Digestive enzyme activities in the guts of bonnethead sharks ( Sphyrna tiburo ) provide insight into their digestive strategy and evidence for microbial digestion in their hindguts

Abstract

Few investigations have studied digestive enzyme activities in the alimentary tracts of sharks to gain insight into how these organisms digest their meals. In this study, we examined the activity levels of proteases, carbohydrases, and lipase in the pancreas, and along the anterior intestine, spiral intestine, and colon of the bonnethead shark, Sphyrna tiburo. We then interpreted our data in the context of a rate-yield continuum to discern this shark's digestive strategy. Our data show anticipated decreasing patterns in the activities of pancreatic enzymes moving posteriorly along the gut, but also show mid spiral intestine peaks in aminopeptidase and lipase activities, which support the spiral intestine as the main site of absorption in bonnetheads. Interestingly, we observed spikes in the activity levels of N-acetyl-β-D-glucosaminidase and β-glucosidase in the bonnethead colon, and these chitin- and cellulose-degrading enzymes, respectively, are likely of microbial origin in this distal gut region. Taken in the context of intake and relatively long transit times of food through the gut, the colonic spikes in N-acetyl-β-D-glucosaminidase and β-glucosidase activities suggest that bonnetheads take a yield-maximizing strategy to the digestive process, with some reliance on microbial digestion in their hindguts. This is one of the first studies to examine digestive enzyme activities along the gut of any shark, and importantly, the data match with previous observations that sharks take an extended time to digest their meals (consistent with a yield-maximizing digestive strategy) and that the spiral intestine is the primary site of absorption in sharks.

Seagrass digestion by a notorious ‘carnivore’

“…As green sea turtles mature, they become almost entirely herbivorous, and their digestibility of seagrass increases (mean seagrass organic matter digestibility of 64.6%) [18] in parallel with a longer digestive tract and a more diverse microbiome [40]. Therefore, bonnetheads are capable of digesting components of seagrass, with similar effectiveness to omnivores, making them the only shark species known to have the ability to digest plant material [2,10]. For comparison, the carnivorous lizard Crotaphytus collaris digested flowers with only 32% efficiency, whereas the herbivorous Sauromalus obesus digested these same flowers with 67% efficiency [41], showing that not all carnivores can digest plant material efficiently.…”

Molecular identification and functional characteristics of peptide transporters in the bonnethead shark (Sphyrna tiburo)

“…Within the stomach, prey is processed into chyme, an acidic fluid consisting of gastric juices and partly digested food, and then passed into the intestine (Camilleri et al 1986). Once chyme enters the shark spiral/scroll valve intestine, it has been determined that pancreatic enzyme activities largely decrease moving down the gut while BBM enzyme activities peak, suggesting that the spiral/scroll valve intestine is the primary site of absorption (Jhaveri et al 2015). Therefore, the strong immunoreactivity of PepT1 within the stomach and scroll valve intestine epithelial lining is likely correlated with important roles in dietary peptide absorption within these organs.…”

“…With this in mind, unlike the teleost and mammalian intestine, the presence of both pept1 and pept2 mRNA within the bonnethead scroll valve intestine may indicate that both proteins are critical for absorbing the necessary amount of peptides needed for survival. The scroll valve intestine has been described as the most active and absorptive section of the shark intestinal system (Jhaveri et al 2015) due to its unique structure, which conserves space within the body cavity by the infolding of the mucosa and submucosa in a spiral or scroll-like fashion. It may be necessary for elasmobranchs, which are known to consume large meals, to hold those meals for an extended period of time in the stomach (Wetherbee et al 1987;Holmgren and Nilsson 1999;Papastamatiou 2007) and to have multiple active peptide transporters within the intestine to maximize nutrient absorbtion.…”

“…In fact, detailed studies on some of these topics have only recently been conducted. For example, Jhaveri et al (2015) recently examined digestive enzyme activity throughout the gastrointestinal tract of the bonnethead Abstract Elasmobranchs are considered to be top marine predators, and in general play important roles in the transfer of energy within marine ecosystems. Despite this, little is known regarding the physiological processes of digestion and nutrient absorption in these fishes.…”

Amino acid isotope discrimination factors for a carnivore: physiological insights from leopard sharks and their diet

“…). For instance, gut microbes have been shown to play an important role in digestion for bonnethead sharks (Sphyrna tiburo;Jhaveri et al 2015). Although it is counterintuitive that an animal consuming a high-protein diet would rely on microbes for essential amino acids that are incorporated into tissue, this could be related to a role for such microbes in the recycling of urea, as discussed below.…”