Social transmission of behavioural traditions in a coral reef fish

doi:10.1016/S0003-3472(84)80272-9

Animal Behaviour

Volume 32, Issue 2, May 1984, Pages 379-384

https://doi.org/10.1016/S0003-3472(84)80272-9 Get rights and content

Abstract

Traditional behaviours involve the non-genetic transmission of social information across age classes or generations. French grunts (Haemulon flavolineatum) exhibit social traditions of daytime schooling sites and twilight migration routes. Individuals transplanted to new schooling sites and allowed to follow residents at the new sites used the new migration routes and returned to the new sites in the absence of resident fish. Control fish with no opportunity to learn showed no such directionality or return. This is the first demonstration of apparent pre-cultural behaviour in free-living fish. Our observations suggest additional classes of behaviour and taxonomic groups in which pre-cultural activities are likely to have evolved.

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Over the last decades, we witnessed a growing interest in animal cognition, in general, and in fish cognition, in particular. Here, we provide various study examples that employ an ecological approach to study cognition through field observations, field manipulations and laboratory tests on wild teleost fishes. In this review, we focus on cases with implications for understanding endotherm vertebrate cognition, that is, cases that show fishes possess supposedly ‘complex’ cognitive processes originally thought to warrant a more complex brain. Furthermore, in contrast to the classic interpretation of high/low performance as high/low cognitive abilities, incorporating an individual-level ecological approach reveals that low performance in a cognitive task may be caused by a mismatch between the experimental paradigm and the individual’s experience. The future avenue for wild fish cognition is to grasp better how individual, population and species differences in performance stem from differences in their ecological conditions.
Previous experience alters individual vulnerability to angling of crucian carp (Carassius auratus)
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In recreational fisheries, fish often undergo catch-and-release angling, which can lead to an indirect selection response of the behavioral traits of the fish. As individuals experience high-intensity angling activities, individuals learn to avoid being selected for artificial bait again, resulting in a change in the vulnerability to angling of fish, which is partly dependent on the cognitive learning ability of the fish. Here, we examined the relationship between vulnerability to angling and learning in juvenile crucian carp (Carassius auratus) under laboratory conditions. Our study had six angling treatments with each containing different group mates (i.e., the angling stress group, all fish that only experienced repeated angling stress practice for a period of three days; the learning group, all fish that only observed individual in the angling stress group to be angled; the control group, all fish that did not undergo any angling or learning; the mixed Group 1, fish are from the control and learning groups; the mixed Group 2, fish are from the control and angling stress groups; the mixed Group 3, fish are from the learning and angling stress groups), each of which consisted of five replicates). All fish were tested for boldness before and after the previous experiences (i.e., angling stress or learning) test. Our results showed that for the stress group, the total angling time, mean individual angling time and total number of bait touches all increased from Day 1 to Day 3, and the total angling rate decreased during the three days of the angling stress practice. After encountering the previous experiences, fish in the control, stress and learning groups all had increased boldness, as assessed by a shortened percent latency to emerge from the refuge. The change in the percent latency of boldness was higher in the stress group than in the learning group, with the control group being intermediate. Furthermore, no differences in the total angling time and total number of bait touches were detected among the six angling treatments, but the stress group exhibited the longest mean individual angling time and lowest angling rate compared with the other five angling treatments, indicating that angling-stressed individuals greatly decreased their vulnerability to angling after the previous angling stress. Our results show that changes in the vulnerability of crucian carp to angling were related to previous individual angling experience but not to visual social learning.
Seasonal offshore/inshore migration of round gobies
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Sampling showed that round gobies migrated away from the shallowest (10 m) site in early October, with larger gobies moving offshore first, and were almost exclusively found deeper than 20 m by November. Round gobies remained offshore (>30 m) until mid-May, when they began the return to nearshore habitat. The cues to start offshore and return migrations were not the focus of this project, but fall offshore migrations coincided with decreasing temperatures nearshore in fall, and in spring, the offshore movement of the thermal bar.
The representation of animal behaviour in the fossil record
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Paleontologists and biologists generally utilize different lines of evidence and approaches to study, conceptualize and categorize animal behaviour, which has led to a divide between the two disciplines and lack of integration of their data. Numerous filters impact the preservation of behaviour in the fossil record. Here, we utilize 13 broad categories of behaviour representing the range of modern studies of animal behaviour and assess how they are represented in the fossil record. The data summarized in an existing compilation of ‘fossil behaviours’ is used to estimate the relative occurrence of each category. We also examine the taxonomic coverage of fossil animal behaviour using the same source. We found that feeding and habitat selection-related behaviours were disproportionately represented. Examples of other behavioural categories, especially social ones, such as mating, communication or parenting were considerably rarer, whereas personality or play were not represented at all. Arthropods tended to be most well represented, including insects in amber, followed by vertebrates. Taxonomic coverage was overall fairly diverse. A broader literature search was used to identify the oldest paleontological evidence of each behavioural category. We found that most categories probably appeared by the end of the Cambrian radiation. Finally, we suggest that the preservation of behaviour in fossils can be estimated from first principles, such as the amount of time animals engage in a behaviour or which behaviours impact a substrate. Reconstructing the evolution of behaviour in deep time requires understanding how the fossil record captures behavioural information. We strongly encourage paleontologists and biologists studying behaviour to work together to help complete our understanding of animal behaviour across the entirety of its evolutionary history.
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^*: Present address: Department of Biological Sciences, University of California, Santa Barbara, CA 93106, U.S.A.

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Animal Behaviour

Abstract

References (36)

Social transmission of acquired behavior: a discussion of tradition and social learning in vertebrates

The ontogeny of twilight migration patterns in grunts (Pisces: Haemulidae)

Anim. Behav.

Paternal care

Anim. Behav.

The social behaviour of anuran amphibians

Anim. Behav.

The evolution of parental care in fishes, with reference to Darwin's rule of male sexual selection

Envir. Biol. Fish.

Correlations between otolith microstructure, growth, and life history transitions in newly recruited French grunts [Haemulon flavolineatum (Desmarest), Haemulidae]

Rapp. P.-V. Reun. Cons. Int. Explor. Mer.

Social behavior in hatchling green iguanas: life at a reptile rookery

Science, N.Y.

Daily and summer-winter variation in mass spawning of striped parrotfish, Scarus croicensis

Fish. Bull. U.S.

Twilight migrations and foraging activities of the copper sweeper, Pempheris schomburgki (Teleostei, Pempheridae)

Mar. Biol.

Twilight activities and temporal structure in a freshwater fish community

Can. J. Fish. Aquat. Sci.

Queuing behavior of spiny lobsters

Science, N.Y.

Activity of Hawaiian reef fishes during evening and morning transitions between daylight and darkness

Fish Bull. U.S.

Diel feeding migrations in tropical reef fishes

Helg. W. Meer.

Life history patterns and reproductive biology of neotropical salamanders

Cited by (181)

The effect of observing trained conspecifics on the performance and motivation of goldfish, Carassius auratus, in a spatial task

Fish ecology and cognition: insights from studies on wild and wild-caught teleost fishes

Previous experience alters individual vulnerability to angling of crucian carp (Carassius auratus)

Seasonal offshore/inshore migration of round gobies

The representation of animal behaviour in the fossil record

Guppies show rapid and lasting inhibition of foraging behaviour