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.

Keywords: behavioral ecology; deep-sea biology; social evolution; visual signaling.

Fig. 1.

Pigmentation patterning associated with foraging and group behaviors in D. gigas. (A and B) PCA and vectors of chromatic components with 50% probability ellipses encircling foraging status clusters (A) and conspecific abundance clusters (B). In both, each of the 30 squid is represented by a point that is colored by foraging status and shaped by conspecific abundance category with proximity indicating behavioral similarity. Red arrows and abbreviations represent the vectors, or relative contribution of different components to the behavioral trends among squid. Var., variation. (C) Venn diagram illustrating the ecological context under which squid utilized specific chromatic components based on component vectors and other PCA results (Materials and Methods). (D) Examples of various chromatic components analyzed in this study. See Table 1 for component abbreviations. In this study, foraging and not foraging distinguish whether or not a squid attempted to capture prey.

Fig. 2.

Consistencies in the arrangement of pigmentation patterns during foraging in D. gigas. (A and B) Representative images of arm strike (A) and tentacle strike (B), the two stereotyped strategies squid used to capture prey. (C and D) PCAs and vectors of postures (C) and locomotion (D) with 50% probability ellipses encircling foraging status clusters. In both, each D. gigas (n = 30) is represented by a point that is colored by foraging status and shaped by conspecific abundance category, with proximity indicating behavioral similarity. Red arrows and abbreviations represent the vectors, or relative contribution of different components to the behavioral trends among squid. Var., variation. (E) The frequency of chromatic components displayed by foraging squid, or those that attempted to capture prey (n = 15), with respect to prey-capture attempts (shaded in purple). The general suite of postures and locomotion is also illustrated. (F–H) Adjacency network heatmaps of chromatic (F), postural (G), and locomotor (H) components displayed by squid during the 4 s preceding and following prey-capture attempts, with loops (i.e., prolonged, single-component display) removed to highlight transitions between different components. Color denotes the number of occurrences that squid transitioned from components on the vertical axes to components on the horizontal axes (warmer, more adjacencies; paler, fewer adjacencies). See Table 1 for component abbreviations.

Fig. 3.

Proposed mechanism by which pigmentation patterns can function as visual signals under low-light conditions. (A) Spatial patterns of s.c. photophore density and size with respect to pigmentation-changing regions in D. gigas. A, Insets are images of photophores illuminated from below using white light. Arrows point to individual photophores. (Scale bars, 0.5 cm.) In the plot, light gray and dark gray boxes and points indicate regions dominated by small or large photophores, respectively. Dark horizontal lines show the mean value, with boxes and vertical lines, respectively, representing the two inner and outer quartiles of the data (shown as points) (n = 4). Examples of pigmentation patterns corresponding to regions with higher than average photophore density are included beneath the plot. (B and C) Fluorescence of s.c. photophores in the fins and mantle tip (B) and along the mantle (C) (photos: Steven Haddock, MBARI). Photophores were illuminated by blue (465 nm) light with a yellow long-pass filter used on the camera lens. See Table 1 for component abbreviations.