Quantifying the Speed of Chromatophore Activity at the Single-Organ Level in Response to a Visual Startle Stimulus in Living, Intact Squid

Stavros P. Hadjisolomou,Rita W. El-Haddad,Alla Chavarga,Kamil Kloskowski,Israel Abramov

doi:10.3389/fphys.2021.675252

Stavros P. Hadjisolomou, Rita W. El-Haddad + Show 3 more

Open Access

https://doi.org/10.3389/fphys.2021.675252

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Abstract

The speed of adaptive body patterning in coleoid cephalopods is unmatched in the natural world. While the literature frequently reports their remarkable ability to change coloration significantly faster than other species, there is limited research on the temporal dynamics of rapid chromatophore coordination underlying body patterning in living, intact animals. In this exploratory pilot study, we aimed to measure chromatophore activity in response to a light flash stimulus in seven squid, Doryteuthis pealeii. We video-recorded the head/arms, mantle, and fin when squid were presented with a light flash startle stimulus. Individual chromatophores were detected and tracked over time using image analysis. We assessed baseline and response chromatophore surface area parameters before and after flash stimulation, respectively. Using change-point analysis, we identified 4,065 chromatophores from 185 trials with significant surface area changes elicited by the flash stimulus. We defined the temporal dynamics of chromatophore activity to flash stimulation as the latency, duration, and magnitude of surface area changes (expansion or retraction) following the flash presentation. Post stimulation, the response’s mean latency was at 50 ms (± 16.67 ms), for expansion and retraction, across all body regions. The response duration ranged from 217 ms (fin, retraction) to 384 ms (heads/arms, expansion). While chromatophore expansions had a mean surface area increase of 155.06%, the retractions only caused a mean reduction of 40.46%. Collectively, the methods and results described contribute to our understanding of how cephalopods can employ thousands of chromatophore organs in milliseconds to achieve rapid, dynamic body patterning.

Highlights

Unlike the slower chromatophore control of flatfish (2–8 s; Ramachandran et al, 1996), coleoid cephalopods can change body patterns in milliseconds
D. pealeii with uniform light skin patterns before stimulation responded to flashes with jetting and chromatophore expansion and lower flash intensities triggered transient darkening in the absence of jetting
Our results demonstrate that it is feasible to use intact, living animals, to measure, non-invasively, the temporal dynamics of chromatophore control during body patterning

Summary

Introduction

Unlike the slower chromatophore control of flatfish (2–8 s; Ramachandran et al, 1996), coleoid cephalopods can change body patterns in milliseconds. Scientists in the field of cephalopod vision have focused on the goal of creating a complete characterization of the sophisticated coleoid body patterning abilities. As a result, existing reports are sufficient to describe and explain several known body patterns in cephalopods for camouflage and communication (Hanlon and Messenger, 1988; Hanlon, 2007; Langridge et al, 2007; Zylinski et al, 2009; How et al, 2017). A theoretical framework on cephalopod body patterning, which does not include the dimension of time, will be inherently inadequate in modeling, holistically, the range of dynamic, rapid transformations observed in animals living in the wild. One approach toward studying this topic is by stimulating the visual system of a living, intact animal, using a light flash to elicit muscular activation of chromatophores, and quantifying the response dynamics by tracking surface area changes in time

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