Monday, March 4, 2013

Living Life at Sea: Diving Physiology in Marine Turtles


By: Morgan Ivens-Duran

Last week, Michael DeLea (check out his recent post on ecological consequences of the exotic pet trade here) and I were in charge of assigning papers for our graduate seminar on how species distributions are shifting with climate change. Given my interest in marine ecology and his interest in reptiles, we decided to meet in the middle and talk about turtles. In addition to having a great discussion last Thursday evening, those papers got me thinking about diving physiology in sea turtles. How deep do turtles dive, and how long do they stay underneath the surface of the ocean? How do they cope with the stresses of continued submergence?
  
Green sea turtle (Chelonia mydas). From http://seapics.com/assets/pictures/020965-450-green-sea-turtle.jpg

It turns out that there are two general classifications of marine organisms that exhibit diving behavior. The first, “divers” includes animals such as sea otters. These organisms spend most of their time near the surface of the water and dive in order to forage for food. Marine turtles are an exemplar of the second type of marine diver, known as “surfacers.” Turtles spend 98% of their time underwater, only rising to the surface to forcefully exhale and then re-fill their lungs, often in a single breath.

Sea otter (Enhydra lutris) foraging in a kelp forest. From http://s4.hubimg.com/u/5829975_f520.jpg 

In order to understand how turtles can stay submerged so much of the time while inhaling so little oxygen, it’s important to understand the difference between endotherms and ecotherms. Endotherms are animals who's internal heat primarily comes from their metabolism. So, as a whale descends, experiencing progressively colder water temperatures, its rate of respiration increases in order to keep its body warm. This depletes its oxygen reserves and decreases the period of time the whale can stay submerged while still performing aerobic (with oxygen) respiration. By contrast, an ectotherm's internal heat primarily comes from their environment. So, as a turtle descends, the cold temperature of the water depresses its rate of respiration because the enzymes that catalyze these reactions slow down, and so the organism uses its oxygen stores at a slower rate. This difference in respiration rates increases the aerobic dive limit (ADL), or the amount of time an animal can spend underwater before it uses up its stores of oxygen, of ecotherms relative to endotherms.

So, we’ve been talking about oxygen stores, but we haven’t discussed exactly how a diving animal stores oxygen. To start with a familiar example, humans gulp air at the surface and hold it in our lungs for as long as possible as we swim. Unless you’re a competitive swimmer, you generally return to the surface fairly quickly as your lungs start to burn, signaling that the air in your lungs is becoming low in oxygen and high in carbon dioxide, a waste product of respiration. 

Diving animals have two different strategies. Hard-shelled turtles, every species of marine turtles except for the leatherback (Dermochelys coriacea), use their lungs as their main reservoir of oxygen during dives. However, marine turtles have a smaller relative lung size as compared to their terrestrial and aquatic relatives, which initially seems counterintuitive. If they are relying on their lungs to store oxygen during a dive, shouldn’t the lungs be relatively large? The answer is, maybe.

Having smaller lungs decreases the buoyancy of the turtle at the surface, making it easier to swim down. If you’ve ever tried to swim to the bottom of the pool with an inflatable ring around your waist, you know how much harder it is to descend with that extra buoyancy. But, turtles aren’t necessarily sacrificing oxygen storage by having smaller lungs. They have secondary folds in their lung tissue that increases the surface area available for gas exchange, even with a smaller lung volume.  

Leatherback sea turtle (Dermochelys coriacea). From http://nmlc.org/wp-content/uploads/2011/07/leatherback.jpg.

Most other marine divers, including the leatherback turtle, rely on oxygen stored in their blood and tissue rather than the oxygen in their lungs. Why does the diving strategy of leatherbacks differ from their marine turtle relatives? The key is dive depth. Most hard-shelled turtles dive to a maximum of 25 meters, while leatherbacks routinely dive much deeper and for longer periods of time. One leatherback has been recorded diving to 1,186 meters (nearly 4,000 feet)! Of course, as you move down in the water column, not only does the water get colder, but the pressure increases. Check out this video showing a Styrofoam cup collapsing as a remotely operated submersible carries it from the surface to 3,000 feet (approximately 1,000 meters). A similar process can happen with deep-diving marine organisms such as leatherback turtles. At these extreme depths, the hydrostatic pressure collapses the animal’s lungs, and any oxygen that was stored there is no longer available. 

A styrofoam cup before (left) and after (right) compression at 2,660 meters. From  http://schooloftheabyss.blogspot.com/2012/06/compressed-styrofoam-cups.html

Earlier, I mentioned the difference between aerobic and anaerobic respiration. For a long time, researchers thought that turtle dives were primarily anaerobic. However, a study by Gatten (1981) showed that, at least in freshwater turtles, the high levels of lactate (a by-product of anaerobic respiration) after dives were an artifact of taking measurements during forced rather than voluntary dives. Subsequent research showing low lactate levels and short surface intervals after dives has verified that marine turtles primarily use aerobic respiration. In addition to fundamentally altering our understanding of turtle diving physiology, Gatten’s work brings up another important point broadly applicable to all physiology studies. Many physiologu studies rely on correctly assessing the effort level of an organism. When working with human subjects, this is easier to ascertain. But when working with animals, there is always a level of uncertainty. It’s important to keep in mind that there can be a very real difference in results based on forced versus voluntary behaviors. 

Hopefully you’ve enjoyed learning about marine turtle diving physiology as much as I’ve enjoyed sharing it with you. I want to close this blog post with a brief word about turtle conservation. Between 1990 and 2008, at least 85,000 marine turtles have died as “bycatch,” caught in nets or on hooks set for other species. That number is likely a severe underestimate, with the true value 2 orders of magnitude higher. Even though marine turtles are well adapted to life at sea, and can dive to great depths for much longer than we can, turtles trapped underwater for too long can still drown. 

Turtles tangled in a net. From http://www.destination-scuba.com/images/greenturtlesbycatch.jpg.
Turtle snared on a longline hook. From http://www.southernfriedscience.com/wp-content/uploads/2011/04/longline-turtle.jpg

What can you do to help? Pay attention to where your seafood comes from. Programs such as Seafood Watch by the Monterey Bay Aquarium (for more information, click here) evaluate the sustainability of fisheries worldwide to help you make responsible choices that, among other things, reduce the amount of bycatch. And that helps keep these intriguing organisms around for generations to come. 


Green sea turtle (Chelonia mydas). From http://seaturtles.org/img/original/GRN-honuAnitaWintner.jpg

Literature Cited

Brischoux, F., X. Bonnet, T.R. Cook, and R. Shine. 2008. Allometry of diving capabilities: ectothermy vs. endothermy. Journal of Evolutionary Biology 21:324-329.

Hays, G.C., C.R. Adams, A.C. Broderick, B.J. Godley, D.J. Lucas, J.D. Metcalfe, and A.A. Prior. 2000. The diving behavior of green turtles at Ascension Island. Animal Behavior 59:577-586.

Hochscheid, S., B.J. Godley, A.C. Broderick, and R.P. Wilson. 1999. Reptilian diving: highly variable dive patterns in the green turtle Chelonia mydas. Marine Ecology Progress Series 185:101-112.

Hochsheid, S., C.R. McMahon, C.J.A. Bradshaw, F. Maffucci, F. Bentivegna, and G.C. Hays. 2007. Allometric scaling of lung volume and its consequences for marine turtle diving performance. Comparative Biochemistry and Physiology 148:360-367.

López-Mendilaharsu, M., C.F.D. Rocha, A. Domingo, B.P. Wallace, and P. Miller. 2009. Prolonged, deep dives by the leatherback turtle Dermochelys coriacea: pushing their aerobic dive limits. JMBA2 Biodiversity Records 1-3.

Luctavage, M.E., P.G. Bushnell, and D.R. Jones. 1990. Oxygen transport in the leatherback sea turtle Dermochelys coriacea. Physiological Zoology 63(5):1012-1024.

Lutz, P.L and T.B. Bentley. 1985. Respiratory Physiology of Diving in the Sea Turtle. Copeia 1985(3): 671-679.

Wallace, B.P., R.L. Lewison, S.L. McDonald, R.K. McDonald, C.Y. Kot, S. Kelez, R.K. Bjorkland, E.M. Finkbeiner, S. Helmbrecht, and L.B. Crowder. 2010. Global patterns of marine turtle bycatch. Conservation Letters 3:131-142.


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