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Sharkbites Saturday

The shark and the side salad

Everyone knows all sharks are carnivores. Or are they?

Leigh, SC, YP Papastamatiou, and DP German. 2018. Seagrass digestion by a notorious ‘carnivore’. Proceedings of the Royal Society B Biological Sciences 285:20181583 http://dx.doi.org/10.1098/rspb.2018.1583

A leafy history

Bonnethead sharks (Sphyrna tiburo) are one of the most abundant coastal shark species in the United States, with an estimated 4.9 million individuals living in the coastal U.S. Atlantic and Gulf of Mexico. Beyond the U.S., they range as far south as Uruguay in the Atlantic and Northern Peru in the Pacific. This small member of the hammerhead family spends most of its time in seagrass meadows and sandy bottom habitats in relatively shallow water, making them fairly accessible for research.

A bonnethead shark swims through an aquarium exhibit (Wikimedia Commons).

For decades, biologists found seagrass in the stomachs of bonnethead sharks while studying their diet. It was always assumed that the seagrass was accidentally swallowed while the sharks were consuming their target prey, mainly crabs, shrimp, and other small crustaceans, and that the sharks received no nutritional benefit from consuming seagrass. Because all sharks are carnivores…right?

Dana Bethea and her collaborators were the first to suggest that seagrass, accidentally swallowed or not, could play an important role in bonnethead diets. In 2007, she noted that plant material was often the second most abundant item found in bonnethead stomachs behind crabs. In fact, for newborn bonnetheads it could comprise up to 62% of their stomach contents. Often the plant material recovered from stomach dissections appeared to be partially digested and she speculated that the bonnetheads could be able to digest seagrass, but to be sure this needed to be tested in the lab.

The experiment

This is where Samantha Leigh and her collaborators come into play. Samantha collected bonnetheads in the field and brought them into a lab setting where she could control their diets to determine if they were capable of digesting and gaining nutrients from seagrass. For three weeks she fed the sharks a controlled diet of 90% seagrass and 10% squid. The seagrass was cultivated in a lab so that it contained a traceable carbon isotope, carbon 13 (13C). An isotope is essentially an atom of an element that contains a different number of neutrons in the nucleus than expected, changing its atomic mass. The atomic mass of carbon is usually 12, meaning that carbon usually has six protons and six neutrons in its nucleus. The 13C isotope simply contains an extra neutron in its nucleus and occurs infrequently in nature. If the bonnetheads were able to digest the cultivated seagrass they would have elevated 13C concentrations in their bodies. To track changes in the shark’s 13C concentrations, blood samples were collected at the start of the feeding trials and once a week after that. Fecal matter was also collected from the shark tanks to determine if the seagrass was digestible. After the completion of the feeding trial, the intestinal tract for each shark was tested in a digestive enzyme assay to determine where seagrass digestion was taking place. Food is broken down through a combination of acidity and enzyme activity and different enzymes specialize in breaking down proteins, fats, and carbohydrates. Seagrass is carbohydrate rich, so researchers were searching for those carbohydrate enzymes in the intestines.

To eat or not to eat?

At the end of the experiment, all sharks had gained weight on their seagrass diet. Digestibility analyses based on the volume of food fed to the sharks and their collected fecal matter showed that bonnetheads digested 50% of the total organic matter fed to them and 52% of the fiber in the seagrass. For a “carnivore” this is a remarkably efficient digestion rate for organic plant matter. To put this into perspective, Leigh and collaborators note that juvenile green sea turtles, which are omnivorous, have a mean seagrass digestibility of 44.7% while mature green sea turtles, which are herbivorous, have a digestibility of 64.6%. Based on their results, Leigh and collaborators have definitively documented omnivory in bonnethead sharks. This is the first time omnivory has ever been demonstrated for any shark species!

After establishing that the sharks could digest seagrass, researchers wanted to establish where this digestion happened. They did this by conducting an assay to determine where specific digestive enzymes were produced along the intestinal tract. They found that protein and fat digestive enzymes were more prevalent in the proximal and spiral intestines (the front half of the intestinal tract), while enzymes that would digest carbohydrates, particularly amylase, were high throughout the intestinal tract. They also found elevated levels of enzymes specialized for breaking down cellulose in the shark’s hindgut, or distal intestine, indicating that much of the seagrass digestion may occur here with assistance from some helpful intestinal bacteria.

So what about that heavy 13C I mentioned earlier? Bonnetheads can break down seagrass, but can they incorporate those nutrients into their bodies to fuel growth? The answer is yes! Stable isotope analysis on blood and muscle samples showed significant increases in 13C throughout the feeding trials. These values were also significantly higher than a control set of wild caught bonnetheads.

Researchers measure a bonnethead shark before releasing it back into the Gulf of Mexico (Wikimedia Commons).

The bonnethead sharks in the experiment were definitely breaking down seagrass and using its energy to generate new blood cells and muscle tissue! Because of their abundance, this could have huge implications ecologically. Bonnethead sharks may serve as important nutrient transporters as they move from one seagrass bed to another. As omnivores, they may also play an important role in stabilizing marine food webs. The question of whether bonnetheads intentionally consume seagrass or if it is accidentally swallowed while chasing other prey still remains. Whether they’re after a full plate or just a seagrass side salad, these omnivorous little sharks are clearly getting the most out of their greens!

Further reading

Bethea, DM, L Hale, JK Carlson, E Cortés, CA Manire, and J Gelsleichter. 2007. Geographic and ontogenetic variation in the diet and daily ration of the bonnethead shark, Sphyrna tiburo, from the eastern Gulf of Mexico. Marine Biology 152:1009-1020 https://doi.org/10.1007/s00227-007-0728-7

Bethea, DM, JK Carlson, LD Hollensead, YP Papastamatiou, and BS Graham. 2011. A comparison of the foraging ecology and bioenergetics of the early life-stages of two sympatric hammerhead sharks. Bulletin of Marine Science 87(4):873-889 https://doi.org/10.5343/bms.2010.1047




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