Cuttlefish perform multiple agonistic displays to communicate a hierarchy of threats

Abstract: Many animals produce multiple displays during agonistic interactions, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis has been proposed to explain their occurrence and posits that different displays convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. This hypothesis suggests that low-risk signals, typically performed at the beginning stages of an interaction, are strong predictors of high-risk signals but weak predictors of physical aggression. High-risk signals, typically produced at later stages of an interaction, are strong predictors of physical aggression. We used giant Australian cuttlefish, Sepia apama, to test these predictions. We combined field observations and laboratory video playback experiments to determine whether (i) male cuttlefish produce specific sequences of displays, (ii) displays in early stages of an interaction predict displays in later stages of an interaction, and (iii) displays produced in later stages of an interaction provide reliable predictors of physical aggression. Field observations suggested that males progressed from low-risk to high-risk signals (i.e., visual signaling to physical aggression). Video playback results zrevealed that the low-risk frontal display, produced during early stages of an interaction, conveys reliable information about the cuttlefish’s intent to escalate to later stages of visual signaling. Both the shovel and lateral displays were produced during the later stages of signaling and were reliable predictors of subsequent physical aggression. Our study supports the hierarchical signaling hypothesis and provides new empirical insights into how cuttlefish use progressive visual signaling to convey increasing levels of threat. Significance statement: Many animals perform multiple displays during fights, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis posits that animals produce multiple displays to convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. We tested this hypothesis in giant Australian cuttlefish, Sepia apama. Specifically, we tested whether (i) displays in early stages of a fight predict displays in later stages of a fight and (ii) displays produced in later stages of a fight provide reliable predictors of physical aggression. Our results support these predictions and reveal that fighting cuttlefish progress from low-risk signals to high-risk signals to convey a hierarchy of threats. This study highlights the generality of hierarchical signaling during animal contests, as cuttlefish are evolutionary far removed from many of the species that have been reported to use this type of signaling.