional school board, pedagogical academy) and NGOs (Birdlife, WWF) on different levels. The common concern should be to identify target groups and to consider suitable measures, which will be worked out by the association and implemented at the research station. For this purpose, a visitor-friendly infrastructure shall be created (especially for people with disabilities), which does not restrict the daily research work. The creation of an outdoor “classroom” can offer such a possibility, as well as barrier-free routing and professional signage of the research facilities.
The project is to be embedded in the structure of the above-mentioned association and managed in close coordination with the professors primarily active at the Haidlhof. Manual work and maintenance should be carried out by a civilian servant (following the example of the KLF Konrad Lorenz Forschungsstelle Grünau). Guided tours and science education are to be carried out by trained students and young scientists against payment of a customary fee. With this project, internationally recognized scientists open their research facility to Lower Austrian schools and the interested public, thus contributing to the strengthening of Lower Austria as a center of knowledge.