Moving calls: a vocal mechanism underlying quorum decisions in cohesive groups

Members of social groups need to coordinate their behaviour when choosing between alternative activities. Consensus decisions enable group members to maintain group cohesion and one way to reach consensus is to rely on quorums. A quorum response is where the probability of an activity change sharply increases with the number of individuals supporting the new activity. Here, we investigated how meerkats (Suricata suricatta) use vocalizations in the context of movement decisions. Moving calls emitted by meerkats increased the speed of the group, with a sharp increase in the probability of changing foraging patch when the number of group members joining the chorus increased from two up to three. These calls had no apparent effect on the group's movement direction. When dominant individuals were involved in the chorus, the group's reaction was not stronger than when only subordinates called. Groups only increased speed in response to playbacks of moving calls from one individual when other group members emitted moving calls as well. The voting mechanism linked to a quorum probably allows meerkat groups to change foraging patches cohesively with increased speed. Such vocal coordination may reflect an aggregation rule linking individual assessment of foraging patch quality to group travel route.     

Quorum responses and consensus decision making

Animal groups are said to make consensus decisions when group members come to agree on the same option. Consensus decisions are taxonomically widespread and potentially offer three key benefits: maintenance of group cohesion, enhancement of decision accuracy compared with lone individuals and improvement in decision speed. In the absence of centralized control, arriving at a consensus depends on local interactions in which each individual''s likelihood of choosing an option increases with the number of others already committed to that option. The resulting positive feedback can effectively direct most or all group members to the best available choice. In this paper, we examine the functional form of the individual response to others'' behaviour that lies at the heart of this process. We review recent theoretical and empirical work on consensus decisions, and we develop a simple mathematical model to show the central importance to speedy and accurate decisions of quorum responses, in which an animal''s probability of exhibiting a behaviour is a sharply nonlinear function of the number of other individuals already performing this behaviour. We argue that systems relying on such quorum rules can achieve cohesive choice of the best option while also permitting adaptive tuning of the trade-off between decision speed and accuracy.     

Species difference in adaptive use of public information in sticklebacks

Animals foraging on variable food sources can refine their estimates of patch quality by monitoring the success of others (i.e. collect 'public information'). Here, we show that both three-spined sticklebacks (Gasterosteus aculeatus) and nine-spined sticklebacks (Pungitius pungitius) use past cues provided by others to locate food but only nine-spined sticklebacks use prior public information to assess patch quality, regardless of whether demonstrators were conspecifics or heterospecifics. Moreover, nine-spined but not three-spined sticklebacks preferentially hid in vegetation during the demonstration, a position from which they could observe both patches simultaneously and collect public information. We conclude that species differences in the use of public information can be explained by variations in habitat choice and response to predation. Our findings expand current understanding of the scope of public-information use in animals by showing that fishes can use public-information in a foraging context and from heterospecifics. The study suggests that public-information use is an adaptation that allows animals vulnerable to predation to acquire valuable foraging information at low risk.     

Reversed brain size sexual dimorphism accompanies loss of parental care in white sticklebacks

Uncovering factors that shape variation in brain morphology remains a major challenge in evolutionary biology. Recently, it has been shown that brain size is positively associated with level of parental care behavior in various taxa. One explanation for this pattern is that the cognitive demands of performing complex parental care may require increased brain size. This idea is known as the parental brain hypothesis (PBH). We set out to test the predictions of this hypothesis in wild populations of threespine stickleback (Gasterosteus aculeatus). These fish are commonly known to exhibit (1) uniparental male care and (2) sexual dimorphism in brain size (males>females). To test the PBH, we took advantage of the existence of closely related populations of stickleback that display variation in parental care behavior: common marine threespine sticklebacks (uniparental male care) and white threespine sticklebacks (no care). To begin, we quantified genetic differentiation among two common populations and three white populations from Nova Scotia. We found overall low differentiation among populations, although F_ST was increased in between‐type comparisons. We then measured the brain weights of males and females from all five populations along with two additional common populations from British Columbia. We found that sexual dimorphism in brain size is reversed in white stickleback populations: males have smaller brains than females. Thus, while several alternatives need to be ruled out, the PBH appears to be a reasonable explanation for sexual dimorphism in brain size in threespine sticklebacks.     

Speciation in ninespine stickleback: reproductive isolation and phenotypic divergence among cryptic species of Japanese ninespine stickleback

Although similar patterns of phenotypic diversification are often observed in phylogenetically independent lineages, differences in the magnitude and direction of phenotypic divergence have been also observed among independent lineages, even when exposed to the same ecological gradients. The stickleback family is a good model with which to explore the ecological and genetic basis of parallel and nonparallel patterns of phenotypic evolution, because there are a variety of populations and species that are locally adapted to divergent environments. Although the patterns of phenotypic divergence as well as the genetic and ecological mechanisms have been well characterized in threespine sticklebacks, Gasterosteus aculeatus, we know little about the patterns of phenotypic diversification in other stickleback lineages. In eastern Hokkaido, Japan, there are three species of ninespine sticklebacks, Pungitius tymensis and the freshwater type and the brackish‐water type of the P. pungitius–P. sinensis species complex. They utilize divergent habitats along coast–stream gradients of rivers. Here, we investigated genetic, ecological and phenotypic divergence among three species of Japanese ninespine sticklebacks. Divergence in trophic morphology and salinity tolerance occurred in the direction predicted by the patterns observed in threespine sticklebacks. However, the patterns of divergence in armour plate were different from those previously found in threespine sticklebacks. Furthermore, the genetic basis of plate variation may differ from that in threespine sticklebacks. Because threespine sticklebacks are well‐established model for evolutionary research, the sympatric trio of ninespine sticklebacks will be an invaluable resource for ecological and genetic studies on both common and lineage‐specific patterns of phenotypic diversification.     

Sex‐selective Predation by Threespine Sticklebacks on Sea Lice: A Novel Cleaning Behaviour

Cleaning interactions have been described in a wide range of fish species and other taxa. We observed a novel cleaning behaviour during a study of the transmission dynamics of sea lice (Lepeophtheirus salmonis) between juvenile pink salmon (Oncorhynchus gorbuscha) and threespine sticklebacks (Gasterosteus aculeatus) in the Broughton Archipelago, British Columbia, Canada. Experiments showed that sticklebacks significantly reduced the number of sea lice on individual juvenile salmon. Adult female lice were preferentially consumed by sticklebacks, and gravid female lice also experienced egg string cropping. Overall, 76% of gravid female lice experienced either consumption, egg string cropping, or both by sticklebacks. This preference by sticklebacks for female parasites may stem from female lice being larger than males and the added nutritional value of egg strings on gravid females. Cleaning by sticklebacks can potentially have an impact on sea louse populations on wild juvenile salmon.     

Conspicuous Female Ornamentation and Tests of Male Mate Preference in Threespine Sticklebacks (Gasterosteus aculeatus)

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.     

Colony size affects collective decision-making in the ant Temnothorax albipennis

Social insects are well-known for their ability to achieve robust collective behaviours even when individuals have limited information. It is often assumed that such behaviours rely on very large group sizes, but many insect colonies start out with only a few workers. Here we investigate the influence of colony size on collective decision-making in the house-hunting of the ant Temnothorax albipennis. In experiments where colony size was manipulated by splitting colonies, we show that worker number has an influence on the speed with which colonies discover new nest sites, but not on the time needed to make a decision (achieve a quorum threshold) or total emigration time. This occurred because split colonies adopted a lower quorum threshold, in fact they adopted the same threshold in proportion to their size as full-size colonies. This indicates that ants may be measuring relative quorum, i.e. population in the new nest relative to that of the old nest, rather than the absolute number. Experimentally reduced colonies also seemed to gain more from experience through repeated emigrations, as they could then reduce nest discovery times to those of larger colonies. In colonies of different sizes collected from the field, total emigration time was also not correlated with colony size. However, quorum threshold was not correlated with colony size, meaning that individuals in larger colonies adopted relatively lower quorum thresholds. Since this is a different result to that from size-manipulated colonies, it strongly suggests that the differences between natural small and large colonies were not caused by worker number alone. Individual ants may have adjusted their behaviour to their colony’s size, or other factors may correlate with colony size in the field. Our study thus shows the importance of experimentally manipulating colony size if the effect of worker number on the emergence of collective behaviour is to be studied. Received 13 December 2005; revised 9 May 2006; accepted 15 May 2006.     

Flexible mate choice when mates are rare and time is short

Female mate choice is much more dynamic than we once thought. Mating decisions depend on both intrinsic and extrinsic factors, and these two may interact with one another. In this study, we investigate how responses to the social mating environment (extrinsic) change as individuals age (intrinsic). We first conducted a field survey to examine the extent of natural variation in mate availability in a population of threespine sticklebacks. We then manipulated the sex ratio in the laboratory to determine the impact of variation in mate availability on sexual signaling, competition, and mating decisions that are made throughout life. Field surveys revealed within season heterogeneity in mate availability across breeding sites, providing evidence for the variation necessary for the evolution of plastic preferences. In our laboratory study, males from both female‐biased and male‐biased treatments invested most in sexual signaling late in life, although they competed most early in life. Females became more responsive to courtship over time, and those experiencing female‐biased, but not male‐biased sex ratios, relaxed their mating decisions late in life. Our results suggest that social experience and age interact to affect sexual signaling and female mating decisions. Flexible behavior could mediate the potentially negative effects of environmental change on population viability, allowing reproductive success even when preferred mates are rare.     

Stop-Signaling Reduces Split Decisions without Impairing Accuracy in the Honeybee Nest-Site Selection Process

In the honeybee swarm nest-site selection process, individual bees gather information about available candidate sites and communicate the information to other bees. The swarm makes an agreement for a candidate site when the number of bees that supports the site reaches a threshold. This threshold is usually referred to as the quorum threshold and it is shown by many studies as a key parameter that is a compromise between the accuracy and speed of decisions. In the present work, we use a model of the honeybee Apis mellifera nest-site selection process to study how the quorum threshold and discovery time of candidate sites have major impact on two unfavorable situations in selecting a nest site: decision deadlock and decision split. We show that cross-inhibitory stop-signaling, delivered among bees supporting different sites, enables swarms to avoid the decision split problem in addition to avoiding the decision deadlock problem that has been previously proposed. We also show that stop-signaling improves decision speed, but compromises decision accuracy in swarms using high quorum thresholds by causing the swarms to be trapped in local optima (e.g., choosing a sub-optimal option that is encountered first). On the other hand, we demonstrate that stop-signaling can reduce split decisions without compromising decision accuracy in swarms using low quorum thresholds when it is compared to the accuracy of swarms using the same threshold values but not exhibiting stop-signaling. Based on our simulations, we suggest that swarms using low quorum thresholds (as well as swarms with large population sizes) would benefit more from exhibiting the stop-signaling activity than not exhibiting it.     

Genetic structure of threespine stickleback,Gasterosteus aculeatus,in Lake Harutori,Japan, with reference to coexisting anadromous and freshwater forms

Both anadromous and freshwater forms of threespine sticklebacks (Gasterosteus aculeatus) inhabit Lake Harutori on the pacific coast of eastern Hokkaido, Japan. Since the two groups of threespine sticklebacks, Pacific Ocean and Japan Sea groups, which showed high genetic differentiation between them, were sympatrically distributed on the Pacific Ocean coast of Hokkaido Island, the genetic structures of the two forms were examined in Lake Harutori. Allozyme analyses of the two forms showed that most specimens from Lake Harutori belonged to the Pacific Ocean group, with a few fish belonging to the Japan Sea group or representing hybrids between the two groups. Both anadromous and freshwater sticklebacks were detected in the Pacific Ocean group. There were no significant differences in allelic frequencies at 17 presumptive loci between the two forms. Analyses of genetic relationships among 5 populations showed that the freshwater population from Lake Harutori was genetically more closely related to the sympatric anadromous population than to the freshwater population from a neighboring river. These results suggested that anadromous and freshwater sticklebacks in Lake Harutori form a single breeding population, and that the two forms might represent a life-history polymorphism within a single population.     

Foraging nine-spined sticklebacks prefer to rely on public information over simpler social cues

Social animals can observe others' behavior and in the processacquire information of varying quality about a given resource.Theoretical models predict that blind copying of others' behavioris more likely when individuals are only able to observe thedecisions (here "social cues") of others rather than the cues(here "public information") on which such decisions are based.We investigated information use by nine-spined sticklebacks(Pungitius pungitius) in a two-patch foraging context. Socialcues were provided by the number of demonstrator fish presentat each patch (two versus six), which either conflicted withthe demonstrators' observed feeding rate at each patch (publicinformation) or was the only information available. Consistentwith predictions, observers preferred the patch previously associatedwith six demonstrators when social cues were the only availablesource of information but preferred the patch previously associatedwith two demonstrators ("rich" patch) when also provided withpublic information. On the bases of these experiments, we arguethat it is because these fish preferentially base decisionson public information rather than social cues that they canpotentially avoid engaging in erroneous informational cascades.Thus, the availability of public information can help socialanimals make adaptive decisions.     

Niche specialization influences adaptive phenotypic plasticity in the threespine stickleback

Phenotypic plasticity may be favored in generalist populations if it increases niche width, even in temporally constant environments. Phenotypic plasticity can increase the frequency of extreme phenotypes in a population and thus allow it to make use of a wide resource spectrum. Here we test the prediction that generalist populations should be more plastic than specialists. In a common-garden experiment, we show that solitary, generalist populations of threespine sticklebacks inhabiting small coastal lakes of British Columbia have a higher degree of morphological plasticity than the more specialized sympatric limnetic and benthic species. The ancestral marine stickleback showed low levels of plasticity similar to those of sympatric sticklebacks, implying that the greater plasticity of the generalist population has evolved recently. Measurements of wild populations show that those with mean trait values intermediate between the benthic and limnetic values indeed have higher morphological variation. Our data indicate that plasticity can evolve rapidly after colonization of a new environment in response to changing niche use.     

Plastic responses to parents and predators lead to divergent shoaling behaviour in sticklebacks

Population divergence in antipredator defence and behaviour occurs rapidly and repeatedly. Genetic differences, phenotypic plasticity or parental effects may all contribute to divergence, but the relative importance of each of these mechanisms remains unknown. We exposed juveniles to parents and predators to measure how induced changes contribute to shoaling behaviour differences between two threespine stickleback species (benthics and limnetics: Gasterosteus spp). We found that limnetics increased shoaling in response to predator attacks, whereas benthics did not alter their behaviour. Care by limnetic fathers led to increased shoaling in both limnetic and benthic offspring. Shoaling helps limnetics avoid trout and avian predation; our results suggest that this adaptive behaviour is the result of a combination of paternal effects, predator-induced plasticity and genetic differences between species. These results suggest that plasticity substantially contributes to the rapid divergence in shoaling behaviour across the post-Pleistocene radiation of sticklebacks.     

A review of competitive resource sharing under constraints in sticklebacks

The best strategy for an animal competing intraspecifically for food depends on its relative competitive ability, its needs, and on the strategies its competitors are using. Three different investigations using threespined sticklebacks, Gasterosteus aculeatus , as predators and Daphnia or Tubifex worms as prey are reviewed: (1) six sticklebacks differing in competitive ability compete for two food patches, of which one is twice as profitable as the other; (2) two sticklebacks differing in competitive ability compete in one patch for two types of prey, of which one is three times as profitable as the other; (3) parasitised and healthy sticklebacks have to decide alone, and in competition with each other, how close they dare approach on their own to a live predator waiting close to profitable food. The best strategy from the point of view of the stickleback is different from that of its parasite. The two parasite species studied, Schistocephalus solidus and Glugea anomala, ought to influence their host's behaviour in opposite directions.     

Patch use behaviour in benthic fish depends on their long-term growth prospects

Animals foraging in a heterogeneous environment may combine prior information on patch qualities and patch sample information to maximize intake rate. Prior information dictates the long-term expectations, whereas prior information in combination with patch sample information determines when to leave an individual food patch. We examined patch use behaviour of benthic feeding fish in their natural environment at different spatial scales to test if they could determine patch quality and if patch use behaviour was correlated with environmental quality. In seven lakes along a gradient of environmental quality (measured as maximum benthivore size), we made repeated measurements of giving-up density (GUD) in artificial food patches of different qualities. At the largest spatial scale, between lakes, we tested if giving-up densities revealed the long-term growth expectation of benthic fish. At the local scale of patches and micro patches we tested for the ability of benthic fish to assess patch quality, and how this ability depended on the patch exploitation levels between the different lakes. We found that GUD was positively related to maximum size of bream, suggesting that short-term behavioural decisions reflected long-term growth expectations. Benthic fish discriminated between nearby rich and poor patches, but not between rich and poor micropatches within a food patch. This suggests that the foraging scale of benthic fish lies between the patch and micro patch scale in our experiments. We conclude that patch use behaviour of benthic fish can provide a powerful measure of habitat quality that reveals how benthic fish perceive their environment.     

Nine-spined sticklebacks exploit the most reliable source when public and private information conflict

Social foragers can potentially use private information gained from personal experience and public information gained from observing the foraging success of others to determine the profitability of a foraging patch. We investigated how nine-spined sticklebacks use conflicting public and private information of variable reliability to make foraging decisions. In a first experiment, when private information was reliable, sticklebacks ignored public information and based their foraging decision on private information. However, when private information was less reliable, sticklebacks tended to use public rather than private information. A second experiment investigated how the time since experiencing private information affected sticklebacks' use of this information when it conflicted with recent public information. Fish based their foraging decisions on recently acquired private information, but reliance on private information diminished as the period since experiencing it increased. Fish used public information if 7 days had elapsed since updating their private information. Our findings suggest that nine-spined sticklebacks flexibly adjust their decision making to exploit the most reliable information available, be it public or private, and that animals will weight private and public information appropriately depending on circumstances.     

Rate of food consumption in a population of threespine sticklebacks,Gasterosteus aculeatus,estimated from the faecal production

Synopsis The daily rate of faecal production by threespine sticklebacks living in a small lake was measured at monthly intervals. Laboratory experiments yielded a regression model which allowed the prediction of the rate of food consumption from faecal production. It was estimated that the annual rate of consumption was 12,800 mg per fish. The highest rate of food consumption was in early summer. The experiments also showed that the absorption efficiency was greater at higher temperatures and for heavier fish.Address all correspondence to R.J. Wootton     

Do heavy burdens of Schistocephalus solidus in juvenile threespine stickleback result in disaster for the parasite?

The diphyllobothriidean cestode Schistocephalus solidus typically infects threespine sticklebacks that are too small to allow the parasite to reach a mature size. As a result, the parasite must allow further growth of its host to reach the size at which it becomes competent to infect and reproduce in the definitive host. At times, however, intensity of infection can be high, leading to crowding among parasites and to heavy burdens causing mortality among hosts. Our data show that, during a previously observed epizootic, large percentages of plerocercoids (average 75% per host, 82% among all parasites pooled) did not grow to become massive enough in 1-yr-old threespine sticklebacks to be capable of establishment and maturation in the definitive host. Massive deaths of 1-yr-old sticklebacks due to infection during the epizootic resulted in the great misfortune of a disaster for a large number of parasites, resulting in dramatically reduced transmission of S. solidus.     

Predation risk and inter-population variation in antipredator behaviour in the three-spined stickleback, Gasterosteus aculeatus L.

Predation risk from fish and bird predators was assessed at seven Scottish Gasterosteus aculeatus L. sites. Samples of adult male and female sticklebacks and fry from each site were tested with either a model heron or a live pike to measure anti-predator responses. Principal Component Analyses were then used to describe the responses, the first factor to emerge from each multivariate analysis providing an index of overall level of response toward the predator. Significant sexual and inter-population differences in behaviour are described. Sticklebacks from populations at high risk from either predatory fish or birds showed higher fright response scores than fish from low risk sites. In general, adult male sticklebacks are bolder than adult females during interactions with predators.