M. F. L. SMITH

1 Dynasty Marine Associates Inc., 10602 7th Avenue, Gulf, Marathon, FL 33050, USA

2 University of Hawaii at Manoa, Hawaii Institute of Marine Biology, PO Box 1346, Kaneohe, HI 96744, USA

3 Rotterdam Zoological & Botanical gardens, PO Box 532, 3000 AM Rotterdam, The Netherlands

4 Oceanário de Lisboa, Doca dos Olivais, 1990-096, Lisboa, Portugal

5 Oceanário de Lisboa / IDEA Inc., Doca dos Olivais, 1990-096, Lisboa, Portugal

ABSTRACT

The capture and transportation of scalloped hammerhead sharks, Sphyrna lewini (Griffith and Smith, 1834), has historically represented a difficult, expensive and uncertain undertaking for the public aquarium community. In this study, techniques were developed to improve the successful long-term transport of S. lewini by mitigating some of the deleterious effects associated with hyperactivity and impaired swimming patterns. The relationship between transport vessel size, shark size, shark number and shark swimming behaviour was considered when formulating the transportation regime. By balancing these factors and adopting a comprehensive water treatment method, it was possible to extend the duration of a successful transportation by up to 60 hours. Implications for the future transportation of S. lewini and other free-swimming sharks are discussed.

RESUME

INTRODUCTION

Larger obligate ram-ventilating demersal and pelagic shark species are often difficult to transport for extended periods of time with any degree of success. Some of the challenges associated with transporting these animals have been outlined in previous studies (Cliff & Thurman, 1984; Andrews & Jones, 1990; Smith, 1992; Arai, 1997). Fortunately, developments in transportation techniques have enabled workers to successfully transport large shark species like the bull shark (Carcharhinus leucas Müller and Henle, 1839) and sandbar shark (Carcharhinus plumbeus Nardo, 1827) for longer periods of time (Andrews and Jones, 1990; Smith, 1992). The authors have also successfully transported the blacktip shark (Carcharhinus limbatus Müller and Henle, 1839), the bonnethead shark (Sphyrna tiburo Linnaeus, 1758) and the blacknose shark (Carcharhinus acronotus Poey, 1860) for periods exceeding 24 hours.

The scalloped hammerhead shark (Sphyrna lewini Griffith & Smith, 1834) has been historically regarded as a difficult prospect to successfully transport for any extended period of time, and hence, for any appreciable distance (Arai, 1997). This paper reports on techniques that attempt to address the challenges presented by this unique species and facilitate their successful transportation for periods exceeding 36 hours.

Hammerhead sharks, in the family Sphyrnidae (Gill, 1872), represent a small group of eight distinct species. They are a wide-ranging, coastal marine shark, with family representatives occurring in warm-temperate and tropical oceans throughout the world. They typically feed on teleost fishes, cephalopods and crustaceans (Compagno, 1984). Hammerheads are distinguished by a distinctive 'hammer' or mallet-shaped lateral expansion of the head known as a 'cephalofoil'. The function of this lateral expansion is not clear, however it has been interpreted as a morphological development to facilitate one or more of the following: (1) improved hydro-dynamic manoeuvrability; (2) enhanced anterior binocular vision; (3) enhanced acuity and directionality of olfaction; and (4) enhanced pressure and electro-reception, through an augmentation of the lateral line canals and the ampullae of Lorenzini (Compagno, 1984).

The uniqueness, notoriety, and sheer visual presence of S. lewini make them a very interesting candidate for public display. Unfortunately, the very morphological feature that make S. lewini so popular, also presents a challenge to workers in relation to the successful capture, transportation and maintenance of this shark. During these processes, specimens are often observed damaging their head and eyes by impacting the physical boundaries of the transportation vessel or the holding facility (Arai, 1997; Howe, 1998). In addition, experience has demonstrated that S. lewini appear to be highly susceptible to the same physiological changes observed in other Carcharhiniformes during capture and transportation, confounding an already difficult recovery (Cliff and Thurman, 1984; Smith, 1992; Howe, 1998). Based on a number of previous studies, it was hypothesised that these changes could be linked to a number of mechanisms. They include: (1) impaired obligate ram-ventilation, whereby the shark cannot pass sufficient water over its gills and effective ventilation and respiration is compromised (Gruber and Keyes, 1981; Hewitt, 1984); (2) an interrupted swimming pattern and associated decreased muscular 'pumping' activity, resulting in a reduced circulation of vascular and lymphatic fluids (Gruber and Keyes, 1981 Lowe, 1996); (3) an elevated energy expenditure through increased turning frequency to avoid tight corners and interactions with conspecifics (Weihs, 1973; Klay, 1977); and (4) anaerobic metabolism and blood acidosis induced by periods of extended hyperactivity (Murdaugh and Robin, 1967; Albers, 1970; Bennett, 1978).

The capture, transport and display of S. lewini has been attempted by a number of public aquaria with varying degrees of success. An historical overview of these attempts has been summarised in Table 1a. Any attempt to transport S. lewini for periods approaching 36 hours has resulted in increased levels of mortality (Table 1a).

It is possible that previous attempts to transport S. lewini may not have entirely addressed the important spatio-dynamic requirements of the species, and therefore, the induced physiological changes. It was hypothesised that any future attempt at a long-term transport of this species must consider the following important challenges: (1) physical injury to the head and eyes; (2) compromised ram-ventilation; (3) compromised systemic circulation through impaired muscular 'pumping'; (4) elevated energy expenditure; (5) anaerobic respiration and blood acidosis; (6) declining water quality, resulting from the excretion of ammonia; and (7) decreasing pH resulting from the excretion of CO2 and H+ ions (Cliff and Thurman, 1984; Smith, 1992).

In light of these concerns, several parameters were considered during the formulation of the transportation regime for this study. Specifically: (1) transport vessel size; (2) transport vessel shape; (3) number of obstructions within the transport vessel; (4) size of the specimens transported; (5) number of specimens transported; and (6) the water treatment regime.

METHODS

All S. lewini specimens were caught in Kaneohe Bay, Oahu, Hawaii, USA using hook and line. Sharks were subjected to 'tonic immobility' during manual handling as per Watsky and Gruber (1990). Once caught, the animals were transferred by boat to a 20.0 m long x 10.0 m wide x 1.3 m deep holding pen within 15 min of capture. They were carried in a 1.3 m diameter hemispherical fibreglass, water-filled tank, similar to the vessel adopted by Keyes (20001) to avoid damage to the eyes and 'cephalofoil'. The animals recuperated in the holding pen for two to three weeks before long-term transportation commenced.

The transport regime was based on a feasibility study undertaken by Kajiura (1999). 18 juvenile S. lewini (45.0 - 68.0 cm TL) were transported in six containers (3 sharks per container). Each container was a white, smooth-walled cylindrical fibreglass tank, 250.0 cm in diameter x 65.0 cm high. In addition, a 112.0 cm long x 112.0 cm wide x 46.0 cm high 'live'-well was mounted on the top of each tank. A perforated Plexiglas plate was fitted into the base of the 'live'-well and acted as a lid (Figure 1). A pump (Model 27D, Rule ITT Industries, USA) of 4.16 m3.h-1 capacity was mounted on the underside of the lid, keeping it off the floor where it could potentially interrupt the swimming pattern of the sharks. This pump was responsible for driving a filtration system consisting of a canister filter filled with activated carbon, that was mounted on the top of the lid. Once the water was filtered, it was sprayed onto the perforated plate and allowed to trickle back into the transportation container. This was done to enhanced gas exchange and CO2 liberation. A second small pump (Model 24, Rule ITT Industries, USA) of 1.36 m3.h-1 capacity was used to provide a very gentle circulation within the body of the transport vessel. Each transport container was filled with seawater, to just below the base of the 'live'-well, in order to prevent 'sloshing'. Hence, each vessel contained approximately 3.20 m3 of seawater. Each container was packed onto a single aircraft pallet and accompanied by two 12V sealed batteries (Model 800 S, Optima, USA) and two pressurised oxygen cylinders, each of 7.98 m3 capacity. Two days before each transportation, fasting began and lasted throughout the entire operation. No anaesthesia or other chemico-therapeutics were administered during the transport.

Water quality was monitored throughout the transportation. Every hour, dissolved oxygen concentrations, ammonia concentrations and pH were measured for each container. Oxygen saturation within the vessels was maintained between 80 - 120% by adjusting the flow of oxygen from the accompanying cylinders. If the concentration of ammonia was found to be higher than 0.5 mg.l-1 then a 420.0 ml dose of an ammonia detoxifier (AmQuel, Kordon-Novalek Inc., USA) was added to the water. This amount of AmQuel had been pre-calculated to neutralise 1.0 mg.l-1 of ammonia in 3.20 m3 of water (i.e. the volume of the transport containers). If pH was found to be lower than 8.0 then a 50.0 g dose of sodium bicarbonate was also added to the water. Approximately half-way through the transportation a 60% water exchange was performed using fresh seawater taken from the point of origin.

Upon arrival, the sharks were acclimated to the water parameters of their new holding facility by slowly replacing 50% of the water in the transport vessel with water from their destination tank. The sharks were then transferred from the transport container to the holding tank by hand, while subjecting the animals to 'tonic immobility'.

No prophylaxsis of any kind was administered to the sharks during the week following the completion of the shipments.

RESULTS

Two intercontinental shipments of S. lewini were undertaken. The first on 28 April 1999 and the second on 17 August 1999. Both transports used Honolulu as the point of departure and Los Angeles as the first stop. Thereafter, the first shipment continued on to its final destination of Beijing. The second shipment continued to Lisbon via Fort Worth and Miami. Half of the shipment remained in Lisbon, while the other half continued on to Rotterdam. The details of each shipment are summarised in Table 1b.

The shortest duration transport of 42 h yielded an 83% survival rate two weeks after their arrival in Beijing (Table 1b). The longest duration transport of 70 h yielded a 33% survival rate two weeks after their arrival in Rotterdam (Table 1b).

Throughout the shipments, the sharks seemed able to avoid both the walls of the containers and conspecifics with ease; sustaining no external physical injuries through obtundation (i.e. colliding with the walls).

In general, water quality was regulated and remained high throughout the early stages of the shipments. However, during the latter stages, water quality control measures appeared to become less effective. This was evidenced by one or more of the animals exhibiting signs of distress (i.e. lying on the bottom of the vessel, increased disorientation, decreased ability to avoid the walls or conspecifics, etc.). Rectification of the water parameters, specifically ammonia and pH, regularly arrested these symptoms. During the Lisbon to Rotterdam 'leg' of the second transportation, pH reached a low of 7.6 despite attempts to reverse the decline. It is conceivable that other water parameters had correspondingly deteriorated and may have contributed to the single mortality observed during that shipment.

Upon introduction to their respective holding tanks, all surviving animals (i.e. 17 of 18) appeared in good health and commenced feeding within two to three days. Nevertheless, two of the six sharks in Lisbon exhibited a slight disorientation and discoloration in the hours immediately following the transportation.

Manual handling of the sharks appeared to leave slightly discoloured 'bruises' on the skin of the animals that persisted during ensuing months. In some cases, these 'bruises' acted as the foci for bacterial infection and required treatment with anti-biotics.

Two weeks after the respective shipments, two of the six sharks were alive in Rotterdam and five of the six sharks were alive in each of Beijing and Lisbon (Table 1b).

DISCUSSION

The results of this study are very empirical and by necessity exceptionally small sample sizes were used. These limitations should be borne in mind and caution exercised when interpreting the results.

The techniques used to capture, handle and transfer the sharks to the holding facility in Hawaii, provided very suitable and healthy specimens for transportation. It should be noted that in every previously recorded instance, hook and line was the technique of preference for capturing S. lewini (Table 1a). This may have been through necessity in many cases. However, in some instances, it also reflects a general understanding of the delicate integument of this species and the profound physiological changes that may take place during a long struggle (Wisner, 19992; Violetta, 20003). Hooking and quickly landing these sharks, without the use of nets, helps to avoid these problems.

The hemispherical fibreglass transfer vessel seemed to provide a good means to move the sharks during the critical minutes following their initial capture. The tapering edge of the vessel appeared to reduce the possibility of obtundation and reduced the risks of physical damage to the eyes and 'cephalofoil' (as per Keyes, 20001).

The two to three week staging period within the holding facility at Kaneohe Bay was considered to be a critical factor in ensuring that the animals were optimally prepared for transportation. Staging for at least 24 h following capture is considered essential for the successful long-term transportation of the species (Wisner, 19993).

Manual handling, in conjunction with tonic immobility, provided a convenient method for manipulating the sharks. However, 'bruising' that resulted from the manual handling, and possible bacterial infection, indicated that physically touching the sharks should be avoided if at all possible (as per Kaiser, 20004 and Rupp, 20005).

The dimensions of the transport container seemed appropriate for the size of the specimens shipped. The animals swam in a continuous manner and exhibited no signs of difficulty avoiding the walls of the vessel. This was enhanced by the fact that the level of the water relative to the 'live'-well helped reduce water movement within the vessel during transport (as per Arai, 1997). In addition, as the circulation pump was mounted on the bottom of the baffle plate it did not obstruct the normal swimming pattern of the sharks, that remained close to the bottom of the tank. The decision to transport no more than three animals per container also seemed vindicated, as the sharks rarely appeared to 'stall' or turn abruptly to avoid conspecifics. It could be suggested that the relatively unencumbered environment within the vessel decreased the consumption of vital energy reserves, reduced the production of toxic metabolites and reduced the risks of metabolic shock. This finding is consistent with observations by previous workers that obligate ram-ventilating sharks need to continuously swim to facilitate systemic circulation and will consume excess energy reserves by frequently turning to avoid conspecifics (Powell, 20006).

It was difficult to conclude anything regarding the appropriateness of the shape of the transport container. It seems likely that the large dimensions of the vessel relative to the size of the sharks, coupled with the lack of directed current, meant that shape did not play a major role. Some workers have found that circular tanks work well with S. lewini for relatively short shipments, where obtundation is an important issue (Wisner, 19993). However, for longer transportations, where physiological changes become increasingly important, there is some thought that short quick turns may be less energetically challenging than continuous turning. In these cases, small circular vessels may not be so advantageous (Powell, 20006).

Activated carbon appeared to maintain a high water quality within the vessels throughout the early stages of the transportation. The spray bar positioned above the baffle plate provided a good means of gas exchange and minimised pH decline through CO2 accumulation. Similarly, the accumulation of H+ ions and the subsequent pH decline appeared to be alleviated to some degree by water exchanges and the periodic addition of sodium bicarbonate. Water exchanges also helped reduce the concentration of the constantly accumulating toxic ammonia. The deleterious effects of ammonia were further mitigated by the periodic additions of the detoxifier AmQuel.

Despite every effort, water quality control measures started to become less effective during the latter stages of the shipments. Probably weakened by the physiological changes induced by hyperactivity and exposure to poorer water quality, some of the sharks suffered irreversible damage and succumbed during the latter stages of the longer transportations, or during the days thereafter. Clearly water quality is paramount during any shark transportation and water treatment mechanisms must be able to provide optimal conditions throughout the entire process. The water treatment regime adopted for this study appeared to be effective until approx. 60 hours. For longer transportations, further water treatment mechanisms should be considered (e.g. additional water exchanges, replacement of activated carbon, 'staging' at an intermediate facility, etc.).

In conclusion, it could be suggested that the interaction of several parameters should be taken into consideration when formulating a transportation regime for this species. They include: (1) the nominal swimming behaviour of the species; (2) size of the transport container; (3) number of obstructions within the container; (4) size of the shark; and (5) the number of sharks. These factors will determine turning frequency, the consumption of important energy reserves and the risks of physical injury. In addition, transportation duration appeared to influence shark survival rates. This may have been the result of decreasing water quality and / or the physiological changes induced by hyperactivity and depleted energy reserves, for although turning frequency was reduced, it was not eliminated altogether. The techniques adopted in this study appear to have extended the possible duration for the transportation of S. lewini by up to 60 hours. It could be cautiously suggested that similar techniques may be adopted for species of an analogous ecology. Further refinements, especially to the management of water quality, may extend transportation times even further. However, 60 hours should be sufficient to transport these animals to almost any destination throughout the world.

ACKNOWLEDGEMENTS

We gratefully acknowledge the assistance and advice of Hiroshi Arai, Angus Barnhart, Jerry Crow, Christopher Daughtry, Steve Kaiser, Ray Keyes, Allan Marshall, Frank McHugh, Miguel Oliveira, John O'Sullivan, Dave Powell, Peter van Putten, John Rupp, Gary Violetta and Marty Wisner.

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