Beside changing color, cuttlefish can also change the texture of their skin by raising little skin papillae. This cuttlefish raised two papillae above its eye and many more over its body to give its skin a rough and granular texture.
Figure 7 from Samson et al., 2014: the experimental set-up. A: Schematic side view with tank (1), net (2), speaker (3), calibration ruler (4), outflow pipe (5), and HD camera (6). B: video frame as recorded by the HD camera.
Sound is a widely available and very important source of information in aquatic environments. Underwater sounds travel relatively fast (~1,500 m/s) and can be detected over long distances, making them a preferred sensory cue for organisms living in low-light conditions and/or organisms communicating over distances too large to be spanned by chemical cues. Most bioacoustic research has focused on sound use and production in marine mammals, especially (toothed) whales and dolphins, because of their social behavior and their ability to echolocate. Sound, however, is also vastly used and produced by marine invertebrates, from crustacean and coral larvae to snapping shrimp.
Cephalopods (cuttlefish, squid, octopus, and their relatives) form a very varied group of molluscs occupying a wide range of habitats, from coastal to pelagic waters and the deep sea. They are most famous for camouflaging skills and their ability to communicate visually through amazing body patterns and color changes, but very little is known about their ability to use acoustic cues, for example in predator evasion. So we set out to test their hearing abilities.
Figure 2 from Samson et al., 2014: types of behavioral responses to sound. A: cuttlefish at rest before the sound stimulus. B: jetting and inking. C: darkening and fast fin movements.
Cuttlefish have three types of chromatophores (red, brown, and yellow) that they expand and shrink to display different body patterns. Below the chromatophore layer, iridophores reflect light and produce iridescent colors, as can be seen on the underside of this cuttlefish.
We started with the common cuttlefish (Sepia officinalis) and then reproduced the experiments with the longfin inshore squid (Doryteuthis pealeii). We played sounds with frequencies ranging from 80 to 1000 Hz and sound pressure levels from 110 to 165 dB* to individual animals and recorded their behavior. The most extreme responses (inking and jetting away) were elicited by lower-frequency sounds, up to about 300 Hz. This lower sound range is also where most maritime activity takes place: commercial shipping, oil drilling, or seismic airgun testing for example.
As anthropogenic activity increases in oceans and seas worldwide, it is important to evaluate the impact of noisier waters on marine ecosystems. Cephalopods occupy a key position in food webs, linking small fish and invertebrates (which they eat) to bigger fish, marine mammals, birds, and humans (which eat them). A shift in the cephalopod population, for example to escape a noisy environment, could have very disruptive effects on local food webs and ecosystems.
*It is important to note that the decibel (dB) is a unit representing the ratio between two values of a physical quantity, in this case the sound pressure level (SPL) measured during the experiment and the reference SPL. The reference SPL is 1 µPa for sounds in water and 20 µPa for sounds in air, so 165 dB in water is not the same as 165 dB in air. In fact, we would experience a 165 dB sound in water as being a lot less loud than the same sound at 165 dB in air.
A cuttlefish enjoying the outdoor sun in what I like to call the "wise elephant" pose. Cuttlefish swim by undulating the fins on each side of their bodies and/or using their funnel to jet away in any direction. In this picture, one can see the left fin gently undulating.
About this project
What started as a 3-month master research internship quickly became a full-time research project that kept me busy for almost two years.
From December 2011 to March 2012, I worked on my internship project with Dr. T. Aran Mooney at the Woods Hole Oceanographic Institution and Dr. Roger T. Hanlon at the Marine Biological Laboratory in Woods Hole, MA, and Dr. Sander W. S. Gussekloo from the Experimental Zoology Group at Wageningen University, the Netherlands. After a mandatory post-graduation vacation, I continued spending time in Woods Hole, running experiments, analyzing data, and raising baby cuttlefish.
This project resulted in several conference presentations and publications (see below) and was also featured in several media, in particular the Dutch National Geographic magazine.
Publications from this project
Mooney, T. A., Samson, J. E., Schlunk, A. D., Zacarias, S. (2016) Loudness-dependent behavioral responses and habituation to sound by the longfin squid (Doryteuthis pealeii), Journal of Comparative Physiology A, 202 (7): 489-501.
>> Find this paper here or on Researchgate.
Samson, J. E., Mooney, T. A., Gussekloo, S. W. S., Hanlon, R. T. (2016) A brief review of cephalopod behavioral responses to sound. In Effects of Noise on Aquatic Life II (eds. A. N. Popper, A. Hawkins), Advances in Experimental Medicine and Biology vol. 875, Springer 969-975.
>> Find this book chapter here or on Researchgate.
Samson, J. E., Mooney, T. A., Gussekloo, S. W. S., Hanlon, R. T. (2014) Graded behavioral responses and habituation to sound in the common cuttlefish Sepia officinalis, Journal of Experimental Biology, 217 (24): 4347-4355.
>> Find this paper here or on Researchgate.