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Leigh SC, Papastamatiou Y, and DP German. 2017. the Nutritional

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Leigh SC, Papastamatiou Y, and DP German. 2017. the Nutritional Rev Fish Biol Fisheries (2017) 27:561–585 DOI 10.1007/s11160-017-9481-2 REVIEWS The nutritional physiology of sharks Samantha C. Leigh . Yannis Papastamatiou . Donovan P. German Received: 28 December 2016 / Accepted: 9 May 2017 / Published online: 25 May 2017 Ó Springer International Publishing Switzerland 2017 Abstract Sharks compose one of the most diverse Keywords Digestive efficiency Á Digestive and abundant groups of consumers in the ocean. biochemistry Á Gastrointestinal tract Á Microbiome Á Consumption and digestion are essential processes for Spiral intestine Á Stable isotopes obtaining nutrients and energy necessary to meet a broad and variable range of metabolic demands. Despite years of studying prey capture behavior and Introduction feeding habits of sharks, there has been little explo- ration into the nutritional physiology of these animals. Sharks make up one of the most abundant and diverse To fully understand the physiology of the digestive groups of consumers in the ocean (Fig. 1, Compagno tract, it is critical to consider multiple facets, including 2008). They may play an important ecological role in the evolution of the system, feeding mechanisms, energy fluxes in marine environments and in impact- digestive morphology, digestive strategies, digestive ing the biodiversity of lower trophic levels that we biochemistry, and gastrointestinal microbiomes. In depend on as a food and economic resource (e.g., each of these categories, we make comparisons to Wetherbee et al. 1990; Corte´s et al. 2008). However, what is currently known about teleost nutritional beyond prey capture methods and dietary analyses, the physiology, as well as what methodology is used, and nutritional physiology of sharks is woefully under- describe how similar techniques can be used in shark studied. They consume a broad range of diet types research. We also identify knowledge gaps and (smaller sharks, marine mammals, teleosts, crus- provide suggestions to continue the progression of taceans, zooplankton, etc.) but are generally known the field, ending with a summary of new directions that to be largely carnivorous, consuming prey items high should be addressed in future studies regarding the in protein and lipids (Wetherbee et al. 1990; Corte´s nutritional physiology of sharks. et al. 2008; Bucking 2016). We will regularly refer to the phylogeny (Fig. 1) in order to show how the diverse families of sharks are related. Indeed, match- & S. C. Leigh ( ) Á D. P. German ing physiological concepts with genetic underpinnings Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA and evolutionary background is crucial to understand- e-mail: [email protected] ing the patterns and processes involved in the evolu- tion of the digestive strategies that sharks possess. Y. Papastamatiou The broader field of nutritional physiology has a Marine Sciences Program, Department of Biological Science, Florida International University, 3000 NE 151st foundation based largely on economic theory: the St, Miami, FL 33181, USA digestive tract is energetically expensive to maintain 123 562 Rev Fish Biol Fisheries (2017) 27:561–585 Callorhinchus callorynchus Chimaera monstrosa Amblyraja radiata Manta birostris Squatina nebulosa Squatiniformes Chlamydoselachidae Hexanchiformes Hexanchidae Echinorhinidae Pristiophoriformes Pristiophoridae Squatinidae Squatiniformes Selachimorpha Etmopteridae Somniosidae Centrophoridae Squaliformes A Somniosidae Dalatiidae B Squalidae (A) Heterodontidae Heterodontiformes Mitsukurinidae C Lamnidae (B) Alopidae Pseudocarchariidae Lamniformes Megachasmidae Cetorhinidae (C) D Odontaspididae Rhincodontidae (D) E Stegostomatidae Orectolobiformes Hemiscyllidae Orectolobidae F Ginglymostomatidae (E) Proscylliidae Scyliorhinidae (F) Pseudotriakidae G Triakidae (G) Scyliorhinidae Hemigaleidae Carcharhiniformes H Leptochariidae Etmopteridae Carcharhinidae (H) Sphyrnidae (I) I Carcharhinidae Fig. 1 Phylogeny of sharks to the family level based on the tree Cetorhinus maximus (basking shark), D) Rhincodon typus from Ve´lez-Zuazo & Agnarsson 2011. Light gray lines show (whale shark), E) Ginglymostoma cirratum (nurse shark), F) which families belong to certain orders. Illustrations of specific Cephaloscyllium ventriosum (swell shark), G) Triakis semifas- shark species discussed in the text are shown (not to scale). The ciata (leopard shark), H) Negaprion brevirostris (lemon shark), letters above each illustration correspond to the family in the I) Sphyrna tiburo (bonnethead shark). Illustrations by R. Aidan phylogeny to which that species belongs. A) Squalus acanthias Martin (2003) (spiny dogfish), B) Carcharodon carcharias (white shark), C) (Cantetal.1996), and thus, from basic economic suggests that gut function should match with what is principles, the Adaptive Modulation Hypothesis (AMH; consumed in terms of quantity and biochemical compo- Karasov 1992; Karasov and Martinez del Rio 2007) sition (Martine and Fuhrman 1995; Karasov and Douglas 123 Rev Fish Biol Fisheries (2017) 27:561–585 563 2013). Shark evolution presumably follows AMH and histology. In recent years, the feeding mechanisms sharks should, therefore, have guts optimized for their of teleost fishes have been studied using modern high-protein, high-lipid diets. Sharks are also generally techniques such as high-speed video kinematics, known for eating large meals on an infrequent basis, Video Reconstruction of Moving Morphology potentially going days, or even weeks, without a meal (VROMM), X-ray Reconstruction of Moving Mor- (Wetherbee et al. 1987;Corte´setal.2008; Armstrong and phology (XROMM), and biorobotic models (Shamur Schindler 2011). Hence, in order to acquire ample et al. 2016; Longo et al. 2016; Laurence-Chasen et al. nutrients from their infrequent meals, sharks must have 2016; Gidmark et al. 2015; Camp et al. 2015; Camp mechanisms of slowing the rate of digesta transit to allow and Brainerd 2014; Kenaley and Lauder 2016; Corn sufficient time for digestion and nutrient absorption, yet et al. 2016; Wilga and Ferry 2016). These types of there has been minimal investigation into shark nutri- methodologies allow researchers to determine the tional physiology. Although the field of comparative exact skeletal elements and muscles involved in the nutritional physiology is relatively young (e.g., Karasov different feeding mechanisms. They also give us the and Diamond 1983; Diamond and Karasov 1987; data necessary to quantify and model exactly how Karasov and Martinez del Rio 2007), much has been these cranio-facial elements move (in terms of volume learned about gut function in ecological and evolutionary of the buccal cavity, angles of skeletal elements, contexts, albeit mostly about terrestrial organisms length of muscle, etc.) before, during, and after a because of research in biomedical and livestock fields feeding event. For example, Camp et al. (2015) used (Choat and Clements 1998; Clements et al. 2009). Within XROMM to show that the power required for buccal marine biology, far more advances have been made cavity expansion during suction feeding in the large concerning the nutritional physiology of teleost fishes mouth bass is generated primarily by axial swimming (e.g., German 2011) than for sharks. New methods of muscles rather than smaller cranial muscles. This investigation have been developed, as well as new research changed the perspective of musculoskeletal theories and models that could be applied to sharks (e.g., function in ray-finned fishes (over 30,000 species) and German et al. 2015; Clements et al. 2017). The most opened doors for further investigation using XROMM. recent reviews of elasmobranch digestive physiology Examples of videos created from XROMM can be (Corte´setal.2008; Bucking 2016; Ballantyne 2016) found at: http://www.xromm.org/movies. Despite the lament the dearth of data available on shark digestion, and success of these methods when studying the feeding thus, make logical connections to the recent advances in mechanics of teleosts, they have yet to become com- the understanding of teleost nutritional physiology, where mon in investigations of shark feeding. Adapting some there have been efforts to integrate diet with digestive of these methods, particularly high-speed video kine- tract function and metabolism. Here, we review what is matics and VROMM, to be used in large tank systems, currently known regarding shark feeding mechanisms, or even in the field, would provide important details on digestive morphology, digestive strategies, digestive shark feeding mechanics that heretofore have gone un- biochemistry, and gastrointestinal microbiomes. In each studied. of these categories, we make comparisons to what is As a result of their broad range of diet types, sharks known about teleost nutritional physiology and describe have highly diverse methods for feeding (Navia et al. how similar techniques can be used in shark research. We 2007). The great diversity of feeding mechanisms that also identify knowledge gaps and provide suggestions to are exhibited by sharks can generally be sorted into continue the progression of the field, ending with a three main categories: bite and retain, suction, and ram summary of new directions that should be addressed in feeding (Motta and Wilga 2001). The biting mecha- future studies regarding the nutritional physiology of nism is likely the most studied. Sharks are historically sharks. known for their sharp teeth and strong jaws that aid in the prey capture process (Corte´s et al. 2008;
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