Cross-species familiarity in shoaling fishes

Preferential association with familiar shoal mates confers a number of potentially important benefits to individuals, including improved anti-predator effects and the reduction of aggression in competitive interactions. Until now, however, familiarity has been demonstrated purely between conspecifics. Here, we present evidence that familiarity preferences can override natural preferences for conspecifics. Individual focal fishes (chub, Leuciscus cephalus) were given a choice of two stimulus shoals of the same size composed of conspecifics or of heterospecifics (minnows, Phoxinus phoxinus) in a flow tank. A series of four treatments was carried out to investigate the effects of familiarity, induced by a 15 day association between the focal fish and the stimulus fishes, on the choices made by the focal fish. Focal fishes showed a significant preference for conspecifics over heterospecifics when both stimulus shoals were composed of non-familiar individuals. Focal fishes also showed a significant preference for stimulus shoals composed of familiar fishes over stimulus shoals composed of non-familiar fishes when both shoals were conspecific and when both shoals were heterospecific. Finally, the preference of focal fishes for conspecifics disappeared when the alternative, a shoal of heterospecifics, was composed of familiar individuals. The importance of this work is discussed in the context of species interactions in free-ranging shoals.     

The effect of sex and shoal size on shoaling behaviour in Danio rerio

Male and female zebra fish Danio rerio were given choices of shoals that differed in sex and size. Male zebra fish preferred to associate with female shoals over male shoals, but had no preference when given a choice between a mixed‐sex shoal and either a male or female shoal. Female zebra fish showed no significant preference when given a choice between male and females shoals, nor between mixed‐sex shoals and either male or female shoals. When given choices between shoals of differing size, females preferred to associate with the larger shoal, whether or not they were composed of males or females. Males, however, had no preference for larger shoals over smaller shoals, whether or not they were composed of males or females. These results showed that male zebra fish were capable of distinguishing between males and females solely on the basis of visual cues. Furthermore, these results demonstrated a significant difference between the shoaling choices of male and female zebra fish, which may indicate a difference in the function of shoaling for the two sexes.     

Effects of fasting on collective movement and fission–fusion dynamics in both homogeneous and heterogeneous shoals of a group-living cyprinid fish species

The present study aimed to reveal the effect of fasting (21 days) on collective movement and interaction dynamics in both homogeneous (eight members fed a commercial diet or deprived of food) and heterogeneous (four fed + four starved members) shoals of juvenile qingbo (Spinibarbus sinensis). The authors of this study measured the shoaling behaviour in both a commonly used rectangular open arena with no spatial complexity and a radial arm maze. When measured in the open arena, the starved shoals had a faster swimming speed and acceleration rate and a longer interindividual distance than the fed shoals, possibly because of the elevated foraging motivation. Nonetheless, the values of the heterogeneous groups were similar to those of the fed groups. Furthermore, in contrast to the fish in homogeneous shoals, the starved fish in heterogeneous shoals showed a slower acceleration rate and speed than fed members in heterogeneous shoals. These results, combined with the relationships of variables at the among- and within-shoal levels, suggested that starved fish limited their motion in heterogeneous shoals to maintain group cohesion but that the fed fish contributed more to maintaining shoal structure, possibly because of the higher energy expenditure required for movement changes. When monitored in a radial arm maze, starved shoals showed more fission–fusion episodes without sacrificing group cohesion, as they adaptively adjusted the frequency and duration of each majority choice. The among-shoal variation revealed that the heterogeneous groups showed less variation in the open arena but more variation in the radius maze than did the homogeneous groups. This difference might arise because dominant members have opposite effects on shoal behaviour and consensus decisions. In conclusion, the present study showed opposite effects of feeding states on collective behaviour between homogeneous and heterogeneous shoals, possibly because of the complicated interactions among members with different energy storage levels and foraging motivations. Furthermore, the heterogeneous groups showed a difference between shoal behaviour in the open area and exploration in the radial arm maze. Future studies manipulating the personality composition of starved and fed members of heterogeneous groups might yield interesting results.     

Shoaling Decisions in Angelfish: The Roles of Social Status and Familiarity

Abstract Past research has shown that angelfish, Pterophyllum scalare , are capable of discriminating between shoals composed of familiar dominant and subordinate companions, whereas they show no preference for shoals of unfamiliar conspecifics. In this study, the relative importance of familiarity and social status (shoal factors) on the shoaling decision of juvenile angelfish, which also differed in social status (individual factor), was investigated as very little is known about such tradeoffs in fishes. Dominant and subordinate individuals were given the choice to shoal with a group of conspecifics composed of familiar dominants vs. unfamiliar dominants and composed of familiar subordinates vs. unfamiliar subordinates. The findings demonstrate that fish with different social status differed in their shoaling preference. Subordinate test fish showed a preferential association with familiar subordinates over unfamiliar subordinates, but preferred the unfamiliar shoal over the familiar one when both shoals were constituted by dominant individuals. The shoaling behaviour shown by dominant test fish, on the other hand, indicated no significant preference for any of the shoals regardless of their composition. A replicate preference test carried out 2 h 30 min after the first one indicated that the association pattern was relatively consistent. Results suggest that angelfish are able to differentiate between the stimulus shoals and demonstrate that the pervasive influence of familiarity on the shoaling decision may be restrained or overridden by the composition of the familiar shoals and the social status of the test fish.     

Differences in the pattern of antipredator behaviour between hatchery‐reared and wild European sea bass juveniles

Shoals of hatchery‐reared and wild sea bass juveniles Dicentrarchus labrax were tested for differences in their antipredator responses towards a potential live predator, the eel Anguilla anguilla . Eight experimental shoals ( i.e . replicates), each composed of 15 individuals from the same stock of juveniles ( i.e . wild or hatchery), were video recorded for 5 min before and after predator exposure. A set of behavioural variables were measured during the pre‐stimulus and stimulus phases of each test and compared between the two groups of replicates. Results showed that in both hatchery‐reared and wild juveniles predator exposure elicited a significant increase in the mean level of shoal cohesiveness and mean shoal distance from the predator, and a significant decrease in the mean shoal distance from the bottom. Shoals of wild juveniles, however, aggregated more quickly and reached higher shoal cohesiveness within the first 20 s of the stimulus period than shoals of hatchery‐reared fish. During this period, the wild fish also reached the highest peak in shoal cohesiveness, which then decreased gradually towards the levels observed before predator exposure. Another component of the antipredator response, the predator inspection behaviour, was fully developed in both wild and hatchery fish. Wild fish, however, tended to inspect the predator at a closer distance than hatchery fish.     

Is there always an influence of shoal size on predator hunting success?

Theoretical and empirical studies predict that there should be a decrease in hunting success of predators with increasing prey group size. Most of these studies investigated situations in which predator and prey were in full view of each other before, during and after an attack. In this study, single rock bass Ambloplites rupestris were given an opportunity to launch surprise attacks at shoals of creek chub Semotilus atromaculatus that ranged in size from two to 13 fish. There was no significant influence of either shoal size or attack distance on predator success rate and no significant relationship between attack distance and shoal size. Furthermore, it was found that the leading fish of a shoal was attacked significantly more often than fish in other shoal positions, indicating that predation risk was not shared equally among shoal members. Also, leading fish in larger shoals (eight to 13 fish) were not more likely to survive a predator attack than ones in small shoals (two to seven fish).The consequences of these results are discussed in the general context of antipredator benefits of grouping.     

Acoustic observation of diel vertical migration and shoaling behaviour in Atlantic redfishes

Acoustic methods were used to study Atlantic redfishes Sebastes spp. vertical migration and shoaling behaviour in Newfoundland waters. Redfishes exhibited consistent patterns of vertical migration in winter, spring and summer, but pelagic shoals were not observed in winter. Pelagic daytime aggregations were generally in close proximity to dense patches of redfishes along the sea floor. Pelagic shoals exhibited high degrees of variability in size, shape and density. Attempts to explain variations in shoal density and area with features of shoal position and structure were unsuccessful. Nearest neighbour distance between fish in shoals had a lower limit near one body length. During the night, fishes were dispersed in the water column and distributions were more homogenous. Diel vertical migration appeared to be a foraging strategy, in which redfishes followed the migration of their euphausiid prey.     

Shoal sex composition affects exploration in the Mediterranean killifish

As a consequence of sexual selection, males and females may exhibit wide behavioural differences, for example, spatial behaviour. In fish, the two sexes often show different exploratory tendencies. This sex difference has been usually studied by testing individual fish. As many fish species live in social groups with different sex composition, the aforementioned approach might not picture the natural variation of the exploratory behaviour expressed by males and females. Here, we observed shoals of four Mediterranean killifish, Aphanius fasciatus, with three different sex compositions (4 females, 4 males, or 2 females and 2 males) during the exploration of a novel environment. Sex composition of the shoals did not predict the latency to emerge from a shelter into the novel environment. However, once emerged, shoals composed by four males displayed reduced exploratory behaviour compared to 4‐female and mixed‐sex shoals. These results indicated that sex differences in exploration subsist also at group level and highlighted the importance of sex composition in determining the behaviour of the entire shoal.     

活跃性和社会性对中华倒刺鲃集群行为的影响

为考察群体中不同的个性组成对鱼类集群行为的影响及其内在机制,选取中华倒刺鲃(Spinibarbus sinensis)幼鱼为实验对象,依次测定其活跃性和社会性,随后分别根据活跃性和社会性的高低分为高、低和混合活跃性(或社会性)鱼群,考察鱼群中不同个性组成对集群时的整体运动特征以及每尾鱼的个体运动特征的影响。研究发现：(1)中华倒刺鲃的个性特征稳定且个体间变异较大;(2)高活跃性鱼群的运动时间比和速度同步性均大于低活跃性鱼群,而混合鱼群位于二者之间且与两个同质性鱼群均无显著差异;高社会性鱼群速度同步性显著小于低社会性和混合社会性鱼群,而后两者之间没有显著差异。(3)活跃性特征与集群运动时每尾鱼的运动特征(速度及其同步性等)相关,社会性特征不仅与上述运动特征关联,还与凝聚力大小(距鱼群质心距离)相关。研究表明：(1)鱼群的活跃性和社会性组成均对集群行为产生重要影响,但其内在机制截然不同。主要表现为：就活跃性而言,群体的运动状态是由群体中所有成员共同决定(平均决定机制);就社会性而言,少数低社会性成员对鱼群的运动水平表现有着主导作用(少数决定机制);(2)实验鱼的活跃性在集群行为中得到了较大...     

The effect of shoal size on patterns of body colour segregation in mollies

Individual white and black mollies Poecilia latipinna spent significantly more time near the larger group when given the choice between two shoals of similar colouration to themselves. When given the choice between a large and a small shoal of dissimilar colouration to themselves, black test fish spent significantly more time with the larger shoal while white test fish showed no preference for either group. Both white and black mollies chose the smaller of two shoals when given the choice between a large dissimilarly coloured shoal and a small similarly coloured shoal. The results indicate that mollies actively discriminate between shoals on the basis of both body colour and shoal size. However, body colour segregation appears to have a stronger influence on shoal choice.     

Body length variation within multi-species fish shoals: the effects of shoal size and number of species

Theory predicts that selection should favour phenotypic homogeneity in fish shoals, and field studies have indeed confirmed that variation in body length within fish shoals is significantly lower than expected from a random distribution of fish among shoals. We investigated the extent to which variation in fish body length within shoals is determined by the shoal mean of body length, the number of species in a shoal, and the overall shoal size. We collected 34 fish shoals, ranging in size from 6 to 776 individuals, from the littoral zone of a Canadian lake. Shoals consisted of up to four different species, with multi-species shoals being larger and more frequent than single-species ones. The strongest determinant of body length variation within shoals was the shoal mean of body length, followed by the number of fish species in a shoal; i.e. multi-species shoals were less size-assorted than single-species ones. A more detailed analysis showed that the higher body length variation observed in multi-species shoals was due to increased body length variation both within and between component species. Shoal size had no significant effect on body length variation within shoals. Potential explanations of the positive relationship between body length variation and the number of species in a shoal are suggested. The implications of the above results for the evolution of multi-species shoals are discussed. Received: 6 May 1997 / Accepted: 14 October 1997     

Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition

Theory predicts several advantages for animals to recognize kin. These include inbreeding avoidance and an increase in inclusive fitness. In shoaling species, kin recognition may lead to an increased amount of altruism among shoal members. Adult, non‐reproductive three‐spined sticklebacks, Gasterosteus aculeatus, prefer to shoal with kin. This preference was shown for familiar as well as for unfamiliar individuals. However, whether it is based on learned cues of familiar individuals or on innate mechanisms like self‐referent phenotype matching or ‘true’ kin recognition through recognition alleles remains unknown. In our experiments, juvenile fish were given the choice between shoals that differed in relatedness and familiarity. The number of testfish who joined each group indicated that sticklebacks prefer to shoal with familiar kin when the alternative shoal was composed of unfamiliar non‐kin. When one shoal consisted of familiar kin while the second consisted of familiar non‐kin testfish did not show any preference. Kin recognition in sticklebacks is thus most likely mediated by social learning.     

Shoal Choice in the Banded Killifish (Fundulus diaphanus,Teleostei, Cyprinodontidae): Effects of Predation Risk,Fish Size,Species Composition and Size of Shoals

Banded killifish (Fundulus diaphanus) were presented individually with a choice of shoaling with either of two stimulus shoals which differed in shoal size, species composition, and fish body size, before and after a simulated avian predator attack. When threatened, test fish preferred to shoal with the larger of two conspecific shoals, but only if members of both stimulus shoals were of the same size class as the test fish. Otherwise, they preferred to shoal with similarly sized fish irrespective of shoal size; threat of predation increased the magnitude of this preference. Furthermore, test fish preferred a shoal of similarly sized shiners (Notemigonus crysoleucas) over larger killifish, when shoal sizes were identical. This indicates that body size plays a key role in shoal choice, overriding the effects of shoal size and species preference. Notwithstanding the above, shoal choice was affected by predator threat only when differences between shoal size or body size of stimulus fish were large.     

The influence of differential swimming speeds on composition of multi‐species fish shoals

The importance of species‐specific swim speeds for the formation of multi‐species fish shoals in a Canadian freshwater system was investigated. Swim speed was positively correlated with total length and differed between species but was unrelated to shoal size.     

Group Choice as a Function of Group Size Differences and Assessment Time in Fish: The Influence of Species Vulnerability to Predation

The shoal-choice behaviour of two species of fish that differ in their vulnerability to predation was compared. Individuals of threespine stickleback, Gasterosteus aculeatus, and creek chub, Semotilus atromaculatus, were presented with a simultaneous choice of two equidistant stimulus shoals of conspecifics that differed in membership size (5 vs. 6 fish, 5 vs. 7, 5 vs. 8, 5 vs. 9 and 5 vs. 10). Test fish were allowed to view the stimulus shoals from a standard distance for either 10–20 or 120–150s before being frightened with a stimulus from an overhead light and released to join either shoal. We observed which shoal (the smaller or the larger one) the test fish approached. Preference for the larger stimulus shoal generally increased with increasing shoal size difference and with the duration of the assessment period, and was more pronounced in chub (the more vulnerable of the two species). For the short assessment period, chub showed a significantly stronger preference for the larger stimulus shoal than sticklebacks, whereas there was no significant difference between species for the long assessment period. Furthermore, chub responded more readily to small differences in shoal size (of 1–3 fish) than sticklebacks, for both short and long assessment periods. The above results are consistent with the hypothesis that chub, as the more vulnerable of the two species (in terms of predation), should be able to identify the larger of two shoals more quickly and should be more sensitive to small differences in shoal size than sticklebacks.     

The importance of stable schooling: do familiar sticklebacks stick together?

Preferences for rejoining shoals composed of familiar individuals have recently been documented in a variety of small, shallow-water fish species. Such preferences are assumed to be adaptive, since familiar groups have improved anti-predator defences and more stable dominance hierarchies. However, the design of these studies may have created conditions that elevate preferences for familiar individuals. Furthermore, in natural habitats, where significant opportunities for inter-shoal transfer may exist, it is unclear whether shoals stay together long enough for such preferences to develop. Here we present the results of a laboratory study examining whether prior familiarity influences the subsequent shoal composition of sticklebacks (Gasterosteus aculeatus) allowed to re-assort freely in a large arena tank. We show that fish from different familiarity groups associate with familiar conspecifics significantly more than predicted by a model of random assortment, suggesting that even when there is ample opportunity for inter-group transfer, shoal composition can remain stable. We discuss the phenomena that may lead to the formation of familiar groups in natural habitats. In addition, we suggest that familiarity benefits may reduce the relative value of transferring to otherwise more attractive (e.g. larger or more phenotypically matched) groups, and thereby stabilize shoal structure.     

Influence of Parasitism on Shoal Choice in the Banded Killifish (Fundulus diaphanus,Teleostei, Cyprinodontidae)

Banded killifish, Fundulus diaphanus, were presented individually with a choice of ‘shoaling’ with either of two conspecific stimulus shoals, one consisting of fish with externally visible black spots (indicating the presence of a parasitic trematode worm, Crassiphiala bulboglossa), the other consisting of fish without such spots. Both parasitized and unparasitized test fish significantly preferred to shoal with unparasitized stimulus shoals over parasitized ones. The relative preference of unparasitized killifish for unparasitized shoals increased with increasing degree of parasite load in parasitized stimulus fish. However, no significant preference by unparasitized fish for unparasitized shoals was observed if unparasitized shoals were presented versus mixed shoals consisting of parasitized and unparasitized fish. We conclude that killifish preferred unparasitized shoals over parasitized shoals only if all fish in the respective stimulus shoals were phenotypically uniform (either with or without black spots). A final experiment showed that killifish used black spots as an indicator of parasite presence to make their shoal choice. The significance of these results for the formation of parasite-assorted shoals is discussed.     

UV matters in shoaling decisions

Shoaling behaviour in fish is influenced by numerous factors, such as familiarity, kinship, group size and shoal composition. Grouping decisions are based on both olfactory and visual cues. The visual system of many vertebrates is extended into the ultraviolet (UV) wave range as in three-spined sticklebacks (Gasterosteus aculeatus, L.). We investigated whether the presence or absence of UV wavelengths has an influence on shoaling behaviour in this species. Reproductively non-active three-spined sticklebacks were given the choice between two shoals, equal in numbers of individuals, which could be seen either through a UV-transmitting [UV(+)] or a UV-blocking [UV(-)] filter. Test fish preferred to join the shoal seen under UV(+) conditions. Due to differences in quantal flux between the UV(+) and UV(-) filters used, control experiments with neutral-density optical filters were performed in order to clarify the role of luminance. Here, test fish spent significantly more time near shoals that were seen in a darker environment, suggesting a potential trade-off between UV radiation and lower brightness during shoal choice.To our knowledge, these results demonstrate for the first time that shoaling decisions are influenced by UV wavelengths.     

Predator-induced neophobia in juvenile cichlids

Predation is an important but often fluctuating selection factor for prey animals. Accordingly, individuals plastically adopt antipredator strategies in response to current predation risk. Recently, it was proposed that predation risk also plastically induces neophobia (an antipredator response towards novel cues). Previous studies, however, do not allow a differentiation between general neophobia and sensory channel-specific neophobic responses. Therefore, we tested the neophobia hypothesis focusing on adjustment in shoaling behavior in response to a novel cue addressing a different sensory channel than the one from which predation risk was initially perceived. From hatching onwards, juveniles of the cichlid Pelvicachromis taeniatus were exposed to different chemical cues in a split-clutch design: conspecific alarm cues which signal predation risk and heterospecific alarm cues or distilled water as controls. At 2 months of age, their shoaling behavior was examined prior and subsequent to a tactical disturbance cue. We found that fish previously exposed to predation risk formed more compact shoals relative to the control groups in response to the novel disturbance cue. Moreover, the relationship between shoal density and shoal homogeneity was also affected by experienced predation risk. Our findings indicate predator-induced, increased cross-sensory sensitivity towards novel cues making neophobia an effective antipredator mechanism.     

Background colouration influences body colour segregation in mollies

When given a choice of swimming against a black background near an empty black end compartment or swimming against a white background near an empty white compartment, black morph mollies Poecilia latipinna spent significantly more time against the black background. The presence of a shoal (either white or black mollies) in the black compartment increased the preference of the test fish for the black background. However, black molly test fish spent significantly less time against a black background if a black shoal was present in the white compartment than in assays in which a white shoal was in the white compartment. In assays where test fish were given the choice between two black shoals, test fish spent significantly more time near the black shoal on the black background. Similarly, when given the choice between two white shoals, test fish spent significantly more time against the black background. The results suggest that the presence of cryptic backgrounds alter shoalmate choices in fish that assort according to body colouration.