Breathing for two

Mammals aren't the only ones that give birth to live young. There are many examples of fish, sharks and rays that do it too (just to name the vertebrates!). Some of these also form placentas, like some poecilid fishes and carcharhinid sharks. For those that don't, there's a variety of ways that mothers supply their developing offspring with oxygen, some of them better known than others. A new paper on manta rays provide some new and interesting information about gas exchange between mother and offspring.

Manta rays and their relatives do not form a placenta. Instead, the uterine wall allows gaseous exchange between the mother's blood stream and the amniotic fluid. What wasn't clear, until the new paper, was how oxygen was getting from the amniotic fluid into the developing embryo. The authors from the Okinawa Churaumi Aquarium, in Japan, were fortunate enough to get their hands on a live, pregnant manta ray caught accidentally by fishermen. And, as you do, they placed her in a shallow tank and took an ultrasound of the embryo.

The ultrasound revealed something really interesting. It suggested that the embryo was breathing in a manner quite unlike the way that adult manta rays do. Adult manta rays breath by ram ventilation, that is they push water over their gills as they swim forward with their mouth open. In contrast, the embryo was breathing by dropping the floor of its mouth to suck water in and then closing its mouth to push the water back over its gills, which is known as buccal pumping.

The top panel is a sequence of ultrasound images showing the opening and closing of the mouth in the embryo. The lower panel shows a 3 dimensional images reconstructed from CT-scan data and displayed in the same orientation as the ultrasound images (image taken from the paper).

Sharks and rays that breath using buccal pumping typically have a larger spiracle, a hole near the top of the head behind the eyes. The spiracle acts like a second mouth to help draw water in. It's generally larger in species that live on the bottom, but is reduced or absent in species that are active in mid-water and those that rely more on ram ventilation. Adult manta rays have a spiracle that is reduced to a small slit, but new born manta rays, and presumably embryos, have one that's more reminiscent of an animal that uses buccal pumping to breath.

The spiracle opening of a new born manta ray, Manta alfredi, above and the same structure in an adult below (image taken from the paper)

The authors argue that because the manta ray embryo has no direct connection to the mother that the buccal pumping behaviour must, therefore, be for respiration. And that the rapid loss of the spiracle after birth indicates a shift from respiration by buccal pumping to respiration by ram ventilation. Buccal pumping respiration is also known in embryos of egg-laying species and it may be the dominant type of respiration among sharks and rays that do not form a placenta.

Tomita, T., Toda, M., Ueda, K., Uchida, S., & Nakaya, K. (2012). Live-bearing manta ray: how the embryo acquires oxygen without placenta and umbilical cord Biology Letters DOI: 10.1098/rsbl.2012.0288