Sensory collectives in natural systems.

Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a 'sensory collective'; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify 'sensescapes'. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution.

Disentangling influence over group speed and direction reveals multiple patterns of influence in moving meerkat groups.

Animals that travel together in groups must constantly come to consensus about both the direction and speed of movement, often simultaneously. Contributions to collective decisions may vary among group members, yet inferring who has influence over group decisions is challenging, largely due to the multifaceted nature of influence. Here we collected high-resolution GPS data from five habituated meerkat groups in their natural habitat during foraging and developed a method to quantify individual influence over both group direction and speed. We find that individual influence over direction and speed are correlated, but also exhibit substantial variation. Comparing patterns across social statuses reveals that dominant females have higher influence than other individuals over both group direction and speed. Individuals with high influence also tend to spend more time in the front of the group. We discuss our results in light of meerkat life-history and current literature on influence during group movement. Our method provides a general approach which can be applied to disentangle individual influence over group direction and speed in a wide range of species with cohesive movement, emphasizing the importance of integrating multiple lines of inquiry when inferring influence in moving animal groups.

Fast estimation of plant growth dynamics using deep neural networks.

BACKGROUND: In recent years, there has been an increase of interest in plant behaviour as represented by growth-driven responses. These are generally classified into nastic (internally driven) and tropic (environmentally driven) movements. Nastic movements include circumnutations, a circular movement of plant organs commonly associated with search and exploration, while tropisms refer to the directed growth of plant organs toward or away from environmental stimuli, such as light and gravity. Tracking these movements is therefore fundamental for the study of plant behaviour. Convolutional neural networks, as used for human and animal pose estimation, offer an interesting avenue for plant tracking. Here we adopted the Social LEAP Estimates Animal Poses (SLEAP) framework for plant tracking. We evaluated it on time-lapse videos of cases spanning a variety of parameters, such as: (i) organ types and imaging angles (e.g., top-view crown leaves vs. side-view shoots and roots), (ii) lighting conditions (full spectrum vs. IR), (iii) plant morphologies and scales (100 µm-scale Arabidopsis seedlings vs. cm-scale sunflowers and beans), and (iv) movement types (circumnutations, tropisms and twining). RESULTS: Overall, we found SLEAP to be accurate in tracking side views of shoots and roots, requiring only a low number of user-labelled frames for training. Top views of plant crowns made up of multiple leaves were found to be more challenging, due to the changing 2D morphology of leaves, and the occlusions of overlapping leaves. This required a larger number of labelled frames, and the choice of labelling "skeleton" had great impact on prediction accuracy, i.e., a more complex skeleton with fewer individuals (tracking individual plants) provided better results than a simpler skeleton with more individuals (tracking individual leaves). CONCLUSIONS: In all, these results suggest SLEAP is a robust and versatile tool for high-throughput automated tracking of plants, presenting a new avenue for research focusing on plant dynamics.

Signalling adjustments to direct and indirect environmental effects on signal perception in meerkats.

The efficiency of communication between animals is determined by the perception range of signals. With changes in the environment, signal transmission between a sender and a receiver can be influenced both directly, where the signal's propagation quality itself is affected, and indirectly where the senders or receivers' behaviour is impaired, impacting for example the distance between them. Here we investigated how meerkats (Suricata suricatta) in the Kalahari Desert adjust to these challenges in the context of maintaining group cohesion through contact calls. We found that meerkats changed their calling rate when signal transmission was affected indirectly due to increased dispersion of group members as during a drought, but not under typical wet conditions, when signal transmission was directly affected due to higher vegetation density. Instead under these wetter conditions, meerkats remained within proximity to each other. Overall, both direct and indirect environmental effects on signal perception resulted in an increased probability of groups splitting. In conclusion, we provide evidence that social animals can flexibly adjust their vocal coordination behaviour to cope with direct and indirect effects of the environment on signal perception, but these adjustments have limitations.

Long-term movements and home-range changes: Rapid territory shifts in meerkats.

Territoriality and stable home ranges are a common space-use pattern among animals. These ranges provide its inhabitants with important resources and thus favourable territories are associated with an increased fitness. While the role of territory quality and changes of territory ownership have often been investigated, the changes of territorial boundaries have been less studied. Here, we investigated space-use changes in a social mammal species, applying a novel analytical approach, calculating long-term dissimilarity in space use using distancematrices based on periodic utilization distributions. This approach makes it possible to identify different space-use patterns, which cannot be distinguished by only considering changes between consecutive time periods. We analysed meerkat (Suricata suricatta) movements of a total of 24 different groups over a 16-year period, resulting in 134 group years. We then correlated the identified home-range changes to life-history events and possible environmental drivers. Groups had stable territories for several years before they abandoned their home range mostly to move quickly to new areas where they again remained for several years. Of 26 identified sudden shifts, 22 occurred in the summer months and often involved distances larger than the original home-range size. Home-range movements that were close together in time were often also spatially clustered and moved in a similar direction. These shifts were often preceded by more frequent interactions between groups, but did not seem to be a product of direct displacements by other groups. The normalized difference vegetation index as a measure of food production and social factors such as dominance changes did not correlate to changes. Against our expectation space-use changes were not accumulations of small changes, but more often involved long-distance moves into unknown ranges. This means that the groups enter areas where they cannot profit from local knowledge. The methods used identify episodes of long stability alternated by sudden changes in meerkats and in general provides insight into long-term space use. Our methods can be used to analyse long-term space use, either within or across species.

The multilevel society of a small-brained bird.

Animal societies can be organised in multiple hierarchical tiers [1]. Such multilevel societies, where stable groups move together through the landscape, overlapping and associating preferentially with specific other groups, are thought to represent one of the most complex forms of social structure in vertebrates. For example, hamadryas baboons (Papio hamadryas) live in units consisting of one male and one or several females, or of several solitary males, that group into clans. These clans then come together with solitary bachelor males to form larger bands [2]. This social structure means that individuals have to track many different types of relationships at the same time [1,3]. Here, we provide detailed quantitative evidence for the presence of a multilevel society in a small-brained bird, the vulturine guineafowl (Acryllium vulturinum). We demonstrate that this species lives in large, multi-male, multi-female groups that associate preferentially with specific other groups, both during the day and at night-time communal roosts.

Group cohesion in foraging meerkats: follow the moving 'vocal hot spot'.

Group coordination, when 'on the move' or when visibility is low, is a challenge faced by many social living animals. While some animals manage to maintain cohesion solely through visual contact, the mechanism of group cohesion through other modes of communication, a necessity when visual contact is reduced, is not yet understood. Meerkats (Suricata suricatta), a small, social carnivore, forage as a cohesive group while moving continuously. While foraging, they frequently emit 'close calls', soft close-range contact calls. Variations in their call rates based on their local environment, coupled with individual movement, produce a dynamic acoustic landscape with a moving 'vocal hotspot' of the highest calling activity. We investigated whether meerkats follow such a vocal hotspot by playing back close calls of multiple individuals to foraging meerkats from the front and back edge of the group simultaneously. These two artificially induced vocal hotspots caused the group to spatially elongate and split into two subgroups. We conclude that meerkats use the emergent dynamic call pattern of the group to adjust their movement direction and maintain cohesion. Our study describes a highly flexible mechanism for the maintenance of group cohesion through vocal communication, for mobile species in habitats with low visibility and where movement decisions need to be adjusted continuously to changing environmental conditions.

Quarantine as a public health measure against an emerging infectious disease: syphilis in Zurich at the dawn of the modern era (1496-1585).

Syphilis is considered as one of the most devastating sexually transmitted diseases in human history. Based on historical records, the "Böse Blattern" (German for "Evil Pocks") spread through Europe after 1495 and shared symptoms with what we know today as syphilis. Many cities took measures to protect their population. Here, transliterations of archival documents from the 15(th) and 16(th) century (provided in the appendix) are used to trace the steps taken by the governing authorities in Zurich to deal with this emerging infectious disease. One of the central measures taken by the city was to establish a quarantine facility referred to as the "Blatternhaus". The city doctors, including the well-known physician and naturalist Conrad Gessner, oversaw the obligatory quarantine and treatment of patients with symptoms. Treatment could range from better nutrition, herbal remedies and skin ointments to aggressive heat therapy and "smoking". Furthermore, the affliction was suspected as a sexually acquired disease, hence prostitutes and infected foreigners were extradited from the city. Meanwhile, the church used its social influence to promote a more "Christian" behavior. In several respects, the public health measures taken in the 16(th) century against a new and menacing epidemic do not diverge in their basic rationale from approaches used during the 20(th) century and today.

Territoriality and home-range dynamics in meerkats, Suricata suricatta: a mechanistic modelling approach.

Multiple approaches exist to model patterns of space use across species, among them resource selection analysis, statistical home-range modelling and mechanistic movement modelling. Mechanistic home-range models combine the benefits of these approaches, describing emergent territorial patterns based on fine-scale individual- or group-movement rules and incorporating interactions with neighbours and the environment. These models have not, to date, been extended to dynamic contexts. Using mechanistic home-range models, we explore meerkat (Suricata suricatta) territorial patterns, considering scent marking, direct group interactions and habitat selection. We also extend the models to accommodate dynamic aspects of meerkat territoriality (territory development and territory shift). We fit models, representing multiple working hypotheses, to data from a long-term meerkat study in South Africa, and we compare models using Akaike's and Bayesian Information Criteria. Our results identify important features of meerkat territorial patterns. Notably, larger groups do not seem to control larger territories, and groups apparently prefer dune edges along a dry river bed. Our model extensions capture instances in which 1) a newly formed group interacts more strongly with its parent groups over time and 2) a group moves its territory core out of aversive habitat. This extends our mechanistic modelling framework in previously unexplored directions.

Renaissance model of an epidemic with quarantine.

Quarantine is one possible solution to limit the propagation of an emerging infectious disease. Typically, infected individuals are removed from the population by avoiding physical contact with healthy individuals. A key factor for the success of a quarantine strategy is the carrying capacity of the facility. This is often a known parameter, while other parameters such as those defining the population structure are more difficult to assess. Here we develop a model where we explicitly introduce the carrying capacity of the quarantine facility into a susceptible-infected-recovered (SIR) framework. We show how the model can address the propagation and control of contact and sexually transmitted infections. We illustrate this by a case study of the city of Zurich during the 16th century, when it had to face an epidemic of syphilis. After Swiss mercenaries came back from a war in Naples in 1495, the authorities of the city addressed subsequent epidemics by, among others, placing infected members of the population in quarantine. Our results suggest that a modestly sized quarantine facility can successfully prevent or reduce an epidemic. However, false detection can present a real impediment for this solution. Indiscriminate quarantine of individuals can lead to the overfilling of the facility, and prevent the intake of infected individuals. This results in the failure of the quarantine policy. Hence, improving the rate of true over false detection becomes the key factor for quarantine strategies. Moreover, in the case of sexually transmitted infections, asymmetries in the male to female ratio, and the force of infection pertaining to each sex and class of sexual encounter can alter the effectiveness of quarantine measures. For example, a heterosexually transmitted disease that mainly affects one sex is harder to control in a population with more individuals of the opposite sex. Hence an imbalance in the sex ratios as seen in situations such as mining colonies, or populations at war, can present impediments for the success of quarantine policies.