Evidence for tactile 3D shape discrimination by octopus.

Octopuses integrate visual, chemical and tactile sensory information while foraging and feeding in complex marine habitats. The respective roles of these modes are of interest ecologically, neurobiologically, and for development of engineered soft robotic arms. While vision guides their foraging path, benthic octopuses primarily search "blindly" with their arms to find visually hidden prey amidst rocks, crevices and coral heads. Each octopus arm is lined with hundreds of suckers that possess a combination of chemo- and mechanoreceptors to distinguish prey. Contact chemoreception has been demonstrated in lab tests, but mechanotactile sensing is less well characterized. We designed a non-invasive live animal behavioral assay that isolated mechanosensory capabilities of Octopus bimaculoides arms and suckers to discriminate among five resin 3D-printed prey and non-prey shapes (all with identical chemical signatures). Each shape was introduced inside a rock dome and was only accessible to the octopus' arms. Octopuses' responses were variable. Young octopuses discriminated the crab prey shape from the control, whereas older octopuses did not. These experiments suggest that mechanotactile sensing of 3D shapes may aid in prey discrimination; however, (i) chemo-tactile information may be prioritized over mechanotactile information in prey discrimination, and (ii) mechanosensory capability may decline with age.

Cyclic nature of the REM sleep-like state in the cuttlefish Sepia officinalis.

Sleep is a state of immobility characterized by three key criteria: an increased threshold of arousal, rapid reversal to an alert state and evidence of homeostatic 'rebound sleep' in which there is an increase in the time spent in this quiescent state following sleep deprivation. Common European cuttlefish, Sepia officinalis, show states of quiescence during which they meet the last two of these three criteria, yet also show spontaneous bursts of arm and eye movements that accompany rapid changes in chromatophore patterns in the skin. Here, we report that this rapid eye movement sleep-like (REMS-like) state is cyclic in nature. Iterations of the REMS-like state last 2.42±0.22 min (mean±s.e.m.) and alternate with 34.01±1.49 min of the quiescent sleep-like state for durations lasting 176.89±36.71 min. We found clear evidence that this REMS-like state (i) occurs in animals younger than previously reported; (ii) follows an ultradian pattern; (iii) includes intermittent dynamic chromatophore patterning, representing fragments of normal patterning seen in the waking state for a wide range of signaling and camouflage; and (iv) shows variability in the intensity of expression of these skin patterns between and within individuals. These data suggest that cephalopods, which are mollusks with an elaborate brain and complex behavior, possess a sleep-like state that resembles behaviorally the vertebrate REM sleep state, although the exact nature and mechanism of this form of sleep may differ from that of vertebrates.

Sexually mature cuttlefish are attracted to the eggs of conspecifics.

Cuttlefish typically are solitary, but form aggregations to spawn. We tested the hypothesis that bioactive factors in the eggs of conspecifics may facilitate the formation of spawning groups of Sepia officinalis. Cuttlefish detected odors from cuttlefish eggs, resulting in an increased ventilation rate. Extracts from female ovaries induced the largest increase in ventilation rate, suggesting that this organ could be a potential source of the bioactive chemicals. In y-maze assays, sexually mature, but not subadult, cuttlefish, were attracted to odors of cuttlefish eggs. These data suggest that Sepia eggs could be a source of reproductive pheromones.

Early exposure to odors changes later visual prey preferences in cuttlefish.

Developmental studies have shown that environmental stimulation received by a developing sensory system can alter the developmental outcome of both that sensory system and other aspects of the nervous system. We investigated the ecologically relevant question of whether prior exposure to prey early in development within one sensory modality could influence later prey choice within a different sensory modality. Cuttlefish are visual predators; they can detect prey odors but attacks on prey cannot be elicited without visual stimulation. Cuttlefish eggs were exposed to the odor of shrimp (preferred prey), crabs (non-preferred prey), mollusks (non-prey), or a seawater control (no prey). Seven days after hatching, prey preferences were tested with a visual choice test between crabs and shrimp. Hatchlings exposed to crabs odors and the seawater control were significantly more likely to attack shrimp. Hatchlings exposed to mollusk odors showed no visual prey preference, while those exposed to shrimp preferentially attacked crabs. These results demonstrate a complex relationship between an early sensory exposure and later prey preference

Short-distance navigation in cephalopods: a review and synthesis.

This paper provides a short overview of the scientific knowledge concerning short-distance navigation in cephalopods. Studies in laboratory controlled conditions and observations in the field provide converging evidence that cephalopods use visual cues to navigate and demonstrate spatial memory. A recent study also provides the first evidence for the neural substrates underlying spatial abilities in cuttlefish. The functions of spatial cognition in cephalopods are discussed from an evolutionary standpoint.

Experimental evidence that ovary and oviducal gland extracts influence male agonistic behavior in squids.

Recent investigations of sensory and behavioral cues that initiate sexual selection processes in the squid Loligo pealeii have determined that egg capsules deposited on the substrate provide a strong visual and chemotactile stimulus to males, even in the absence of females (1, 2, 3). The visual stimulus of egg capsules attracts males to the eggs, and when the males touch the eggs, they encounter a chemical stimulus that leads to highly aggressive fighting behavior. We have recently demonstrated that egg capsule extracts implanted in artificial egg capsules elicit this aggressive behavior (4). In this communication, we present evidence that the salient chemical factor originates in the ovary and perhaps the oviducal gland of the female reproductive tract.

A preliminary analysis of sleep-like states in the cuttlefish Sepia officinalis.

Sleep has been observed in several invertebrate species, but its presence in marine invertebrates is relatively unexplored. Rapid-eye-movement (REM) sleep has only been observed in vertebrates. We investigated whether the cuttlefish Sepia officinalis displays sleep-like states. We find that cuttlefish exhibit frequent quiescent periods that are homeostatically regulated, satisfying two criteria for sleep. In addition, cuttlefish transiently display a quiescent state with rapid eye movements, changes in body coloration and twitching of the arms, that is possibly analogous to REM sleep. Our findings thus suggest that at least two different sleep-like states may exist in Sepia officinalis.

Extreme aggression in male squid induced by a ß-MSP-like pheromone.

Male-male aggression is widespread in the animal kingdom and subserves many functions related to the acquisition or retention of resources such as shelter, food, and mates. These functions have been studied widely in the context of sexual selection, yet the proximate mechanisms that trigger or strengthen aggression are not well known for many taxa. Various external sensory cues (visual, audio, chemical) acting alone or in combination stimulate the complex behavioral interactions of fighting behaviors. Here we report the discovery of a 10 kDa protein, termed Loligo ß-microseminoprotein (Loligo ß-MSP), that immediately and dramatically changes the behavior of male squid from calm swimming and schooling to extreme fighting, even in the absence of females. Females synthesize Loligo ß-MSP in their reproductive exocrine glands and embed the protein in the outer tunic of egg capsules, which are deposited on the open sea floor. Males are attracted to the eggs visually, but upon touching them and contacting Loligo ß-MSP, they immediately escalate into intense physical fighting with any nearby males. Loligo ß-MSP is a distant member of the chordate ß-microseminoprotein family found in mammalian reproductive secretions, suggesting that this gene family may have taxonomically widespread roles in sexual competition.

Contact chemosensory cues in egg bundles elicit male-male agonistic conflicts in the squid Loligo pealeii.

Male Loligo pealeii engage in frequent agonistic bouts to gain access to female mates while aggregated at communal egg beds. Male squids are attracted to eggs in the field and in the laboratory. It was recently demonstrated that visual detection followed by physical contact with egg capsules elicited male-male aggression. We tested specific physical and chemical features of the egg capsules that may cause this strong behavioral reaction. Male squids were presented with either natural or artificial egg stimuli and scored for four selected behaviors (egg touch, egg blowing, forward-lunge grab, and fin-beating), the last two of which are highly aggressive behaviors. First, squids were presented with natural eggs versus eggs sealed in agarose-coated tubes (ESACT), which eliminated both tactile and chemical stimuli. Second, males were presented with natural eggs versus eggs sealed in agarose coated tubes containing C18 Sep-Pak-purified extracts (TCPE) from squid egg capsules, which provided chemical cues from natural eggs without the physical stimulus of the egg capsules. Third, natural eggs versus heat-denatured eggs were tested to determine whether the active factor in natural eggs is heat-labile. Squids responded aggressively when contacting natural eggs and TCPE, whereas squids did not respond after touching ESACT or denatured eggs. These results suggest that aggressive behavior is elicited by a heat-labile factor that is embedded within squid egg capsules. This chemosensory cue appears to be a contact pheromone that stimulates the agonistic interactions that characterize the mating behavior of migratory squids on inshore spawning grounds.