(C) PLOS One
This story was originally published by PLOS One and is unaltered.
. . . . . . . . . .



Schooling of light reflecting fish [1]

['Assaf Pertzelan', 'Faculty Of Life Sciences', 'Ben Gurion University', 'Beer-Sheva', 'The Interuniversity Institute For Marine Sciences At Eilat', 'Iui', 'Eilat', 'Gil Ariel', 'Department Of Mathematics', 'Bar-Ilan University']

Date: 2023-08

Abstract One of the hallmarks of the collective movement of large schools of pelagic fish are waves of shimmering flashes that propagate across the school, usually following an attack by a predator. Such flashes arise when sunlight is reflected off the specular (mirror-like) skin that characterizes many pelagic fishes, where it is otherwise thought to offer a means for camouflage in open waters. While it has been suggested that these ‘shimmering waves’ are a visual manifestation of the synchronized escape response of the fish, the phenomenon has been regarded only as an artifact of esthetic curiosity. In this study we apply agent-based simulations and deep learning techniques to show that, in fact, shimmering waves contain information on the behavioral dynamics of the school. Our analyses are based on a model that combines basic rules of collective motion and the propagation of light beams in the ocean, as they hit and reflect off the moving fish. We use the resulting reflection patterns to infer the essential dynamics and inter-individual interactions which are necessary to generate shimmering waves. Moreover, we show that light flashes observed by the school members themselves may extend the range at which information can be communicated across the school. Assuming that fish pay heed to this information, for example by entering an apprehensive state of reduced response-time, our analysis suggests that it can speed up the propagation of information across the school. Further still, we use an artificial neural network to show that light flashes are, on their own, indicative of the state and dynamics of the school, and are sufficient to infer the direction of attack and the shape of the school with high accuracy.

Citation: Pertzelan A, Ariel G, Kiflawi M (2023) Schooling of light reflecting fish. PLoS ONE 18(7): e0289026. https://doi.org/10.1371/journal.pone.0289026 Editor: Pilwon Kim, UNIST: Ulsan National Institute of Science and Technology, REPUBLIC OF KOREA Received: January 10, 2023; Accepted: July 9, 2023; Published: July 21, 2023 Copyright: © 2023 Pertzelan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the paper and its Supporting information files. Funding: The author(s) received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist.

1. Introduction Free-ranging animals that move in large aggregates, such as schooling fish and flocking birds, are often required to maneuver in unison to evade attacking predators. The collective evasive maneuvers change macroscopic properties of the aggregate, such as its direction, polarization, and density [1–4]. These changes are often manifested as “waves of agitation” or “escape waves” that follow the propagation of information regarding the attack across the aggregate. The complex inter-individual interactions, which bring about such large-scale dynamical patterns, are not fully understood [2–4]. One of the main empirical obstacles to a fuller understanding of these interactions and the consequent escape dynamics is the difficulty of tracking individuals within very large schools; using either cameras (e.g. [5]) or sonars [2, 5]. Large schools of silvery fish are common in the world’s oceans [6]. When swimming close to the surface, the specular (mirror-like) skins of these fish will often reflect direct sunlight. To an underwater observer, these reflections appear as highly conspicuous flashes of light (Fig 1), which increase the fish’s contrast by at least one order of magnitude [7]. When under attack, an agitation wave crossing a school of specular fish, may appear as a shimmering wave of flashes (e.g. Fig 1). The wave arises as the succession of evasive maneuvers by neighboring school members momentarily brings their bodies to an angle that reflects the sun in the direction of the observer [1–4]. As such, shimmering waves could contain information regarding the dynamics of the school and individuals within it, which is more discernable than the actual trajectories of the individual fish. For example, the dark bands typical of agitation waves in starling flocks, which are analogous to shimmering waves, have been used to measure wave intensity and propagation speeds [8]. PPT PowerPoint slide

PNG larger image

TIFF original image Download: Fig 1. Propagation of an agitation (shimmering) wave in a school of A. lacunosus (top-right corner), filmed at 60 frames per second. The flashes arise when the fish, initially facing to the left, turn into the school (here into the page, perpendicular to the advancing wave), causing their body to face the observer at just the right angle to generate a flash of reflected sunlight. The wave propagates as the decision to turn is taken sequentially by the fish, starting from the left. Bottom-left corner: a “predator’s view” of the wave, taken from a camera mounted on a spear shot into the school. The video clips, from which the snapshot were taken, were filmed while snorkeling along the shoreline of the Golf of Eilat, using Sony RX100 IV and Paralenz Dive Cameras. See S1 and S2 Videos for the actual video clips. https://doi.org/10.1371/journal.pone.0289026.g001 In this paper, we use individual-based simulations to study the dynamics of shimmering-waves. We begin by testing whether a shimmering wave can arise in possible schooling scenarios. We continue by addressing the possibility that flashes observed by the fish themselves can be used to induce apprehension and, thereby, speed-up the transfer of information within the school. We then continue to test the complementary question of whether the dynamic properties of the waves (e.g., their duration and speed of propagation) can be used to differentiate between competing hypotheses relating to the inter-individual interactions that give rise to them; as well as to infer the occurrence and direction of an attack. Fish schools under attack In schooling fish, the response to an attack amounts to moving closer together or rolling sideways [1–3]. Once initiated, waves of agitation often propagate faster than the speed at which individuals are moving within the group; a phenomenon often referred to as the ’Trafalgar effect’ [9]. In cases where the stimulus is an approaching predator, the waves have also been found to travel faster than the predator itself [4]. Surprisingly, waves can travel even faster than expected given the estimated response-latencies [3], i.e., the time between the perception of the stimulus and the fear/escape response. The unexpected speed of information-transfer led to speculations regarding possible mechanisms that enhance synchrony and extend beyond the scale of localized social interactions. A prominent example is the “chorus-line hypothesis” [10], which assumes a reduction in latency due to a heightened state of anticipation. Importantly, the flashes of light reflected off specular fish are visible not only from outside the school but also from within it; and thus, could potentially serve to inform the school members themselves. Indeed, it has been previously hypothesized that the reflective structures on fish can be used for “communicating information on relative positions, orientations, and movements between neighbors” [11]. Here, we explore a hypothesis that the heightened state of anticipation described above is caused by changes in the pattern of reflected light, as perceived by school members found downstream of the propagating wave. Particularly, we propose that observing a large change in the number of flashes reduces the latency and, as a result, speed-up the propagation of information. Modelling schools under attack Standard models of schooling typically fall short of generating agitation waves following localized perturbations, such as an attacking predator; presumably because the perturbation is perceived by only a small number of agents [4, 12]. In most models (for example the three-zones model e.g. [13–15]), individuals modify their position and direction based on the average response of neighboring agents. As a result, the initial reaction to the perturbation is “averaged out” [1–3, 12], i.e., the response of an agent close to the perturbation is averaged with agents that are farther away and, thus, did not perceive it. As most agents are far from the perturbation, the intensity of the reaction decreases with distance. Indeed, subsequent models have shown that additional responses, that are not due to a direct observation of the predator but leads to preemptive evasive maneuvers, are needed in order to generate agitation waves [3, 8, 12]. For example, [12] assumed that when an agent sees another agent whose behavior is clearly different from other school members, it will copy its behavior. With this added behavioral component, information of an approaching predator can propagate through the school, forming a response wave that travels at a (approximately) constant speed [4]. The agitation wave gives rise to a collective evasive response, even though the number of individuals that directly experience the perturbation is small [12]. The simulations introduced below accommodate the three basic local-interaction rules which are typically included in collective-motion models (repulsion, attraction, and alignment), as well as the copy response suggested in [12]. On this collective-motion model we superimpose a ray-tracing model [7] that ‘records’ the light-flashes perceived from a pre-prescribed location, either within or outside the school. To the best of our knowledge, our model is the first attempt to model shimmering waves, based on first principles of light propagation and reflectance. The paper is organized as follows. Section 2 describes the basic methodology underlying our modeling and simulation. More specific details are provided at the beginning of each of the three subsequent sections (3,4 and 5), and in the S1 File. Sections 3,4 and 5 focus on the results pertaining to our three main objectives. In section 3, we demonstrate that the model successfully produces shimmering waves using realistic parameter values (Table 1); contingent on the inclusion of a copy response, i.e. consistent with [12]. We then test, in section 4, the hypothesis that the shimmering wave caused by an attack can: 1) be seen by fish found downstream from the propagating wave; and, were the fish to use this information, 2) leave a discernable signature in the dynamics of the waves. In section 5 we demonstrate the ability to distinguish between different characteristics of the school, based only on observed flash patterns. The characteristics we focus on include: the direction of the attack, the shape of the school, and the underling rules of motion used by the individual; and in particular the use of the flash signature as input. We discuss our results in section 6. PPT PowerPoint slide

PNG larger image

TIFF original image Download: Table 1. Translation of the simulation parameters to real-world values. https://doi.org/10.1371/journal.pone.0289026.t001

6. Discussion The main goal of this work is three-fold. First, to establish whether models of schooling fish can generate realistic flash waves that propagate across the school in response to an attack. Second, to explore the possibility that school members are using this source of information themselves, and test how that can, in principle, affect the attack-response behavior. Third, to demonstrate that flash patterns indeed contain accessible information relating to the dynamics of the school, the behavior of individuals within it (in particular, their response to threats) and to the nature of the attack. Overall, the simulations provide a proof-of-concept which demonstrates that, on the one hand, flash patterns are indeed indicative of the state and dynamics of the school and the behavior of the individuals that compose it; and, on the other hand, that the flashes may be an important causative factor in shaping the escape behavior of the fish. Models of collective motion typically view the propagation of information as proceeding at a highly localized scale (e.g. [36–39]). This raises fundamental questions on the efficiency of information transfer within schools. First, noise and measurement errors may add up over long distances so that the signal (or information), for example regarding an approaching predator, is lost or averaged out. For this reason, it has been hypothesized that natural flocks are in a critical state, which implies long range correlations, that can extend over the entire flock [40–42]. Such models are motivated by models of statistical physics in which the interaction is instantaneous [43]. Such an assumption is not realistic in natural groups, including fish schools. For example, the reaction time of a typical fish is around 5–150 msecs [21]. This sets theoretical bounds on the possible speed of propagation of information within a school. It has long been suggested that, at least in some examples, the actual speed of propagation may be higher [4]. To this end, based on observations of dunlin (Calidris alpina), Potts [10] suggested a “chorus-line” hypothesis according to which “individuals observe the approaching maneuver wave and time their own execution to coincide with its arrival”. From a mechanistic perspective, this suggests long-range instantaneous transfer information, even if very limited. However, the rapid attenuation of light underwater (as opposed to the situation in air [44, 45]) implies that the mechanism suggested for birds, is not relevant for fish. Our results suggest light flashes as a plausible mechanism for a “chorus-line” effect in near-surface schooling fish. As demonstrated in our simulations, light flashes, due to their high contrast [7], can act as macroscopic, long-distance, many-to-one emergent signaling. Moreover, it may play a role in synchronizing the schooling fish. We explore two hypothesis regarding the information fish can retrieve from a propagating wave of flashes, and their possible response to it. First, if the fish can infer the direction of an attack, as with the flash-direct model, fish can act accordingly and start preemptive measure to escape the attack. Such a response would alleviate the assumption of criticality because the information travels directly from its source, rather than from each individual to its neighbor. Alternatively, as with the flash-latency model, the critical state may still be required for the information to propagate across the school. In this case, fish only use the flash to increase the propagation speed, as discussed above. A similar idea was been proposed for flocks of starlings (Sturnus vulgaris) [46], in which the group converges to a marginal opacity state where the rate of visible sky provides to the individual information which is complementary to the one it gets from local interactions. Our results show that flash-signatures convey enough information to differentiate between schooling scenarios. Event-detection, individual motion rules, properties of school geometries, and their combinations, could all be explored using the flash signature of schools. These results pave the way to empirical studies of flash waves and other flash-patterns. As we demonstrated using simulations, analyzing flash patterns as they appear for an external observer may also provide insight to the underlying decision-making process of the individuals, and hence bypass, at least partially, the need to track the trajectories of individuals. The abilities demonstrated in this study together with the fact that these flashes may be perceivable by the fish, lead to a possibility that a complex and rich flash-language is awaiting to be discovered, which is possibly already in use by the schooling fish and their predators.

[END]
---
[1] Url: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0289026

Published and (C) by PLOS One
Content appears here under this condition or license: Creative Commons - Attribution BY 4.0.

via Magical.Fish Gopher News Feeds:
gopher://magical.fish/1/feeds/news/plosone/

You are viewing proxied material from magical.fish. The copyright of proxied material belongs to its original authors. Any comments or complaints in relation to proxied material should be directed to the original authors of the content concerned. Please see the disclaimer for more details.