Self-organized fish schools: an examination of emergent properties

Heterogeneous, "aggregated" patterns in the spatial distributions of individuals are almost universal across living organisms, from bacteria to higher vertebrates. Whereas specific features of aggregations are often visually striking to human eyes, a heuristic analysis based on human vision is usually not sufficient to answer fundamental questions about how and why organisms aggregate. What are the individual-level behavioral traits that give rise to these features? When qualitatively similar spatial patterns arise from purely physical mechanisms, are these patterns in organisms biologically significant, or are they simply epiphenomena that are likely characteristics of any set of interacting autonomous individuals? If specific features of spatial aggregations do confer advantages or disadvantages in the fitness of group members, how has evolution operated to shape individual behavior in balancing costs and benefits at the individual and group levels? Mathematical models of social behaviors such as schooling in fishes provide a promising avenue to address some of these questions. However, the literature on schooling models has lacked a common framework to objectively and quantitatively characterize relationships between individual-level behaviors and group-level patterns. In this paper, we briefly survey similarities and differences in behavioral algorithms and aggregation statistics among existing schooling models. We present preliminary results of our efforts to develop a modeling framework that synthesizes much of this previous work, and to identify relationships between behavioral parameters and group-level statistics.     

Mate search and aggregation behaviour in the Galician hybrid zone of Littorina saxatilis

In Galician rocky shores two ecotypes of the snail L. saxatilis can be found in sympatry. A ridged and banded ecotype (RB-morph) and a smooth and unbanded ecotype (SU-morph) overlap in midshore with the production of some hybrids. The distinct morphs mate assortatively and there is evidence of a partial reproductive barrier between them. This sexual isolation is caused by a nonrandom microdistribution and mate choice behaviour. Mucus trail-following, movement rate and aggregation behaviour were studied to determine their roles in the mating behaviour and sexual isolation of this species. Morph-specific mucus trail-following could not, in our experiments, explain either of these two processes. The reasons for the aggregation of morphs were investigated by Monte Carlo simulations of data from natural populations, which showed that size aggregation (refuge sizes fit different sized morphs differently) could explain only about 36% of the morph aggregation in adult snails. In the laboratory, morph aggregation was still present, and simulations suggested that size aggregation was the possible explanation. Thus, morph aggregation in Galician L. saxatilis has to be explained also by other causes in addition to size aggregation. These may be a combination of contrasting preferences for barnacle and mussel patches in the two morphs, and possibly longer copulation and pair formation time with similar sized snails of the same morph. Thus aggregation behaviour, but not trail-following, contributes to incipient reproductive isolation and perhaps sympatric speciation in Galician L. saxatilis populations.     

Emergence of self-organised oscillatory domains in fungal mycelia

Fungi play a central role in the nutrient cycles of boreal and temperate forests. In these biomes, the saprotrophic wood-decay fungi are the only organisms that can completely decompose woody plant litter. In particular, cord-forming basidiomycete fungi form extensive mycelial networks that scavenge scarce mineral nutrients and translocate them over long distances to exploit new food resources. Despite the importance of resource allocation, there is limited information on nutrient dynamics in these networks, particularly for nitrogen, as there is no suitable radioisotope available. We have mapped N-translocation using photon-counting scintillation imaging of the non-metabolised amino acid analogue, (14)C-aminoisobutyrate. We describe a number of novel phenomena, including rapid, preferential N-resource allocation to C-rich sinks, induction of simultaneous bi-directional N-transport, abrupt switching between different pre-existing transport routes, and emergence of locally synchronised, oscillatory phase domains. It is possible that such self-organised oscillatory behaviour is a mechanism to achieve global co-ordination in the mycelium.     

Insights on bias and information in group-level studies

Ecological and aggregate data studies are examples of group-level studies. Even though the link between the predictors and outcomes is not preserved in these studies, inference about individual-level exposure effects is often a goal. The disconnection between the level of inference and the level of analysis expands the array of potential biases that can invalidate the inference from group-level studies. While several sources of bias, specifically due to measurement error and confounding, may be more complex in group-level studies, two sources of bias, cross-level and model specification bias, are a direct consequence of the disconnection. With the goal of aligning inference from individual versus group-level studies, I discuss the interplay between exposure and study design. I specify the additional assumptions necessary for valid inference, specifically that the between- and within-group exposure effects are equal. Then cross-level inference is possible. However, all the information in the group-level analysis comes from between-group comparisons. Models where the group-level analysis provides even a small percentage of information about the within-group exposure effect are most susceptible to model specification bias. Model specification bias can be even more serious when the group-level model isn't derived from an individual-level model.     

Prey-induced changes to a predator's behaviour and morphology: Implications for shell-claw covariance in the northwest Atlantic

Whereas many plasticity studies demonstrate the importance of inducible defences among prey, far fewer investigate the potential role of inducible offences among predators. Here we ask if natural differences in a snail's shell hardness can induce developmental changes to a predatory crab's claw size. To do this, we fed Littorina obtusata snails from either thick- or thin-shelled populations to captive European green crabs Carcinus maenas. The crabs' shell-breaking behaviour dominated among those fed thin-shelled snails, whereas crabs fed thick-shelled snails mostly winkled flesh through the shell opening without damaging the shell itself (a.k.a. aperture-probing behaviour). Significantly, the size of crab crusher claws grew in proportion to the frequency of shell-crushing behaviour and, for a same shell-crushing frequency, crabs fed thick-shelled snails grew larger crusher claws than those fed thin-shelled snails after two experimental moults. Diet and behaviour had no effect on the growth of the smaller cutter claws of same individuals, providing good evidence that allometric changes to crusher claws were indeed a result of differential use while feeding. Findings indicate that both predation habits and claw sizes are affected by green crabs' diet, supporting the hypothesis that prey-induced phenotypic plasticity contributes to earlier accounts of shell-claw covariance between this predator and its Littorina prey in the wild.     

Collective predator evasion: Putting the criticality hypothesis to the test

According to the criticality hypothesis, collective biological systems should operate in a special parameter region, close to so-called critical points, where the collective behavior undergoes a qualitative change between different dynamical regimes. Critical systems exhibit unique properties, which may benefit collective information processing such as maximal responsiveness to external stimuli. Besides neuronal and gene-regulatory networks, recent empirical data suggests that also animal collectives may be examples of self-organized critical systems. However, open questions about self-organization mechanisms in animal groups remain: Evolutionary adaptation towards a group-level optimum (group-level selection), implicitly assumed in the “criticality hypothesis”, appears in general not reasonable for fission-fusion groups composed of non-related individuals. Furthermore, previous theoretical work relies on non-spatial models, which ignore potentially important self-organization and spatial sorting effects. Using a generic, spatially-explicit model of schooling prey being attacked by a predator, we show first that schools operating at criticality perform best. However, this is not due to optimal response of the prey to the predator, as suggested by the “criticality hypothesis”, but rather due to the spatial structure of the prey school at criticality. Secondly, by investigating individual-level evolution, we show that strong spatial self-sorting effects at the critical point lead to strong selection gradients, and make it an evolutionary unstable state. Our results demonstrate the decisive role of spatio-temporal phenomena in collective behavior, and that individual-level selection is in general not a viable mechanism for self-tuning of unrelated animal groups towards criticality.     

Individual-level personality influences social foraging and collective behaviour in wild birds

There is increasing evidence that animal groups can maintain coordinated behaviour and make collective decisions based on simple interaction rules. Effective collective action may be further facilitated by individual variation within groups, particularly through leader–follower polymorphisms. Recent studies have suggested that individual-level personality traits influence the degree to which individuals use social information, are attracted to conspecifics, or act as leaders/followers. However, evidence is equivocal and largely limited to laboratory studies. We use an automated data-collection system to conduct an experiment testing the relationship between personality and collective decision-making in the wild. First, we report that foraging flocks of great tits (Parus major) show strikingly synchronous behaviour. A predictive model of collective decision-making replicates patterns well, suggesting simple interaction rules are sufficient to explain the observed social behaviour. Second, within groups, individuals with more reactive personalities behave more collectively, moving to within-flock areas of higher density. By contrast, proactive individuals tend to move to and feed at spatial periphery of flocks. Finally, comparing alternative simulations of flocking with empirical data, we demonstrate that variation in personality promotes within-patch movement while maintaining group cohesion. Our results illustrate the importance of incorporating individual variability in models of social behaviour.     

Mechanisms of adaption to salinity stress in marine gastropods <Emphasis Type="Italic">Littorina saxatilis</Emphasis>: a proteomic analysis

Salinity is one of the most important abiotic environmental factors for marine animals. If salinity deviates from optimum, adaptive mechanisms switch on to maintain organism’s physiological activity. In this study the proteome of the marine snails Littorina saxatilis from natural habitats (12, 23 and 32‰ and in response to experimental salinity decreasing (from 20‰ to 10‰) was analyzed. The isolation of all snails inside their shells and gradually declining mortality was observed under an acute experimental salinity decrease. Proteomic changes were evaluated in the survived experimental mollusks compared to control individuals using differential 2D gel-electrophoresis (DIGE) and subsequent LC-MS/MS-identification of proteins. Approximately 10% of analyzed proteins underwent upor down regulation during the experiment. Proteins of folding, antioxidant response, intercellular matrix, and metabolic enzymes were identified among them. Proteomic changes observed in experimental hypoosmotic stress partially reproduced in the proteomes of molluscs that live in conditions of natural freshening (estuaries). Possible mechanisms involved in the adaptation process of L. saxatilis individuals to hypoosmotic stress are discussed.     

Altered behavior of the snail Biomphalaria glabrata as a result of infection with Schistosoma mansoni

In this comparative behavioral study, the effect of infection with Schistosoma mansoni on its snail intermediate host Biomphalaria glabrata was investigated. Three groups of snails were compared for their activity: (1) uninfected, (2) infected with male parasites, and (3) infected with female parasites. In solitary movement trials, uninfected snails traveled greater distances at faster rates, explored more surface area, and had shorter rest periods than snails infected with either male or female schistosomes. In Y-maze experiments designed to determine attraction, the uninfected snails more often and more quickly moved toward other snails than the infected individuals. Snails from all 3 groups were more attracted to infected individuals than to uninfected ones. There was no difference in attraction toward snails infected with male or female parasites. These experiments provide evidence that behavioral alterations as a result of infection may lead to aggregation of infected snails in the field. We propose that such an effect may result in enhanced parasite transmission.     

Social Aggregation in Pea Aphids: Experiment and Random Walk Modeling

From bird flocks to fish schools and ungulate herds to insect swarms, social biological aggregations are found across the natural world. An ongoing challenge in the mathematical modeling of aggregations is to strengthen the connection between models and biological data by quantifying the rules that individuals follow. We model aggregation of the pea aphid, Acyrthosiphon pisum. Specifically, we conduct experiments to track the motion of aphids walking in a featureless circular arena in order to deduce individual-level rules. We observe that each aphid transitions stochastically between a moving and a stationary state. Moving aphids follow a correlated random walk. The probabilities of motion state transitions, as well as the random walk parameters, depend strongly on distance to an aphid''s nearest neighbor. For large nearest neighbor distances, when an aphid is essentially isolated, its motion is ballistic with aphids moving faster, turning less, and being less likely to stop. In contrast, for short nearest neighbor distances, aphids move more slowly, turn more, and are more likely to become stationary; this behavior constitutes an aggregation mechanism. From the experimental data, we estimate the state transition probabilities and correlated random walk parameters as a function of nearest neighbor distance. With the individual-level model established, we assess whether it reproduces the macroscopic patterns of movement at the group level. To do so, we consider three distributions, namely distance to nearest neighbor, angle to nearest neighbor, and percentage of population moving at any given time. For each of these three distributions, we compare our experimental data to the output of numerical simulations of our nearest neighbor model, and of a control model in which aphids do not interact socially. Our stochastic, social nearest neighbor model reproduces salient features of the experimental data that are not captured by the control.     

Resilience of Self-Organised and Top-Down Planned Cities—A Case Study on London and Beijing Street Networks

The success or failure of the street network depends on its reliability. In this article, using resilience analysis, the author studies how the shape and appearance of street networks in self-organised and top-down planned cities influences urban transport. Considering London and Beijing as proxies for self-organised and top-down planned cities, the structural properties of London and Beijing networks first are investigated based on their primal and dual representations of planar graphs. The robustness of street networks then is evaluated in primal space and dual space by deactivating road links under random and intentional attack scenarios. The results show that the reliability of London street network differs from that of Beijing, which seems to rely more on its architecture and connectivity. It is found that top-down planned Beijing with its higher average degree in the dual space and assortativity in the primal space is more robust than self-organised London using the measures of maximum and second largest cluster size and network efficiency. The article offers an insight, from a network perspective, into the reliability of street patterns in self-organised and top-down planned city systems.     

Intrinsic differences in dispersal between populations of gastropods separated by a few metres: Evidence from reciprocal experimental transplantation

Differences between populations in dispersive behaviour can strongly influence population and community structure and have important implications for evolution. Differences in dispersal can be caused by intrinsic differences among populations or by different extrinsic cues. In a semi exposed shore in Co. Wicklow, Ireland, intertidal gastropods, Littorina littorea moved long distances in areas with low natural population density compared to areas with high natural density but were not influenced by density per se. A reciprocal experimental transplantation distinguished between intrinsic and extrinsic factors as causes of differences in dispersive behaviour. Snails from the area of high density were transplanted to the area of low density and vice versa. Comparisons were also carried out with controls (disturbed and undisturbed individuals) in each area. Dispersal of transplanted snails was compared with that of snails translocated within each area. Mean distances displaced and percentage dispersal were monitored after two days period. To test temporal generality the experiment was done twice. The two experiments yielded different outcomes. The majority of evidence supported the intrinsic model: transplanted snails dispersed differently from controls in their new area and similarly to controls in their area of origin. However, in one of the experiments there was some evidence suggesting influence of extrinsic factors or an interaction between extrinsic and intrinsic factors. Further research is required to identify whether the observed intrinsic differences are genetic or due to internal conditions that have been modified by the animal's present and/or past environment. This study reinforces the value of repeated experimental transplantation to characterize factors causing differences in behaviour.     

Levels of selection, altruism, and primate behavior.

Altruistic behaviors seem anomalous from a traditional view of Darwinian natural selection, and evolutionary explanations for them have generated much discussion. The debate centers around four major explanations: classic individual-level selection, reciprocity and game theory, kin selection, and trait-group selection. The historical context and defining criteria of each model must be reviewed before its validity can be assessed. Of these proposed mechanisms, group selection historically has been the most controversial. Although the extent to which empirical data support group selection hypotheses is uncertain, there is evidence for group-level selection among avirulent virus strains and foraging ant queens. Researchers studying mammalian behavior, particularly primatologists, have largely dismissed models of group-level selection. Most discussion of altruism among primates has focused on differences in fitness among individuals within a single group, but students of altruistic behaviors exhibited by primates also need to investigate intergroup variation with respect to these behaviors. Various altruistic behaviors are likely to have evolved through different forms of selection, and each example of apparent altruism therefore needs to be evaluated separately.     

Effects of pyrrolizidine alkaloids and sesquiterpenes on snail feeding

Summary We determined in the laboratory the feeding response of two populations of the generalist herbivorous snail Arianta arbustorum (Helicidae) towards the composite Adenostyles alliariae and towards various allelochemicals. These were: a pyrrolizidine alkaloid (PA) extract of Adenostyles leaves; senecionine (a PA present in Adenostyles); retrorsine (a PA not present in Adenostyles) and two sesquiterpene (ST) fractions from Adenostyles: a mixture of the STs adenostylone and neoadenostylone, and deacyladenostylone. Tertiary PAs and PA N-oxides were tested separately. For each allelochemical, we tested whether it was deterrent or whether it induced changes of feeding behaviour (i.e. whether it had pre- or postingestive effects), and whether the effects were more pronounced with younger (smaller) snails. The tertiary PA extract from Adenostyles was deterrent, especially for young snails, but did not induce changes of feeding behaviour. Tertiary PA senecionine was deterrent for young snails only and induced changes of feeding behaviour. Also, consumption of untreated Petasites was higher after this treatment. Tertiary PA retrorsine was not deterrent, but induced changes of feeding behaviour. The PA N-oxides showed no activity against the snails. The mixture of adenostylone and neoadenostylone was deterrent and induced feeding aversions. Deacyladenostylone was highly deterrent, but did not induce changes of feeding behaviour. At the Jura site, PA content of Adenostyles was lower than at the Black Forest site. The snails from Jura consumed much less Adenostyles than the snails from Black Forest, and also ate a little less of the treated leaf discs. The PAs which are encountered by the snails in their natural food plants (PA extract and senecionine) were more deterrent than retrorsine (a novel compound). This suggests that the snails have mechanisms for the rejection of allelochemicals which they encounter in their natural food plants, but not for novel allelochemicals. The results suggest two hypotheses regarding the function of the allelochemicals in Adenostyles: (1) The allelochemicals act mainly on very young snails. (2) PAs render Adenostyles toxic, while STs act as feeding deterrents.     

Adaptive site selection rules and variation in group size of barn swallows: individual decisions predict population patterns

Variation in group size is ubiquitous among socially breeding organisms. An alternative to the traditional examination of average reproductive success in groups of different sizes is to examine individual decision making by determining the cues used for site selection. Once factors used for decision making are known, one can determine whether group-level patterns, such as group size variation, are emergent properties of individual-level decision rules. The advantage of this alternative approach is that it can explain the distribution of group sizes rather than just the occurrence of optimal group sizes. Using barn swallows, I tested, but did not support, the hypothesis that individuals settle at sites based on the previous success of conspecifics (i.e., performance-based conspecific attraction). Instead, I demonstrate that an adaptive site selection decision rule--to breed where it is possible to reuse previously constructed nests--predicts 83% of the variation in the number of breeding pairs at a site. Furthermore, experimental nest removals demonstrated that settlement decisions are also strongly influenced by site familiarity. I discuss the interaction of the cue-based site selection rule with the occurrence of site fidelity and how, more generally, a consideration of individual-level decision rules can improve our understanding of variation in many social behaviors.     

Aggregation as an antipredator strategy in the rock-paper-scissors model

We study a nonhierarchical tritrophic system, whose predator-prey interactions are described by the rock-paper-scissors game rules. In our stochastic simulations, individuals may move strategically towards the direction with more conspecifics to form clumps instead of moving aimlessly on the lattice. Considering that the conditioning to move gregariously depends on the organism's physical and cognitive abilities, we introduce a maximum distance an individual can perceive the environment and a minimum conditioning level to perform the gregarious movement. We investigate the pattern formation and compute the average size of the single-species spatial domains emerging from the grouping behaviour. The results reveal that the defence tactic reduces the predation risk significantly, being more profitable if individuals perceive further distances, thus creating bigger groups. Our outcomes show that the species with more conditioned organisms dominate the cyclic spatial game, controlling most of the territory. On the other hand, the species with fewer individuals ready to perform aggregation strategy gives its predator the chance to fill the more significant fraction of the grid. The spatial interactions assumed in our numerical experiments constitute a data set that may help biologists and data scientists understand how local interactions influence ecosystem dynamics.     

An experimental investigation of the behaviour and mortality of artificial and natural morphs of Cepaea nemoralis (L.)

Two population cage experiments which examined the mortality and behaviour of artificial and natural morphs of the landsnail C. nemoralis ( L .) are described. In the first experiment artificial 'morphs' were manufactured from one genetically homogeneous founder group of snails by painting the shells black or white. Differences in behaviour and mortality between these two 'morphs' were observed during the course of the experiment. Daylight and weather conditions were important in determining the activity patterns of the two types of snail.
In the second experiment naturally occurring brown and yellow colour morphs were used. These exhibited very similar behaviour patterns to those of their artificial 'mimics' and it is concluded that phenotype must play an important role in determining the behavioural responses of the snails to their environment. Thermal relationships are suggested as causal factors for the differences between the experimental morphs.     

The principles of collective animal behaviour

In recent years, the concept of self-organization has been used to understand collective behaviour of animals. The central tenet of self-organization is that simple repeated interactions between individuals can produce complex adaptive patterns at the level of the group. Inspiration comes from patterns seen in physical systems, such as spiralling chemical waves, which arise without complexity at the level of the individual units of which the system is composed. The suggestion is that biological structures such as termite mounds, ant trail networks and even human crowds can be explained in terms of repeated interactions between the animals and their environment, without invoking individual complexity. Here, I review cases in which the self-organization approach has been successful in explaining collective behaviour of animal groups and societies. Ant pheromone trail networks, aggregation of cockroaches, the applause of opera audiences and the migration of fish schools have all been accurately described in terms of individuals following simple sets of rules. Unlike the simple units composing physical systems, however, animals are themselves complex entities, and other examples of collective behaviour, such as honey bee foraging with its myriad of dance signals and behavioural cues, cannot be fully understood in terms of simple individuals alone. I argue that the key to understanding collective behaviour lies in identifying the principles of the behavioural algorithms followed by individual animals and of how information flows between the animals. These principles, such as positive feedback, response thresholds and individual integrity, are repeatedly observed in very different animal societies. The future of collective behaviour research lies in classifying these principles, establishing the properties they produce at a group level and asking why they have evolved in so many different and distinct natural systems. Ultimately, this research could inform not only our understanding of animal societies, but also the principles by which we organize our own society.     

Dispersal and upstream migration of an amphidromous neritid snail: implications for restoring migratory pathways in tropical streams

1. The amphidromous life cycle of several species of neritid snails, shrimp and gobies throughout the tropics includes juveniles that migrate from the ocean to breed in fresh water. In many Hawaiian streams, the decline of Neritina granosa, an endemic gastropod, has been associated with habitat degradation and water withdrawal, which are common factors affecting tropical rivers around the world. 2. We investigated the effects of water withdrawal and density on dispersal and upstream migration of N. granosa using three experimental treatments: (i) reduced flow (RF) owing to a stream diversion, (ii) natural flow (NF) and (iii) natural flow with artificially increased snail density. For each treatment, snails were differentially tagged and released in a stream without a natural, extant population of N. granosa. 3. Capture rates ranged from 17 to 65% over a 63‐day period following release. Captures on 2–6 days after release measured initial dispersal and migration, whereas longer‐term migration rates were calculated from snails captured 16–63 days after release. Snails under NF displayed positive rheotactic behaviour, with only 3–12% demonstrating initial downstream movement. Under RF, 22–77% of snails moved downstream or showed no bias either way. 4. Initial mean upstream migration rate (UMR) was 0.25, 0.66 and 1.16 m day^?1 under RF, NF and natural flow with increased snail density, respectively. Longer‐term migration rates did not differ significantly between treatments, and the overall mean was 0.62 m day^?1. 5. Principal component analysis and generalised linear models were used to identify habitat characteristics important to UMR, with habitat and reach‐scale hydraulics as the most important factors. The relationship between discharge and UMR suggested it would take 11–35 years for snails to migrate past the most upstream water diversion. However, rates from published studies of neritid snail species migrating en masse or in long lines under natural situations suggested that N. granosa could migrate above stream diversions within 72 days–2.5 years (when in an aggregation) and 29 days–1.1 years (when following in long lines of individuals). 6. An understanding of upstream neritid snail migration can be used for the management and conservation of this and other migratory species in tropical streams.     

Natural selection by avian predators on size and colour of a freshwater snail (Pomacea flagellatd)

We identify two avian predators of the Neotropical apple snail, Pomaceaflagellata, and estimate the strength, direction and form of multivariate natural selection by these predators on size and colour of snail shells. Limpkins are tactile predators and act as agents of disruptive selection on snail size, selecting average-sized snails disproportionately more often than small or large snails (y = 0.39, SE = 0.08). In addition, we were able to identify variation in handling behaviours and snail size selection among individual limpkins. Individual limpkins showed preferences for snails of different sizes and punctured the snail shells opposite the aperture mainly when handling large snails. Snail kites are visual predators and seem to be agents of directional selection against lighter coloured snails (β= 0.66, SE = 0.33). The ecological interaction between the apple snail and its predators provides a powerful system to further explore the role of predation in determining evolutionary changes in snail behaviour, morphology and life history.