Heroes in a Half Shell: Butt Power!?

Turtles are neat.

They lay leathery eggs, have a shell that is fused to and developed from their ribcage, and range in size from teeny-tiny to 2,000-pound leatherbacks. The diverse range of habitats that different species live in has allowed for a highly variable collection of adaptations to evolve across turtle species around the world. For the purpose of this story, I'd like to mention two, starting with the more popular.

From Left to Right: Michelangelo, Raphael (front), Leonardo (back), and Donatello. Image from: TVtropes.com.

From Left to Right: Michelangelo, Raphael (front), Leonardo (back), and Donatello. Image from: TVtropes.com.

Closely sharing a habitat with a Japanese rat and having Renaissance inspired names, these strangely anthropomorphic creatures are a fantastical biological mystery. Dwelling within the New York City sewer system, the teenage mutant ninja turtle has certainly found its niche. While much focus has been on presenting the tumultuous aspects of their daily lives, I find myself interested in their physiology. With a 2 minute and 20 second time limit on the notoriously excruciating Nintendo underwater dam level, I have to wonder what’s the rush?

What is limiting their ability to breathe underwater?

Most animals, including humans, have one way (or one dominant way) to obtain oxygen from their environment. Tigers have lungs. Romeo, my handsome electric yellow African cichlid, has gills. It’s nice when things are simple, but it can be more interesting when they are complicated.

Of course we can hold our breath and go for a dive, but the mammalian body must go through a bunch of physiological adjustments underwater in an attempt to minimize oxygen consumption and acclimate to the challenge of no breathing. This is aptly named the “diving response”. Specialized animals like seals have evolved impressive adaptations that decrease heart rate and energy use, reduce cardiac output, and even redistribute blood flow to the most important places in the body. All of this helps to give aquatic mammals more time underwater as well as reach greater depths, useful skills when you must chase and successfully hunt your seafood dinner. But even seals eventually feel the pangs of oxygen depletion and hypercapnia (high carbon dioxide) and must return to the air to inhale.

Like Jordin Sparks, you may be saying to yourself,

Tell me how I’m supposed to breathe with no air.” 

 

Canal Street Sewer System, NYC. Image from: Observatoryroom.org.

Canal Street Sewer System, NYC. Image from: Observatoryroom.org.

For an animal with lungs, is there a way to breathe without air?

Well, oddly enough, the answer can be found by linking this question back to teenage, mutant, ninja turtles.

The habitat of these ninjutsu-trained reptiles is the sewer.

Diagram of basic turtle anatomy.  

Diagram of basic turtle anatomy.  

Etymology connects the word “sewer” to “cloaca”.

The cloaca is an anatomical structure that all reptiles possess. It’s a posterior opening that serves as the exit for the digestive and urinary tracts, as well as the opening for reproductive purposes.

 Simply put?

A butt.

 

What does a butt have to do with breathing?

Well my dear data monster friends, that’s exactly the question I wanted you to ask. Remember when I said that turtles are neat? They are about to get a whole lot neater.

I should start by saying many species of turtles are bimodal breathers. This means that they have two ways of getting oxygen (O2) and expelling carbon dioxide (CO2): either by way of the air and their lungs, or from the water through aquatic respiration. Turtles don’t have gills and have instead evolved the ability to exchange gases across skin, membranes in the mouth region, and for some… (here’s the clincher) within the cloaca. 

Tucked away inside the cloaca there are structures called bursae. These paired sac-like structures are lined with small projections called papillae, which serve to greatly increase surface area exposed to the aquatic environment. By contracting muscles in these nether-regions, water is passed over the cloacal bursae and O2 is extracted while CO2 is released. This has structural and functional parallels to the gills in fish, except it happens in the butt! It’s called cloacal respiration. It’s awesome, and there’s one species that is truly a professional.

Meet the Fitzroy River turtle (Rheodytes leukops).

Fitzroy River turtle, Rheodytes leukops. Image from: Queensland Blog.

Fitzroy River turtle, Rheodytes leukops. Image from: Queensland Blog.

Papillae covering the cloacal bursae.

Papillae covering the cloacal bursae.

Identified in 1980 by John M. Legler and John Cann, Rheodytes leukops (R. leukops) makes its home in the (you guessed it) Fitzroy River system in Queensland, Australia. This bottom-feeder is known for dives of impressive duration; reaching lengths of several hours, days, and even weeks. What allows R. leukops to maintain its oxygen levels and blood chemistry for this long? It is able to heavily utilize specialized cloacal bursae, acquiring up to around 70% of the total oxygen supply needed for survival from the water!

The morphology, or shape, of its cloacal bursae is considered modified relative to other diving turtles, more vascularized (meaning more blood flow) with a greater number of long papillae that are multi-branching and covering their surface. The more papillae, the more surface area, and the more efficiently oxygen obtained from the water.

Because the Fitzroy River turtle is able to readily obtain oxygen from the surrounding water, it is able to maintain aerobic energy production (meaning in the presence of O2) within the cells of its body. This is a good situation because aerobic respiration is the most efficient route of producing the energy molecules needed to fuel all the processes we take for granted in our bodies (and in those of turtles). If you’ve ever experienced those nagging cramps in your abdomen during a long run in the park, you may recognize it as the result of infamous lactic acid build-up. Lactic acid, or lactate, is a nasty byproduct of our bodies working to keep producing energy while not enough oxygen is floating around in our blood (anaerobic conditions). So by not having to resort to anaerobic means, our friend R. leukops avoids accumulation of lactate and prevents the otherwise problematic shift in blood pH! But it gets cooler!

Butt biology to blood biochemistry.

When specific characteristics of their blood itself were compared to that of other closely related turtle species, R. leukops showed some specialized differences. They had a much higher concentration of hemoglobin molecules in their blood; almost double the amount in some cases. Hemoglobin functions to hold and carry oxygen molecules around the body, delivering them where necessary, so the more hemoglobin, the greater oxygen carrying capacity! Going along with this, it has also been found that the Fitzroy’s plentiful hemoglobin molecules themselves may have a higher oxygen affinity, meaning they are able to more readily attract and bind oxygen from the water! 

In general, respiration by extra-pulmonary means (other than the lungs) is suggested to help prevent hypercapnia (accumulation of CO2), provide an additional route for nitrogen excretion, and help maintain internal ion and acid/base balance in turtles. When you put all this into perspective, the biological ability of the Fitzroy River turtle to rely on cloacal respiration may be a result of the evolutionary push of its ecology. Specialized anatomy and blood chemistry allows it to extend the time it has to dive for food, lessens the need to surface (thereby saving energy), and reduces competition for valuable resources by allowing it to inhabit areas where others cannot.

Screenshot from the Teenage Mutant Ninja Turtles Nintendo video game circa 1989.

Screenshot from the Teenage Mutant Ninja Turtles Nintendo video game circa 1989.

Maybe if Michelangelo or Leonardo could have utilized cloacal respiration, Nintendo game designers may have allowed just a little more time underwater.

 

For now, I can only hope that my questions of teenage mutant ninja turtle biology get answered in the future …

... but I’m not holding my breath.