CORRELATIONS OF CAPTURE, TRANSPORT, AND NUTRITION WITH SPINAL DEFORMITIES IN SANDTIGER SHARKS,CARCHARIAS TAURUS, IN PUBLIC AQUARIA

Abstract

A number of captive sandtiger sharks (Carcharias taurus) in public aquaria have developed spinal deformities over the past decade, ranging in severity from mild curvature to spinal fracture and severe subluxation. To determine the frequency and etiologic basis of this disease, U.S. public aquaria participated in a two-stage epidemiologic study of resident sharks: 1) a history and husbandry survey and 2) hematology, clinical chemistry, and radiography conducted during health exams. Eighteen aquaria submitted data, samples, or both from 73 specimens, including 19 affected sharks (26%). Sharks caught off the Rhode Island coast or by pound net were smaller at capture and demonstrated a higher prevalence of deformity than did larger sharks caught from other areas via hook and line. Relative to healthy sharks, affected sharks were deficient in zinc, potassium, and vitamins C and E. Capture and transport results lead to two likely etiologic hypotheses: 1) that the pound-net capture process induces spinal trauma that becomes exacerbated over time in aquarium environments or 2) that small (and presumably young) sharks caught by pound net are exposed to disease-promoting conditions (including diet or habitat deficiencies) in aquaria during the critical growth phase of their life history. The last hypothesis is further supported by nutrient deficiencies among affected sharks documented in this study; potassium, zinc, and vitamin C play critical roles in proper cartilage-collagen development and maintenance. These correlative findings indicate that public aquaria give careful consideration to choice of collection methods and size at capture and supplement diets to provide nutrients required for proper development and maintenance of cartilaginous tissue.

Mechanical properties of sand tiger sharkCarcharias taurusvertebrae in relation to spinal deformity

“…Significant, though sometimes weak, relationships have been identified between mineral content and stiffness in shark vertebrae and numerous other vertebrate endoskeletal materials (Currey, 2002;Currey, 2008;Porter et al, 2006;Porter et al, 2007). The lack of predictability between mineral content and material properties in this study may be associated with vitamin C and zinc deficiencies observed in C. taurus from public aquaria, as these metabolites affect both the quantity and quality of collagen and mineralization in skeletal elements (Anderson et al, 2012). Vitamin C is an enzymatic cofactor involved in the crosslinking of polypeptide subunits into tropocollagen triple helices, which are subsequently bundled into collagen fibrils and fibers that serve as the scaffold for deposition and orientation of mineral in connective tissues (Hulmes, 2002;Holmes and Kadler, 2006;Lall and Lewis-McCrea, 2007); the orientation of mineral can affect stiffness, as seen in the anisotropic behavior of bone (Currey, 2002;Currey, 2008).…”

“…Stage I of the survey collected historical, clinical and husbandry data, while Stage II of the survey collected spinal radiographs, blood samples for immunological and clinical chemistry analyses, and videography of swimming for behavioral analysis; these results are reported elsewhere (Anderson et al, 2012;Tate et al, 2013). Stage III of the survey entailed a necropsy of sharks that had been euthanized because of severity of spinal deformity or those that expired from other causes (senescence, post-capture mortality).…”

“…The average size at capture of affected C. taurus is 122 cm TL, which corresponds to approximately 1 year of age (Goldman et al, 2006), and those sharks captured via net instead of hook-and-line are five times more likely to develop spinal deformity in aquaria. Fortunately, only 8% of C. taurus caught via hook-and-line develop these deformities (Anderson et al, 2012). It is likely that the spines of young sharks are less able to withstand the mechanical stress of capture, perhaps indicating ontogenetic variation in the mineralization of vertebrae, and that this fragility is exacerbated by the stress of being hauled out of the water by net.…”

“…Many of these animals are eventually euthanized because of the gradual deterioration of their condition, thereby increasing pressure on wild stocks for exhibit specimens despite dwindling wild populations (Anderson et al, 2012). Hoenig and Walsh (Hoenig and Walsh, 1983), Berzins et al (Berzins et al, 1998;Berzins et al, 2002) and Preziosi et al (Preziosi et al, 2006) were the first to describe these spinal deformities, along with a variety of other skeletal tissue abnormalities including curled pectoral fins, gingival hyperplasia and permanently protruded upper jaws.…”

“…Anderson et al found that animals caught via net were more likely to develop spinal deformities than those caught by hook and line (Anderson et al, 2012). Affected sharks were caught at a smaller size than nonaffected sharks (122 and 186 cm, respectively), had higher Fulton condition factors (body mass/length 3 ), and had lower serum concentrations of vitamins C and E, potassium, and zinc as well (Anderson et al, 2012); deficiencies in vitamin C and zinc are known to affect collagen synthesis and crosslinking, as well as the skeletal mineralization process in other vertebrates (Starcher et al, 1980;Lall and Lewis-McCrea, 2007). Another study (Tate et al, 2013) found that affected sharks spend more time using powered swimming (greater swim-to-glide ratio) and have longer tail-beat durations than non-affected sharks, and that all C. taurus in public aquaria spend nearly 100% of their time swimming asymmetrically (turning as opposed to linear locomotion) regardless of spinal deformity.…”