Bioluminescent backlighting illuminates the complex visual signals of a social squid in the deep sea

Abstract

Visual signals rapidly relay information, facilitating behaviors and ecological interactions that shape ecosystems. However, most known signaling systems can be restricted by low light levels—a pervasive condition in the deep ocean, the largest inhabitable space on the planet. Resident visually cued animals have therefore been hypothesized to have simple signals with limited information-carrying capacity. We used cameras mounted on remotely operated vehicles to study the behavior of the Humboldt squid, Dosidicus gigas, in its natural deep-sea habitat. We show that specific pigmentation patterns from its diverse repertoire are selectively displayed during foraging and in social scenarios, and we investigate how these behaviors may be used syntactically for communication. We additionally identify the probable mechanism by which D. gigas, and related squids, illuminate these patterns to create visual signals that can be readily perceived in the deep, dark ocean. Numerous small subcutaneous (s.c.) photophores (bioluminescent organs) embedded throughout the muscle tissue make the entire body glow, thereby backlighting the pigmentation patterns. Equipped with a mechanism by which complex information can be rapidly relayed through a visual pathway under low-light conditions, our data suggest that the visual signals displayed by D. gigas could share design features with advanced forms of animal communication. Visual signaling by deep-living cephalopods will likely be critical in understanding how, and how much, information can be shared in one of the planet’s most challenging environments for visual communication.

The limits of convergence in the collective behavior of competing marine taxa

“…Pacific sardine has several spots running along its lateral surface (Figure 1b ), while California market squid produces a large repertoire of stereotyped pigmentation patterns involving stripes and splotches (Hunt et al, 2000 ; Zeidberg, 2004 ). Pigmentation patterning in fish could have signaling value during collective movements, determine group behaviors, facilitate organization, and reinforce unification (Pavlov & Kasumyan, 2000 ), and the same may be true of social squid (Burford & Robison, 2020 ; Hanlon & Messenger, 2018 ). High alignment in both squid and sardine could therefore indicate behavioral convergence in collective motion in these species due to the functional importance of information transfer.…”

“…About 50% of fish species are known to live in groups for at least part of their lives, and many of these species exhibit collective motion (Pavlov & Kasumyan, 2000 ). For squid species that have been studied in sufficient detail (e.g., commercially important, epipelagic, and/or nearshore species), 82% (58 species) are known to form social groups (Burford et al, 2019 ; Burford & Robison, 2020 ; Jereb & Roper, 2010 ). Of these social squids, some are capable of collective motion, as evidenced by video, laboratory, and acoustic studies of group organization and observations of coordinated group movements (Adamo & Weichelt, 1999 ; Benoit‐Bird & Gilly, 2012 ; Hurley, 1978 ; Mather & O’Dor, 1984 ; Moynihan & Rodaniche, 1982 ; Sugimoto & Ikeda, 2012 ; Sugimoto et al, 2013 ).…”

Bioluminescence and Photoreception in Unicellular Organisms: Light-Signalling in a Bio-Communication Perspective

“…For example, communication through visual signals is widespread in the animals that display various degrees of social behaviours. Many properties of light such as colours, skin patterns, iridescence and bioluminescence have been developed by evolution for intra- or inter-species signalling [ 421 , 422 , 423 , 424 , 425 , 426 , 427 , 428 ]. While intra-species communication generally involves social interactions and mating, inter-species communication mediates symbiotic relationships or shapes ecosystem interactions.…”

Glowing Plants Can Light Up the Night Sky? A Review

“…Luminescence is a common physical phenomenon to create light, which was discovered among more than 10,000 species, i.e., bacteria, fungi, protists and animals (Desjardin et al, 2008;Haddock et al, 2010;Meighen, 1991). Luminescence is a kind of specific communication approaches for signaling, such as alarming predators (Burford & Robison, 2020), trapping prey (Verdes & Gruber, 2017;Wainwright & Longo, 2017) and attracting mates (Ellis & Oakley, 2016). During the past years, it was found that fluorescent proteins (FPs) and bioluminescent systems are responsible for induction of most native luminescence (Kim & Paulmurugan, 2021).…”