Sleeping with one eye open – the Delphinidae and curious sleep phenomena
The family Delphinidae, known commonly as the oceanic dolphins, are a clade of toothed whales (Odontoceti) within the order Cetacea. Most people have a decent understanding of what dolphins are, being smaller than most whales, and entirely carnivorous. Like all Cetacea, the dolphins are marine mammals with terrestrial ancestors. DNA sequence data and fossil evidence indicate that millions of years ago, these ancestors (Artiodactyl – even-toed ungulates) made the transition from a land-dwelling to aquatic lifestyle. The extreme change of environment resulted in selection pressures forming a diverse range of adaptations that allow the Delphinidae and close relatives to survive in the oceans. Some of these adaptations are quite well understood, while others are currently the subject of intense research and debate among scientists.
I’d like to give a quick introduction to two fairly obvious adaptations (body-shape and skin-shedding) to give you a taste of the problems faced by marine mammals, and the adaptations that have evolved to solve them. Then, I’d like to take a look at something I find most interesting: the evolution of some truly weird and wonderful sleep phenomena.
We’ll start with the most obvious. A common adaptation in marine mammals is a fusiform (sleek, streamlined) body shape. Even the polar bear has a relatively more fusiform shape than other species of bears. The marine environment makes quick movement difficult due to the drag and resistance caused by the water. A fusiform body shape aids swimming and this is essential for members of the Delphinidae as they chase and catch fast-moving prey such as schools of fish. Both the fusiform shape of dolphins and their reduced limb size decreases the drag of water resistance. A common theme in Delphinidae research is that an adaptation often helps solve more than one environmental problem. Selection pressures may have also brought about the fusiform shape due to thermoregulation. A lot of body heat is lost to the ocean, so marine mammals have evolved a range of adaptations in order to conserve heat efficiently. The fusiform shape decreases the organism’s surface area exposed to the environment, and this reduces heat loss. In fact, we see evidence for this adaptation when we observe the species in deeper, cooler waters that tend to have larger bodies and smaller flippers than coastal species.
The benefits of a fusiform body shape have been relatively well understood for many years. Other phenotypic traits of the Delphinidae have only recently been intensively studied and new explanations for adaptations are emerging. One curious trait is the speed that dolphins shed their skin. Most animals such as insects and reptiles shed a whole layer of skin in one rapid growth known as moulting. In contrast, us mammals continuously shed individual dead skin cells. This process can take a couple of days to completely replace all the dead skin on the mammalian body in most terrestrial species. Dolphins replace every dead skin cell on their body within 2 hours. This striking difference in the rate of sloughing has interested many biologists, but also physicists. This is a fine example of researchers studying naturally evolved solutions to problems and developing new technologies that improve our vehicles and other applications. For example, scientists have looked at how birds and insects fly when trying to develop efficient technologies for air travel. Similarly, some physicists are interested in knowing what adaptations allow dolphins to maximize their speed in water in the hopes that future technologies could mimic the adaptations. As mentioned previously, dolphins have adaptations that allow them to maximize swimming speed in order to catch prey and avoid predators. Hypothesizing that the dramatic rate of sloughing aided swimming speed, scientists in Japan used sophisticated computer simulations modeling every single skin cell and exactly how each is shed from the body of a dolphin. These techniques revealed that the soft, “waviness” of dolphin skin reduces drag and shedding often maintains this condition. More importantly for their own research, they also discovered that drag was reduced significantly because of the shed skin reducing turbulence. The tiny flakes of skin that are lost end up reducing the number-density of hairpin vortices that occur in the flow around the surface of the skin. With less hairpin vortices forming, the drag is once again reduced and the dolphin’s swimming speed is increased. This knowledge might someday be useful in the future design of boats or submarines and underwater equipment.
So, body-shape and the speed of skin-shedding have evolved to help survive in a marine environment. As you can imagine, these characteristics wouldn’t have been found in the terrestrial ancestors. Switching to life in the oceans has required some dramatic changes in body-structure. But we can see these adaptations before our very eyes. We’re talking about fairly obvious physical structures. To discuss the adaptations that I find most curious, we need to consider the less obvious, and think about what’s happening in the brain.
A hot topic in Delphinidae research is the neurological activity and behaviour associated with sleep. Dolphins are known to sleep for 33% of the day. All mammals sleep, but many marine mammals, including all the Cetacea and therefore Delphinidae, demonstrate unusual sleep phenomena not seen among terrestrial mammals. Viewing the various sleep phenomena of Cetaceans as adaptations to a marine lifestyle, biologists have also recently been attempting to identify the original selection pressures that may explain their evolution. Unfortunately, mental processes and behaviour aren’t the most obvious things to discover from the fossil record.
Sleeping behaviour has been observed in whales and dolphins for almost a century. In the early 20th century it was already understood that dolphins sometimes slept with one eye open, and sometimes appeared to sleep while still swimming. Early attempts to explain these behaviours resulted in many novel ideas (especially during the 60s) including the hypothesis that dolphins were capable of unihemispheric sleep, and that breathing was a voluntary process. Dolphins have a brain with two hemispheres, like all mammals. In 1964, J.C. Lilly believed that dolphins were able to put one hemisphere of their brain to sleep while the other stayed awake, explaining why one eye would remain open during these times. His explanation was that breathing was entirely voluntary in dolphins, and they therefore needed to stay partially awake at all times in order to swim to the surface to take a breath when required. Since the 1960s, Lilly’s novel ideas regarding unihemispheric sleep have been confirmed by strong evidence, but his ideas about voluntary breathing have been rejected. Even so, this research still isn’t well understood by many non-scientists and it is still a very common misunderstanding that dolphins only breath voluntarily. It simply isn’t true.
Complex anesthetizing experiments performed by McCormick in 1969 contradicted Lilly’s earlier prediction, and demonstrated that the respiration of dolphins can be cortically controlled or autonomic, just like other mammals. McCormick also demonstrated that while sleeping with one hemisphere at a time, dolphins are partially aware of their surroundings, able to react to other organisms, and swim continuously. It turns out that all Cetacea are capable of unihemispheric sleep (and lack REM). Biologists obviously felt this dramatic characteristic might be explained by the extreme environment the dolphins have evolved to survive, but the adaptation first had to be understood before selection pressures could be considered.
Unihemispheric slow wave sleep (USWS) in dolphins (seen in the image above) is characterized by the brain producing slow delta waves in one hemisphere, while the other half shows reduce voltage activity. Put simply: dolphins sleep with one side of their brain at a time, rather than putting both sides to sleep like we do. In the bottlenose dolphin, Tursiops truncatus, each half of the brain sleeps for approximately 4 hours a day. On the theoretical basis that this interhemispheric EEG asymmetry was an adaptation to an aquatic environment, studies began to focus on other aquatic mammals (non-Cetaceans). Since the 1980s, sleep has been studied extensively in pinnipeds, manatees, the walrus, the sea otter, and even the hippopotamus, and it turns out USWS isn’t exclusive to the Cetacea. All pinnipeds belonging to the family Otariidae were shown to sleep unihemispherically. USWS was also observed in the the walrus and the manatees. Entirely different clades of aquatic mammals with unique terrestrial origins demonstrated USWS, which could be interpreted as evidence that it is a convergently evolved adaptation to the aquatic environment. Further evidence is that the fur seal, Callorhinus ursinus, shows great variability in its sleeping behaviour. USWS is observed in this species while it sleeps in water, but ordinary bihemispheric sleep (like ours) occurs when sleeping on land. Several proposals have been made for the selection pressures that may have driven these sleep adaptations for an aquatic environment.
The first possibility is that USWS evolved simply due to the necessity to breathe. For most mammals, sleeping results in a relatively stationary state. Just picture yourself sleeping in bed. If dolphins fell fully asleep underwater and didn’t move, they would drown, unable to reach the surface. But during USWS, dolphins are able to move freely and swim to the surface to breathe when required. Diazepam can induce bilateral slow wave sleep (like ours) in dolphins, and they are unable to breathe in this state, despite clearly trying to. This means dolphins have evolved to the point where USWS is now required for them to breathe. USWS may have evolved in order to assist breathing, but a much simpler solution seen in other aquatic mammals is to dramatically improve how long breath can be held, and sleep through that period. Perhaps necessity to breathe played a role in the evolution of USWS, but it seems likely that there were other pressures involved.
A second possibility is that USWS evolved to aid sentinel behaviour even while asleep. The ancestors of dolphins and other modern Cetacea made the transition gradually from terrestrial to fully aquatic. Some ancestors would have spent some time on land and in water. Eventually, some of the early aquatic ancestors would have spent all their time in the water, but would not yet have evolved the adaptations required to dive for long periods of time. These ancestors would have to sleep at the surface of the water, where aquatic animals are most at risk of predation. By keeping one eye open and remaining partially awake, the ancestor could watch for danger while getting some sleep at the same time. This may help explain the evolution of USWS together with loss of REM.
Marine mammals can be difficult to study because they live in such an extreme environment. New discoveries are being made every year, but clearly there is still much to be learned. Some adaptations are well understood, but these are often examples of adapted physical anatomy. The evolution of behaviour and neurology are harder to study because behaviour and sleep do not fossilize. Biologists have taken steps to understanding the early evolution of these adaptations we see in modern Delphinidae and close relatives, but there is still a lot of debate over which selection pressures were more powerful in shaping the dolphins we see today. Judging from the burst of research seen recently, perhaps we’ll be more confident of the answers in a few short years. Or maybe not. I’ll keep an eye on it.
Lilly, J. C. (1964). Animals in aquatic environments: adaptations of mammals to the ocean. In: Handbook of Physiology (ed. Dill, D. B.), pp 741-747. Environment, American Physiology Society, Washington, DC.
Lyamin, O. I. and Chetyrbok, I. S. (1992). Unilateral EEG activation during sleep in the cape fur seal, Arctocephalus pusillus. Neurosci. Lett., 143, pp. 263–266.
Lyamin, O. I., Manger, P. R., Mukhametov, L. M., Siegel, J. M. and Shpak, O. V. (2000). Rest and activity states in a grey whale. J. Sleep Res, 9, pp. 261–267.
Lyamin, O. I., Manger, P. R., Ridgway, S. H., Mukametov, L. M. and Siegel, J. M. (2008). Cetacean sleep: An unusual form of mammalian sleep. Neuroscience and Biobehavioral Reviews, Volume 32, Issue 8, pp1451-1484.
Lyamin, O. I., Mukhametov, L.M., Chetyrbok, I. S. and Vassiliev, A. V. (2002). Sleep and wakefulness in the southern sea lion. Behav. Brain Res, 128, pp. 129–138.
Lyamin, O. I., Mukhametov, L. M. and Siegel, J. M. (2004). Relationship between sleep and eye state in Cetaceans and Pinnipeds. Arch. Ital. Biol., 142, pp. 557–568.
Lyamin, O. I., Pryaslova, J. P., Kosenko, O., Lapierre, J. L., Mukhametov, L. M. and Siegel, J. M. (2006). Sleep and rest states in the walrus. Abstract Book of the 34th Annual Symposium of European Association for Aquatic Mammals, pp. 14.
Lyamin, O. I. and Siegel, J. M. (2005). Rest and activity states in the hippopotamuses. Abstract Book of the 33rd Annual Symposium of European Association for Aquatic Mammals, pp. 15.
McCormick, J. G. (1969). Relationship of sleep, respiration, and anesthesia in the porpoise: a preliminary report. Proc. Natl. Acad. Sci. U.S.A., 62, pp. 697–703.
McCormick, J. G. (2007). Behavioral Observations of Sleep and Anasthesia in the Dolphin: Implications for Bispectral Index Monitoring of Unihemispheric Effects in Dolphins. Anasthesia and Analgesia, Volume 104, No.1, 239-241.
Mukhametov, L. M., Supin, A. Y. and Polyakova, I. G. (1984). Sleep in Caspian seals (Phoca caspica). J. High Nerve Activity, 34, pp. 259–264.
Nagamine, H. (2004). Turbulence modification by compliant skin and strata-corneas desquamation of a swimming dolphin. Institute of Physics, Journal of Turbulence, volume 5, no.18.
Ridgway, S. H. (1990). The Central Nervous System of the Bottlenose Dolphin. In: The Bottlenose Dolphin 1990 (ed. Leatherwood, S. and Reeves, R. R.), pp. 69-97. San Diego: Academic Press, Inc.
Ridgway, S. H. (1972). Mammals of the Sea. Biology and Medicine. Springfield, Illinois, Charles C. Thomas.
Ridgway, S. H., Houser, D., Finneran, J., Carder, D., Keogh, M., van Bonn, W., Smith, C., Scadeng, M., Dubowitz, D., Mattery, R. and Hoh, C. (2006). Functional imaging of dolphin brain metabolism and blood flow. J. Exp. Biol., 209, pp. 2902–2910.
Sokolov, V. E. and Mukhametov, L. M. (1982). Electrophysiological study of the sleep on the manatee, Trichechus manarts. J. Evol. Biochem. Physiol., 18, pp. 191–193.