Embryonic exposure to predator odour modulates visual lateralization in cuttlefish

Abstract

Predation pressure acts on the behaviour and morphology of prey species. In fish, the degree of lateralization varies between high-and low-predation populations. While lateralization appears to be widespread in invertebrates, we do not know whether heredity and early experience interact during development as in vertebrates. Here we show, for the first time, that an exposure to predator odour prior to hatching modulates visual lateralization in newly hatched cuttlefish. Only cuttlefish that have been exposed to predator odour display a left-turning bias when tested with blank seawater in a T-shaped apparatus. Exposure to predator odour all the incubation long could appear as an acute predictor of a high-predation surrounding environment. In addition, cuttlefish of all groups display a left-turning preference when tested with predator odour in the apparatus. This suggests the ability of cuttlefish to innately recognize predator odour. To our knowledge, this is the first clear demonstration that lateralization is vulnerable to ecological challenges encountered during embryonic life, and that environmental stimulation of the embryo through the olfactory system could influence the development of subsequent visual lateralization.

Behavioral development in embryonic and early juvenile cuttlefish (Sepia officinalis)

“…They can then use this information to prepare for the post‐hatching environment. Indeed, several experiments have found that predator and prey stimuli strongly influence juvenile behavior (e.g., Darmaillacq, Lesimple, & Dickel, ; Guibé, Dickel, & Boal, ; Guibé, Poirel, Houdé, & Dickel, ; Jozet‐Alves et al, ; Jozet‐Alves & Hébert, ). Careful field observations documenting the identity and prevalence of other species at spawning sites would be extremely useful in piecing together a picture of the sensory experience of embryos during development.…”

“…Lateralization is the tendency to process information through one side of the brain in a particular type of situation. Potentially, lateralization yields advantages in speed and efficiency of information processing via the specialization of each side of the brain (Jozet‐Alves & Hébert, ). Lateralization is seen in numerous vertebrates, including primates, birds, fishes, and amphibians.…”

Asymmetry of brain and behavior in animals: Its development, function, and human relevance

“…Olfactory and auditory experience may also influence the development of lateralization. Indeed, it has been shown recently that laterality of turning behavior in the cuttlefish Sepia officinalis is modulated by exposing the eggs to the odor of seabass, a predator of the species (Jozet‐Alves and Hébert, ). Left side turning bias in the hatched cuttlefish is enhanced by this chemosensory experience.…”

When and Why Did Brains Break Symmetry?

“…There has also been an elegant demonstration of experience affecting lateralization in an invertebrate species, the cuttlefish [57]. Exposure of cuttlefish to the odour of a predator throughout the incubation period prior to hatching leads to the development of a left-turning preference, even when the cuttlefish are tested in water that has no odour of a predator present.…”