The Delicate Balance of Shark Nutrition
Sharks, being apex predators in various marine ecosystems, hold a significant ecological importance. However, they are also among the most endangered vertebrates on the planet. Zoos and public aquaria house a variety of elasmobranch species, yet there is a notable dearth of knowledge to effectively manage these captive populations and enhance their long-term viability (Janse et al., 2004a, 2004b).
The establishment of a well-adapted and accurate feeding regimen is a fundamental determining factor in the maintenance of shark species in captivity. Replicating the natural diet in captivity is commonly accepted and recommended. Given the diverse nutritional composition of prey, supplementation may become necessary. The captive environment poses unique challenges, making sharks susceptible to an array of health issues, including numerous diseases.
Mitigating these risks demands detailed husbandry practices, an appropriate physical environment and a balanced diet. Supplementation, encompassing vitamins and minerals, becomes imperative for the provision of essential nutrients. This complexity has rendered the formulation of an adapted feeding plan for aquarists exceptionally challenging. The scarcity of information in these species adds to the issue, mandating extrapolation from various shark groups and to species with analogous characteristics.
This literature review concentrates predominantly on benthic and pelagic shark species prevalent in contemporary aquariums. The central argument posits that dietary choices in captivity rely on factors such as availability, quality and consistency of supply. The advocated approach highlights the importance of a balanced, diverse feeding that closely mirrors natural diets. It is then crucial to emphasize that these are general guidelines, and the specific dietary requisites may diverge between shark species. Collaborating with experts in marine biology, shark husbandry and veterinary care is imperative for the formulation and perpetuation of an adapted diet for captive sharks.
Understanding Shark Nutritional Needs
To better understand the feeding requirements of the elasmobranch species kept in an aquarium, it is necessary to know the nutritional values of the main components. Examples include the protein to energy ratio, the proportion of carbohydrates, lipids, vitamins and minerals in their food. The optimal diet for a captive shark is a copy of its diet in the wild, both in quantity and quality (Janse et al., 2004a, 2004b).
Proteins
Proteins play an essential role in fish nutrition as well, promoting growth and constituting a significant portion of body tissue. Fish efficiently utilize proteins, as they are ammoniotelic and excrete ammonia through gills, requiring less energy than ureotelic mammals (Paul, 2017). Bowen (1987) provides insights into the dietary protein requirements of fish, highlighting the importance of essential amino acids. A study by Jhaveri et al. (2015a, 2015b) on bonnethead sharks (Sphyrna tiburo, Linnaeus, 1758) indicates notably high aminopeptidase activity, a protein digestive enzyme, suggesting the significance of proteins in shark nutrition.
The high-level activity of protein digestive enzymes across species implies their critical role in the nutrition of these animals, despite variations in metabolic rates (Jhaveri et al., 2015a, 2015b; Newton et al., 2015; Leigh et al., 2018). Investigations by Bernal et al. on blue sharks (Prionace glauca, Linnaeus, 1758), a pelagic species, demonstrated that diets containing 65% protein led to improved swimming performance and higher metabolic rates (Bernal et al., 2012a, 2012b). Another study on great white sharks (Carcharodon carcharias, Linnaeus, 1758) revealed that a protein-rich diet (around 68%) was essential for their rapid growth rates and reproductive success, especially considering the long gestation periods and infrequent breeding cycles (Domeier and Nasby-Lucas, 2008).
Lipids
Lipids serve a dual role, as high-energy storage molecules and as an integral component of cellular membranes. Fish exhibit high digestibility of lipids, with a preference over carbohydrates as an energy source (Newton et al., 2015). Fatty acids are essential components of the cellular membrane and are vital, as fish lack the capacity to synthesize them. Arachidonic acid, metabolized into prostaglandins, plays a role in follicle maturation and steroid production in female elasmobranchs during reproduction (Izquierdo et al., 2001). Omega-3 polyunsaturated fatty acids (PUFA) play a crucial role in vertebrate reproduction, influencing immune responses, inflammatory processes and the development of the brain and the eyes (Tocher, 2010).
Epipelagic sharks exhibit high metabolic rates due to their active and migratory lifestyles. They rely heavily on lipids (e.g. triacylglycerols and squalene) stored in their livers. These lipids provide a dense energy source necessary for long-distance swimming and capturing fast-moving prey (Pethybridge et al., 2014; Davidson et al., 2014). In contrast, benthic sharks, like the nurse shark, have lower metabolic rates and a more sedentary lifestyle. They store lipids not only in the liver but also in muscle tissues. These sharks consume slower-moving or sessile prey influencing their lipid composition.
Studies reveal that placental sharks are born with low concentrations of arachidonic acid (AA) and docosahexaenoic acid (DHA). This may be attributed to either low PUFA-provision during pregnancy or increased PUFA-utilization by pups during intrauterine development, highlighting the significance of lipid metabolism during this period (Lund et al., 2008).
Carbohydrates
Carbohydrates constitute a fundamental component of plants, encompassing sugars, starches, gums, and cellulose. In animals, notably sharks, carbohydrates manifest as glycogen, sugars and their derivatives (Janse et al., 2004a, 2004b). Despite the identification of a relatively low level of maltase, an enzyme responsible for carbohydrate degradation, in the intestines of certain sharks, such as the bonnethead shark, these marine creatures often include crustaceans in their diet. Notably, crustaceans feature a substantial amount of chitin in their shells.
The distinct dietary preferences of sharks, as exemplified by the bonnethead, are evident in their enzyme profiles. For instance, a twofold increase in the activity of B-glucosidase, observed in herbivorous teleost fish, suggests the capacity to digest cellulose and laminarin. Moreover, elasmobranchs exhibit elevated concentrations of N-acetyl-B-d-glucosidase (NAG), surpassing levels found in carnivorous teleost fishes by up to five times, particularly in the distal portion of their intestines. NAG primarily functions in the digestive system, specifically within the intestinal tract, aiding in the breakdown of chitin, a major component of the exoskeletons of crustaceans and other marine organisms that constitute a substantial part of the diet of benthic sharks.
Minerals
It is widely presumed that the dietary requirements for minerals in elasmobranchs are very similar to the needs of teleost species. Nevertheless, they are very difficult to establish because those minerals are required only in trace amounts and that some are absorbed via the environment (aqua) through the gills. It is also important to note that significant interactions between mineral-mineral and mineral-vitamin also exist (Janse et al., 2004a, 2004b) and complexes can be formed, interfering with the actual diet of the animal.
Sharks, both benthic and pelagic, require a range of minerals for critical physiological functions such as growth, reproduction and maintaining homeostasis. Essential minerals include calcium and phosphorus, which are crucial for the formation and maintenance of their cartilaginous skeletons. Magnesium is another essential mineral, playing a vital role in enzymatic reactions, muscle function, and the synthesis of proteins and nucleic acids. Sodium and potassium are critical electrolytes for maintaining osmotic balance and proper nerve function.
The predominant mineral deficiency observed in elasmobranchs, particularly in sharks, is iodine deficiency, a condition that, under specific conditions and levels, can result in goitre (Janse et al., 2004a, 2004b). Meeting this mineral requirement is pivotal for ensuring normal growth and survival and is also essential to physiological cellular metabolism (Paul, 2017).
Vitamins
Approximately 15 vitamins are identified in fish, with symptoms of deficiency in elasmobranchs often inconsistently manifested, complicating identification until necropsy or histopathology (NRC, 2011). Determining precise vitamin requirements for captive sharks is challenging, given the diverse parameters (sex, age, species, environment) which influence their needs (Leigh et al., 2017).
Vitamin A is crucial for vision, growth and immune function. Vitamin D plays a pivotal role in calcium absorption and bone health. Vitamin E acts as an antioxidant, protecting cellular membranes from oxidative damage. Vitamin C is essential for collagen synthesis, wound healing and immune function.
Aquarium shark diets primarily consist of frozen food for transport, parasitological concerns, and quality maintenance, and nutrient loss. Supplementation becomes necessary, typically preceding feeding or incorporation into pre-frozen feed. The most common and successful way is still the usage of tablets via the oral or abdominal cavity, or under the skin of the feed item.
Nutritional Diseases in Captive Sharks
Nutritional disorders can arise for diverse reasons: nutritional imbalance (including vitamin and mineral deficiencies), incorrectly stored food, vitamin deficiency, infected live food and feed toxicity (for example mycotoxins). However, biological stress is another parameter that seems to be essential in the emergence of this unfavourable imbalance, especially during a change of environment from wild to captive.
Vitamin A Imbalance
As a fat-soluble vitamin, vitamin A can accumulate in the body. Vitamin A hypo/hypervitaminosis is well described in the literature in fish but not clearly documented in elasmobranchs. Vitamin A plays a crucial role in shark vision by facilitating the production of 11-cis-retinal, a photosensitive chromophore essential for the visual pigments in their retinal rods and cones. Vitamin A deficiency in sharks can result in conditions such as night blindness and reduced visual acuity. Conversely, excessive vitamin A can lead to structural damage to the retina and optic nerves, causing symptoms like blurred vision, photophobia, exophthalmia and depigmentation.
Imbalances in vitamin A levels in sharks can lead to systemic issues such as ascites, anorexia, decreased growth and lethargy. Both hypo- and hypervitaminosis A can impair reproductive performance and increase the embryonic death rate in sharks. Excess vitamin A disrupts normal embryonic development, leading to teratogenic effects such as deformities, spinal anomalies, craniofacial malformations in shark larvae.
Iodine Deficiency and Goitre
The predominant mineral deficiency observed in elasmobranchs, particularly in sharks, is iodine deficiency, a condition that, under specific conditions and levels, can result in goitre. Iodine appears as an essential component of the elasmobranchs’ metabolism, particularly of their thyroid glands, since the thyroid gland will assimilate and concentrate the iodide ion originating from the feed and from the environment. The thyroid gland produces hormones that regulate metabolism, growth and development.
If the ingested food has an insufficient level of iodine, the thyroid gland will have reduced T3 and T4 production resulting in a lack of tyrosine binding to those hormones. Consequently, a negative feedback in the up-regulation of the TSH by the pituitary gland as well as of the TRH on the hypothalamus will arise. The result will be an elevation of TSH in the bloodstream and the development of goitre.
Goitrous tissue histology can reveal 3 types of goitres in sharks: diffuse colloid goitre, multinodular colloid goitre, and diffuse hyperplastic goitre. In advanced cases of goitre, individuals can show swelling under the midline of the jaw, which can reach up to 10 times the size of a healthy thyroid gland. Clinical signs will result in general symptoms like inappetence due to an improper capability to eat which can eventually result in death.
Fatty Liver Disease
Fatty liver disease is a common health issue in captive sharks. This condition is characterized by the excessive accumulation of fat in the liver, which can lead to impaired liver function and overall health deterioration. Sharks, lacking adipose tissues, accumulate high levels of polyunsaturated fatty acids (PUFA) in their liver, derived from the omega-3 and omega-6-rich diet of various fishes. The liver serves as a storage site for ketone bodies, contributing to energy metabolism in different tissues.
In captivity, a rare energy imbalance due to aquarium feeding and husbandry conditions may lead to ultra-vacuolization of hepatocytes, indicating pathological hepatic steatosis. One of the primary causes of fatty liver in captive sharks is an imbalanced diet, particularly one that is too high in fat. Overfeeding is another significant factor contributing to fatty liver in captive sharks. Deficiencies in certain nutrients, such as vitamins and essential fatty acids, can also predispose sharks to fatty liver.
Preventing and Treating Nutritional Diseases
Preventive measures against nutritional diseases in captive sharks include oral supplementation for vitamin A and the addition of iodine solution to tank water or the use of a vitamin mix formula. Antiparasitic injections may be used as a treatment for infections, but stress should be minimized to prevent the development of foodborne diseases.
The field of shark nutrition and physiology relies heavily on extrapolated knowledge from teleost fish, with limited research specifically focusing on elasmobranchs. Captive care involves replicating a shark’s natural diet through collaboration between caretakers, marine biologists and nutritionists. Tailoring care and feeding protocols to the unique requirements of each shark species in captivity is essential.
Rigorous record-keeping of shark diets and feeding patterns by institutions is crucial for knowledge transfer and long-term insights. Necropsies and histopathological studies on captive deceased elasmobranchs are essential to identify causes of death and gather information on potential pathogens or physiological factors. These investigations into shark nutritional physiology, metabolism and requirements represent practical research pathways that can benefit from the resources and management programs within public aquaria.
The formulation of an optimal feeding regimen for captive sharks is crucial for their health and well-being, particularly in zoo environments where maintaining a balanced diet can be challenging. Despite extensive studies on teleosts, there is a notable lack of specific data on the nutritional needs of elasmobranchs, complicating the establishment of a definitive diet for these species in captivity. Prevention plays a crucial role in elasmobranch health in public aquaria, and a proper dietary regime can help avoid foodborne diseases.
The prevailing recommendation is to replicate the natural diet of sharks as closely as possible, yet the diversity in the nutritional composition of their natural prey necessitates careful supplementation of essential vitamins and minerals. Collaborative efforts and ongoing research are essential to optimize the dietary management of captive sharks, ensuring their health and longevity.
Conclusion
Sharks possess a remarkable capacity for extensive lipid and glycogen storage in their liver and differentiating normal from pathological conditions proves challenging due to the inherent variability in hepatocyte vacuolization. Physiological hepatocyte hypertrophy, characterized by enlarged cells resulting from increased tissue cell size, is evident in pregnant specimens undergoing vitellogenesis.
Understanding the intricate interactions between parasites and their hosts, as well as their relationship with the environment and life cycle, is necessary for the inspection, manipulation and husbandry practices related to feed management. This understanding aids in mitigating potential adverse effects on captive sharks.
The field of shark nutrition and physiology requires continued research and collaboration between caretakers, marine biologists, and veterinary experts. Tailoring feeding protocols to the unique needs of each shark species, while replicating their natural diets as closely as possible, is crucial for maintaining the health and longevity of these remarkable apex predators in captivity.
