Defensive Behaviors of Deep-sea Squids: Ink Release, Body Patterning, and Arm Autotomy

The deep sea is the largest habitat on Earth and holds the majority of its' animal biomass. Due to the limitations of observing, capturing and studying these diverse and numerous organisms, little is known about them. The majority of deep-sea species are known only from net-caught specimens, therefore behavioral ecology and functional morphology were assumed. The advent of human operated vehicles (HOVs) and remotely operated vehicles (ROVs) have allowed scientists to make one-of-a-kind observations and test hypotheses about deep-sea organismal biology. Cephalopods are large, soft-bodied molluscs whose defenses center on crypsis. Individuals can rapidly change coloration (for background matching, mimicry, and disruptive coloration), skin texture, body postures, locomotion, and release ink to avoid recognition as prey or escape when camouflage fails. Squids, octopuses, and cuttlefishes rely on these visual defenses in shallow-water environments, but deep-sea cephalopods were thought to perform only a limited number of these behaviors because of their extremely low light surroundings. The Monterey Bay Aquarium Research Institutes' ROVs were used to determine whether or not deep-sea squids are limited in their behaviors compared to their shallow-water relatives. First, eighteen species of deep-sea squids were observed to release ink when encountered by an ROV (Chapter 2). Ink release was observed from the surface to below 1800 m and included six types of ink release, some of which have not been observed from shallow-water cephalopods. Ink release could serve as a visual defense by blocking the cephalopods' silhouette or bioluminescence stimulated by the squids' movement, or causing predators to confuse ink pseudomorphs with potential prey. It could also, or instead, have a chemical function by having distasteful or noxious qualities, blocking predator olfactory senses, stimulating feeding behaviors, or functioning as an attractant so that predators attack the ink. To investigate potential chemical functions, ink collected from deep-sea and shallow-water cephalopods was analyzed using liquid chromatography - mass spectroscopy (Chapter 3). The goal was to compare ink chemical composition between species to see if deep-sea species or a few particular species had vastly different chemical compositions that may warrant further investigations. An ethogram - a catalogue of every behavior a species performs - of the deep-sea squid Octopoteuthis deletron Young 1972 was produced from over eight hours of ROV video footage of 76 individuals (Chapter 4). Octopoteuthis deletron is capable of numerous color, posture, and locomotor changes. Individuals can also change patterns of bioluminescence produced by their arm-tip photophores, leading to the first description of bioluminescence as a cephalopod behavioral component. Additional work was performed with O. deletron to determine if this species can autotomize arms (Chapter 5). ROV observations, laboratory and in situ experimentation, and histological sectioning were conducted. Octopoteuthis deletron can autotomize any of the eight arms at numerous points along the length. This species is the first squid described to autotomize arms, has the uncommon capability of economy of autotomy, and is one of very few animals that can perform attack autotomy. Our understanding of cephalopod behavioral ecology has been greatly advanced by the research presented here. The hypotheses that deep-sea squids do not release ink and that their defensive behaviors are very limited were both falsified. Clearly there is much additional work to be done on these and other deep-sea animals to understand the ecology of the deep sea