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Herbert-Read, James E.ORCID iD iconorcid.org/0000-0003-0243-4518
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Publications (10 of 14) Show all publications
Romenskyy, M., Herbert-Read, J. E., Ward, A. J. W. & Sumpter, D. J. T. (2017). Body size affects the strength of social interactions and spatial organization of a schooling fish (Pseudomugil signifer). Royal Society Open Science, 4(4), Article ID 161056.
Open this publication in new window or tab >>Body size affects the strength of social interactions and spatial organization of a schooling fish (Pseudomugil signifer)
2017 (English)In: Royal Society Open Science, E-ISSN 2054-5703, Vol. 4, no 4, 161056Article in journal (Refereed) Published
Abstract [en]

While a rich variety of self-propelled particle models propose to explain the collective motion of fish and other animals, rigorous statistical comparison between models and data remains a challenge. Plausible models should be flexible enough to capture changes in the collective behaviour of animal groups at their different developmental stages and group sizes. Here, we analyse the statistical properties of schooling fish (Pseudomugil signifer) through a combination of experiments and simulations. We make novel use of a Boltzmann inversion method, usually applied in molecular dynamics, to identify the effective potential of the mean force of fish interactions. Specifically, we show that larger fish have a larger repulsion zone, but stronger attraction, resulting in greater alignment in their collective motion. We model the collective dynamics of schools using a self-propelled particle model, modified to include varying particle speed and a local repulsion rule. We demonstrate that the statistical properties of the fish schools are reproduced by our model, thereby capturing a number of features of the behaviour and development of schooling fish.

Place, publisher, year, edition, pages
ROYAL SOC, 2017
Keyword
collective motion, interactions, statistical mechanics, fish school
National Category
Zoology Mathematics
Identifiers
urn:nbn:se:uu:diva-323662 (URN)10.1098/rsos.161056 (DOI)000400527200022 ()28484622 (PubMedID)
Available from: 2017-06-20 Created: 2017-06-20 Last updated: 2017-06-20Bibliographically approved
Herbert-Read, J. E., Rosén, E., Szorkovszky, A., Ioannou, C. C., Rogell, B., Perna, A., . . . Sumpter, D. J. T. (2017). How predation shapes the social interaction rules of shoaling fish. Proceedings of the Royal Society of London. Biological Sciences, 284(1861), Article ID 20171126.
Open this publication in new window or tab >>How predation shapes the social interaction rules of shoaling fish
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2017 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 284, no 1861, 20171126Article in journal (Refereed) Published
Abstract [en]

Predation is thought to shape the macroscopic properties of animal groups, making moving groups more cohesive and coordinated. Precisely how predation has shaped individuals' fine-scale social interactions in natural populations, however, is unknown. Using high-resolution tracking data of shoaling fish (Poecilia reticulata) from populations differing in natural predation pressure, we show how predation adapts individuals' social interaction rules. Fish originating from high predation environments formed larger, more cohesive, but not more polarized groups than fish from low predation environments. Using a new approach to detect the discrete points in time when individuals decide to update their movements based on the available social cues, we determine how these collective properties emerge from individuals' microscopic social interactions. We first confirm predictions that predation shapes the attraction-repulsion dynamic of these fish, reducing the critical distance at which neighbours move apart, or come back together. While we find strong evidence that fish align with their near neighbours, we do not find that predation shapes the strength or likelihood of these alignment tendencies. We also find that predation sharpens individuals' acceleration and deceleration responses, implying key perceptual and energetic differences associated with how individuals move in different predation regimes. Our results reveal how predation can shape the social interactions of individuals in groups, ultimately driving differences in groups' collective behaviour.

Place, publisher, year, edition, pages
ROYAL SOC, 2017
Keyword
group living, collective motion, Poecilia reticulata, collective behaviour, interaction rules
National Category
Zoology Ecology
Identifiers
urn:nbn:se:uu:diva-334852 (URN)10.1098/rspb.2017.1126 (DOI)000408662400016 ()
Funder
Knut and Alice Wallenberg Foundation, 0962-8452NERC - the Natural Environment Research Council, NE/K009370/1
Available from: 2017-11-28 Created: 2017-11-28 Last updated: 2017-12-01Bibliographically approved
Zajitschek, S., Herbert-Read, J. E., Abbasi, N. M., Zajitschek, F. & Immler, S. (2017). Paternal personality and social status influence offspring activity in zebrafish. BMC Evolutionary Biology, 17, Article ID 157.
Open this publication in new window or tab >>Paternal personality and social status influence offspring activity in zebrafish
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2017 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 17, 157Article in journal (Refereed) Published
Abstract [en]

Background: Evidence for the transmission of non-genetic information from father to offspring is rapidly accumulating. While the impact of chemical and physical factors such as toxins or diet on the fitness of the parents and their offspring have been studied extensively, the importance of behavioural and social circumstances has only recently been recognised. Behavioural traits such as personality characteristics can be relatively stable, and partly comprise a genetic component but we know little about the non-genetic transmission of plastic behavioural traits from parents to offspring. We investigated the relative effect of personality and of social dominance as indicators at the opposite ends of the plasticity range on offspring behaviour in the zebrafish (Danio rerio). We assessed male boldness, a behavioural trait that has previously been shown previously to possess genetic underpinnings, and experimentally manipulated male social status to assess the association between the two types of behaviour and their correlation with offspring activity. Results: We found a clear interaction between the relatively stable and putative genetic effects based on inherited differences in personality and the experimentally induced epigenetic effects from changes in the social status of the father on offspring activity. Conclusions: Our study shows that offspring behaviour is determined by a combination of paternal personality traits and on-genetic effects derived from the social status of the father.

Keyword
Behavioural syndrome, Boldness, Context-dependence, Dominance, Sperm trait, Transgenerational effects
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-330000 (URN)10.1186/s12862-017-1005-0 (DOI)000404926600003 ()
Funder
Knut and Alice Wallenberg Foundation, 102 2013.0072Swedish Research CouncilWenner-Gren FoundationsEU, European Research Council
Available from: 2017-10-13 Created: 2017-10-13 Last updated: 2017-11-29Bibliographically approved
Kurvers, R. H. J., Krause, S., Viblanc, P. E., Herbert-Read, J. E., Zaslansky, P., Domenici, P., . . . Krause, J. (2017). The Evolution of Lateralization in Group Hunting Sailfish. Current Biology, 27(4), 521-526.
Open this publication in new window or tab >>The Evolution of Lateralization in Group Hunting Sailfish
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2017 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 27, no 4, 521-526 p.Article in journal (Refereed) Published
Abstract [en]

Lateralization is widespread throughout the animal kingdom [1-7] and can increase task efficiency via shortening reaction times and saving on neural tissue [8-16]. However, lateralization might be costly because it increases predictability [17-21]. In predator-prey interactions, for example, predators might increase capture success because of specialization in a lateralized attack, but at the cost of increased predictability to their prey, constraining the evolution of lateralization. One unexplored mechanism for evading such costs is group hunting: this would allow individual-level specialization, while still allowing for group-level unpredictability. We investigated this mechanism in group hunting sailfish, Istiophorus platypterus, attacking schooling sardines, Sardinella aurita. During these attacks, sailfish alternate in attacking the prey using their elongated bills to slash or tap the prey [22-24]. This rapid bill movement is either leftward or rightward. Using behavioral observations of identifiable individual sailfish hunting in groups, we provide evidence for individual-level attack lateralization in sailfish. More strongly lateralized individuals had a higher capture success. Further evidence of lateralization comes from morphological analyses of sailfish bills that show strong evidence of one-sided micro-teeth abrasions. Finally, we show that attacks by single sailfish are indeed highly predictable, but predictability rapidly declines with increasing group size because of a lack of population-level lateralization. Our results present a novel benefit of group hunting: by alternating attacks, individual-level attack lateralization can evolve, without the negative consequences of individual-level predictability. More generally, our results suggest that group hunting in predators might provide more suitable conditions for the evolution of strategy diversity compared to solitary life.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-318962 (URN)10.1016/j.cub.2016.12.044 (DOI)000394724600022 ()28190733 (PubMedID)
Available from: 2017-03-29 Created: 2017-03-29 Last updated: 2017-11-29Bibliographically approved
Herbert-Read, J. E., Romanczuk, P., Krause, S., Strömbom, D., Couillaud, P., Domenici, P., . . . Krause, J. (2016). Proto-cooperation: group hunting sailfish improve hunting success by alternating attacks on grouping prey. Proceedings of the Royal Society of London. Biological Sciences, 283(1842), Article ID 20161671.
Open this publication in new window or tab >>Proto-cooperation: group hunting sailfish improve hunting success by alternating attacks on grouping prey
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2016 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 283, no 1842, 20161671Article in journal (Refereed) Published
Abstract [en]

We present evidence of a novel form of group hunting. Individual sailfish (Istiophorus platypterus) alternate attacks with other group members on their schooling prey (Sardinella aurita). While only 24% of attacks result in prey capture, multiple prey are injured in 95% of attacks, resulting in an increase of injured fish in the school with the number of attacks. How quickly prey are captured is positively correlated with the level of injury of the school, suggesting that hunters can benefit from other conspecifics' attacks on the prey. To explore this, we built a mathematical model capturing the dynamics of the hunt. We show that group hunting provides major efficiency gains (prey caught per unit time) for individuals in groups of up to 70 members. We also demonstrate that a free riding strategy, where some individuals wait until the prey are sufficiently injured before attacking, is only beneficial if the cost of attacking is high, and only then when waiting times are short. Our findings provide evidence that cooperative benefits can be realized through the facilitative effects of individuals' hunting actions without spatial coordination of attacks. Such 'proto-cooperation' may be the pre-cursor to more complex group-hunting strategies.

Keyword
group hunting, sailfish, Istiophorus platypterus, cooperation, proto-cooperation
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-312086 (URN)10.1098/rspb.2016.1671 (DOI)000388718700009 ()
Available from: 2017-02-01 Created: 2017-01-04 Last updated: 2017-11-29Bibliographically approved
Herbert-Read, J. E. (2016). Understanding how animal groups achieve coordinated movement. ACTA CRYSTALLOGRAPHICA SECTION F-STRUCTURAL BIOLOGY COMMUNICATIONS, 72, 2971-2983.
Open this publication in new window or tab >>Understanding how animal groups achieve coordinated movement
2016 (English)In: ACTA CRYSTALLOGRAPHICA SECTION F-STRUCTURAL BIOLOGY COMMUNICATIONS, ISSN 2053-230X, Vol. 72, 2971-2983 p.Article, review/survey (Refereed) Published
Abstract [en]

Moving animal groups display remarkable feats of coordination. This coordination is largely achieved when individuals adjust their movement in response to their neighbours' movements and positions. Recent advancements in automated tracking technologies, including computer vision and GPS, now allow researchers to gather large amounts of data on the movements and positions of individuals in groups. Furthermore, analytical techniques from fields such as statistical physics now allow us to identify the precise interaction rules used by animals on the move. These interaction rules differ not only between species, but also between individuals in the same group. These differences have wide-ranging implications, affecting how groups make collective decisions and driving the evolution of collective motion. Here, I describe how trajectory data can be used to infer how animals interact in moving groups. I give examples of the similarities and differences in the spatial and directional organisations of animal groups between species, and discuss the rules that animals use to achieve this organisation. I then explore how groups of the same species can exhibit different structures, and ask whether this results from individuals adapting their interaction rules. I then examine how the interaction rules between individuals in the same groups can also differ, and discuss how this can affect ecological and evolutionary processes. Finally, I suggest areas of future research.

Keyword
Collective motion, Collective behaviour, Interaction rules, Leadership, Social responsiveness
National Category
Zoology
Identifiers
urn:nbn:se:uu:diva-309478 (URN)10.1242/jeb.129411 (DOI)000385758900009 ()
Funder
Knut and Alice Wallenberg Foundation, 2013.0072
Available from: 2016-12-05 Created: 2016-12-05 Last updated: 2017-02-20Bibliographically approved
Herbert-Read, J. E., Romenskyy, M. & Sumpter, D. J. T. (2015). A Turing test for collective motion. Biology Letters, 11(12), Article ID 20150674.
Open this publication in new window or tab >>A Turing test for collective motion
2015 (English)In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 11, no 12, 20150674Article in journal (Refereed) Published
Abstract [en]

A widespread problem in biological research is assessing whether a model adequately describes some real-world data. But even if a model captures the large-scale statistical properties of the data, should we be satisfied with it? We developed a method, inspired by Alan Turing, to assess the effectiveness of model fitting. We first built a self-propelled particle model whose properties (order and cohesion) statistically matched those of real fish schools. We then asked members of the public to play an online game (a modified Turing test) in which they attempted to distinguish between the movements of real fish schools or those generated by the model. Even though the statistical properties of the real data and the model were consistent with each other, the public could still distinguish between the two, highlighting the need for model refinement. Our results demonstrate that we can use 'citizen science' to cross-validate and improve model fitting not only in the field of collective behaviour, but also across a broad range of biological systems.

Keyword
collective motion, Alan Turing, citizen science
National Category
Bioinformatics and Systems Biology Evolutionary Biology Computational Mathematics
Identifiers
urn:nbn:se:uu:diva-274944 (URN)10.1098/rsbl.2015.0674 (DOI)000367482000003 ()
Funder
Knut and Alice Wallenberg Foundation, 2013.0072
Available from: 2016-01-26 Created: 2016-01-26 Last updated: 2017-11-30Bibliographically approved
Herbert-Read, J. (2015). Collective Behaviour: Leadership and Learning in Flocks. Current Biology, 25(23), R1127-R1129.
Open this publication in new window or tab >>Collective Behaviour: Leadership and Learning in Flocks
2015 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 25, no 23, R1127-R1129 p.Article in journal, Editorial material (Other academic) Published
Abstract [en]

A new study has decoded which birds become leaders in homing pigeon flocks, finding an unexpected benefit of leadership: faster birds emerge as leaders, and these leaders learn more about their environment than their followers.

National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-276925 (URN)10.1016/j.cub.2015.10.031 (DOI)000366388600008 ()
Available from: 2016-02-23 Created: 2016-02-16 Last updated: 2017-11-30Bibliographically approved
Herbert-Read, J. E., Buhl, J., Hu, F., Ward, A. J. W. & Sumpter, D. J. T. (2015). Initiation and spread of escape waves within animal groups. ROYAL SOCIETY OPEN SCIENCE, 2(4), Article ID 140355.
Open this publication in new window or tab >>Initiation and spread of escape waves within animal groups
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2015 (English)In: ROYAL SOCIETY OPEN SCIENCE, ISSN 2054-5703, Vol. 2, no 4, 140355Article in journal (Refereed) Published
Abstract [en]

The exceptional reactivity of animal collectives to predatory attacks is thought to be owing to rapid, but local, transfer of information between group members. These groups turn together in unison and produce escape waves. However, it is not clear how escape waves are created from local interactions, nor is it understood how these patterns are shaped by natural selection. By startling schools of fish with a simulated attack in an experimental arena, we demonstrate that changes in the direction and speed by a small percentage of individuals that detect the danger initiate an escape wave. This escape wave consists of a densely packed band of individuals that causes other school members to change direction. In the majority of cases, this wave passes through the entire group. We use a simulation model to demonstrate that this mechanism can, through local interactions alone, produce arbitrarily large escape waves. In the model, when we set the group density to that seen in real fish schools, we find that the risk to the members at the edge of the group is roughly equal to the risk of those within the group. Our experiments and modelling results provide a plausible explanation for how escape waves propagate in nature without centralized control.

Keyword
escape waves, collective animal behaviour, fish schools, self-organization
National Category
Mathematics
Identifiers
urn:nbn:se:uu:diva-303559 (URN)10.1098/rsos.140355 (DOI)000377965400006 ()26064630 (PubMedID)
Available from: 2016-10-14 Created: 2016-09-20 Last updated: 2017-02-20Bibliographically approved
Marras, S., Noda, T., Steffensen, J. F., Svendsen, M. B. S., Krause, J., Wilson, A. D. M., . . . Domenici, P. (2015). Not So Fast: Swimming Behavior of Sailfish during Predator-Prey Interactions using High-Speed Video and Accelerometry. Integrative and Comparative Biology, 55(4), 719-727.
Open this publication in new window or tab >>Not So Fast: Swimming Behavior of Sailfish during Predator-Prey Interactions using High-Speed Video and Accelerometry
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2015 (English)In: Integrative and Comparative Biology, ISSN 1540-7063, E-ISSN 1557-7023, Vol. 55, no 4, 719-727 p.Article in journal (Refereed) Published
Abstract [en]

Synopsis Billfishes are considered among the fastest swimmers in the oceans. Despite early estimates of extremely high speeds, more recent work showed that these predators (e.g., blue marlin) spend most of their time swimming slowly, rarely exceeding 2 m s(-1). Predator-prey interactions provide a context within which one may expect maximal speeds both by predators and prey. Beyond speed, however, an important component determining the outcome of predator-prey encounters is unsteady swimming (i.e., turning and accelerating). Although large predators are faster than their small prey, the latter show higher performance in unsteady swimming. To contrast the evading behaviors of their highly maneuverable prey, sailfish and other large aquatic predators possess morphological adaptations, such as elongated bills, which can be moved more rapidly than the whole body itself, facilitating capture of the prey. Therefore, it is an open question whether such supposedly very fast swimmers do use high-speed bursts when feeding on evasive prey, in addition to using their bill for slashing prey. Here, we measured the swimming behavior of sailfish by using high-frequency accelerometry and high-speed video observations during predator-prey interactions. These measurements allowed analyses of tail beat frequencies to estimate swimming speeds. Our results suggest that sailfish burst at speeds of about 7 m s(-1) and do not exceed swimming speeds of 10 m s(-1) during predator-prey interactions. These speeds are much lower than previous estimates. In addition, the oscillations of the bill during swimming with, and without, extension of the dorsal fin (i.e., the sail) were measured. We suggest that extension of the dorsal fin may allow sailfish to improve the control of the bill and minimize its yaw, hence preventing disturbance of the prey. Therefore, sailfish, like other large predators, may rely mainly on accuracy of movement and the use of the extensions of their bodies, rather than resorting to top speeds when hunting evasive prey.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-265833 (URN)10.1093/icb/icv017 (DOI)000362672100015 ()25898843 (PubMedID)
Available from: 2015-11-03 Created: 2015-11-03 Last updated: 2017-12-01Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0003-0243-4518

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