Timothy M. Schaerf

Inferring the rules of interaction of shoaling fish

Collective motion, where large numbers of individuals move synchronously together, is achieved when individuals adopt interaction rules that determine how they respond to their neighbors’ movements and positions. These rules determine how group-living animals move, make decisions, and transmit information between individuals. Nonetheless, few studies have explicitly determined these interaction rules in moving groups, and very little is known about the interaction rules of fish. Here, we identify three key rules for the social interactions of mosquitofish (Gambusia holbrooki): (i) Attraction forces are important in maintaining group cohesion, while we find only weak evidence that fish align with their neighbor’s orientation; (ii) repulsion is mediated principally by changes in speed; (iii) although the positions and directions of all shoal members are highly correlated, individuals only respond to their single nearest neighbor. The last two of these rules are different from the classical models of collective animal motion, raising new questions about how fish and other animals self-organize on the move.

Deciding on the wing: in-flight decision making and search space sampling in the red dwarf honeybee Apis florea

During reproductive swarming and seasonal migration, a honeybee swarm needs to locate and move to a new, suitable nest site. While the nest-site selection process in cavity-nesting species such as the European honeybee Apis mellifera is very precise with the swarm carefully selecting a single site, open-nesting species, such as Apis florea, lack such precision. These differences in precision in the nest-site selection process are thought to arise from the differing nest-site requirements of open- and cavity-nesting species. While A. florea can nest on almost any tree, A. mellifera is constrained by the scarcity of suitable nest sites. Here we show that imprecision in the nest-site selection process allows swarms to quickly reach a decision when many nest sites are available. In contrast, a very precise nest-site selection process slows down the decision-making process when nest sites are abundant.Nest-site selection in A. florea appears to be more similar to search-space sampling than to a decision-making process. Bees appear to scout the environment for general areas in which potential nest sites are abundant. Bees involved in searching the environment for suitable nest sites are also involved in guiding the swarm once the decision to depart has been made. Generally A. florea swarms exhibit a lack of consensus in the direction indicated by dancers prior to take-off. Because of this lack of consensus a swarm of A. florea will need to determine its exact direction of travel while in flight. We show that in the absence of directional consensus a swarm of bees can still be guided towards an area containing suitable nest sites provided directional dissent is not too great and nest sites are abundant. However, if the swarm needs to move to a very specific location (a single point in space), directional dissent should be avoided, resulting in a more lengthy decision-making process prior to departure. We further show that the guidance mechanism of bee swarms, so-called ‘streaking’, functions both when directional dissent is present and when it is absent, making it a more general mechanism of group movement than previously thought.

Moving home: nest-site selection in the Red Dwarf honeybee (Apis florea)

The Red Dwarf honeybee (Apis florea) is one of two basal species in the genus Apis. A. florea differs from the well-studied Western Hive bee (Apis mellifera) in that it nests in the open rather than in cavities. This fundamental difference in nesting biology is likely to have implications for nest-site selection, the process by which a reproductive swarm selects a new site to live in. In A. mellifera, workers show a series of characteristic behaviors that allow the swarm to select the best nest site possible. Here, we describe the behavior of individual A. florea workers during the process of nest-site selection and show that it differs from that seen in A. mellifera. We analyzed a total of 1,459 waggle dances performed by 197 scouts in five separate swarms. Our results suggest that two fundamental aspects of the behavior of A. mellifera scouts—the process of dance decay and the process of repeated nest site evaluation—do not occur in A. florea. We also found that the piping signal used by A. mellifera scouts to signal that a quorum has been reached at the chosen site, is performed by both dancing and non-dancing bees in A. florea. Thus, the piping signal appears to serve a different purpose in A. florea. Our results illustrate how differences in nesting biology affect the behavior of individual bees during the nest-site selection process.

Selection against heteroplasmy explains the evolution of uniparental inheritance of mitochondria.

Why are mitochondria almost always inherited from one parent during sexual reproduction? Current explanations for this evolutionary mystery include conflict avoidance between the nuclear and mitochondrial genomes, clearing of deleterious mutations, and optimization of mitochondrial-nuclear coadaptation. Mathematical models, however, fail to show that uniparental inheritance can replace biparental inheritance under any existing hypothesis. Recent empirical evidence indicates that mixing two different but normal mitochondrial haplotypes within a cell (heteroplasmy) can cause cell and organism dysfunction. Using a mathematical model, we test if selection against heteroplasmy can lead to the evolution of uniparental inheritance. When we assume selection against heteroplasmy and mutations are neither advantageous nor deleterious (neutral mutations), uniparental inheritance replaces biparental inheritance for all tested parameter values. When heteroplasmy involves mutations that are advantageous or deleterious (non-neutral mutations), uniparental inheritance can still replace biparental inheritance. We show that uniparental inheritance can evolve with or without pre-existing mating types. Finally, we show that selection against heteroplasmy can explain why some organisms deviate from strict uniparental inheritance. Thus, we suggest that selection against heteroplasmy explains the evolution of uniparental inheritance.

Do small swarms have an advantage when house hunting? The effect of swarm size on nest-site selection by Apis mellifera

Reproductive swarms of honeybees are faced with the problem of finding a good site to establish a new colony. We examined the potential effects of swarm size on the quality of nest-site choice through a combination of modelling and field experiments. We used an individual-based model to examine the effects of swarm size on decision accuracy under the assumption that the number of bees actively involved in the decision-making process (scouts) is an increasing function of swarm size. We found that the ability of a swarm to choose the best of two nest sites decreases as swarm size increases when there is some time-lag between discovering the sites, consistent with Janson & Beekman (Janson & Beekman 2007 Proceedings of European Conference on Complex Systems, pp. 204–211.). However, when simulated swarms were faced with a realistic problem of choosing between many nest sites discoverable at all times, larger swarms were more accurate in their decisions than smaller swarms owing to their ability to discover nest sites more rapidly. Our experimental fieldwork showed that large swarms invest a larger number of scouts into the decision-making process than smaller swarms. Preliminary analysis of waggle dances from experimental swarms also suggested that large swarms could indeed discover and advertise nest sites at a faster rate than small swarms.

The effect of hunger on the exploratory behaviour of shoals of mosquitofish Gambusia holbrooki

The question of how hunger affects locomotory behaviour, in particular how it affects the kinematics of movement and an animal’s interaction with the physical structures in its environment is of broad relevance in behavioural ecology. We experimentally manipulated the hunger levels of individual mosquitofish ( Gambusia holbrooki ) and recorded their swimming behaviour in shoals of 4 fish. We found that hungry individuals in shoals moved at greater speeds and had higher turning speeds than satiated individuals in shoals, as well as a greater variance in speed and turning speeds. We also found that hungry individuals explored more of the arena and used more of its internal space, away from the square arena’s walls and displayed less wall-following behaviour than satiated individuals. A functional explanation for this change in swimming behaviour and interaction with environmental heterogeneity is discussed in the context of social foraging, as is the consequence of these results for models of search patterns and collective movement.

The influence of nutritional state on individual and group movement behaviour in shoals of crimson-spotted rainbowfish ( Melanotaenia duboulayi )

Groups of animals are often heterogeneously structured and may be composed of selfish individuals responding to different internal stimuli. Group-level behaviour can be determined by the slight differences in simple behavioural movement parameters structuring local interactions between conspecifics. To accurately understand individual behaviour within groups and how it affects whole-group behaviour, we need to measure the responses of individuals in groups to changes in internal state and examine the outcome of these responses within the social context. Therefore, we quantified the influence of nutritional state on the individual and group movement parameters of free swimming shoals of eight rainbow fish, Melanotaenia duboulayi. Individual fish were experimentally manipulated to be in one of two nutritional states, hungry or satiated, and were assayed in three group compositions: all-hungry (8:0 hungry/satiated), mixed (4:4) or all-satiated (0:8). We showed that the internal nutritional state of individual fish affected basic behaviours relating to spatial positioning. The interaction between pairs of fish was dependent on the nutritional state of both fish, and there was an additive effect of individual behaviour on group behaviour, which meant that group behaviour reflected the motivations of its individual members in such a way that allowed individuals to fulfil their own behavioural needs whilst still attaining the benefits of grouping.

The effects of external cues on individual and collective behavior of shoaling fish

We examine changes in interaction rules, predictability, and vigilance of x-ray tetras due to external food and alarm cues. Collective animal behavior is an emergent phenomenon arising from the local interactions of the members of animal groups. Considerable progress has been made in characterizing these interactions, particularly inferring rules that shape and guide the responses of animals to their near neighbors. To date, experimental work has focused on collective behavior within a single, stable context. We examine the individual and collective behavior of a schooling fish species, the x-ray tetra (Pristella maxillaris), identifying their response to changes in context produced by food cues or conspecific alarm cues. Fish exposed to alarm cues show pronounced, broad-ranging changes of behavior, including reducing speed and predictability in their movements. Alarmed fish also alter their responses to other group members, including enacting a smaller zone of repulsion and increasing their frequency of observation of, and responsiveness to, near neighbors. Fish subject to food cues increased speed as a function of neighbor positions and reduced encounter frequency with near neighbors. Overall, changes in individual behavior and the interactions among individuals in response to external cues coincide with changes in group-level patterns, providing insight into the adaptability of behavior to changes in context and interrelationship between local interactions and global patterns in collective behavior.

Crimson Spotted Rainbowfish (Melanotaenia duboulayi) Change Their Spatial Position according to Nutritional Requirement.

Decision making in moving animal groups has been shown to be disproportionately influenced by individuals at the front of groups. Therefore, an explanation of state-dependent positioning of individuals within animal groups may provide a mechanism for group movement decisions. Nutritional state is dynamic and can differ between members of the same group. It is also known to drive animal movement decisions. Therefore, we assayed 6 groups of 8 rainbowfish foraging in a flow tank. Half of the fish had been starved for 24h and half had been fed 1h prior to experimental start. Groups were assayed again one week later but individuals were allocated to the opposite nutritional treatment. During the assay the positions of individually identified fish were recorded as were the number of food items they each ate and the position within the group they acquired them from. Food-deprived fish were more often found towards the front of the shoal; the mean weighted positional score of food-deprived fish was significantly larger than that of well-fed fish. Individuals were not consistent in their position within a shoal between treatments. There was a significant positive correlation between mean weighted positional score and number of food items acquired which displays an obvious benefit to front positions. These results suggest that positional preferences are based on nutritional state and provide a mechanism for state-dependent influence on group decision-making as well as increasing our understanding of what factors are important for group functioning.

Local interactions and global properties of wild, free-ranging stickleback shoals

Collective motion describes the global properties of moving groups of animals and the self-organized, coordinated patterns of individual behaviour that produce them. We examined the group-level patterns and local interactions between individuals in wild, free-ranging shoals of three-spine sticklebacks, Gasterosteus aculeatus. Our data reveal that the highest frequencies of near-neighbour encounters occur at between one and two body lengths from a focal fish, with the peak frequency alongside a focal individual. Fish also show the highest alignment with these laterally placed individuals, and generally with animals in front of themselves. Furthermore, fish are more closely matched in size, speed and orientation to their near neighbours than to more distant neighbours, indicating local organization within groups. Among the group-level properties reported here, we find that polarization is strongly influenced by group speed, but also the variation in speed among individuals and the nearest neighbour distances of group members. While we find no relationship between group order and group size, we do find that larger groups tend to have lower nearest neighbour distances, which in turn may be important in maintaining group order.