The physiological ecology of the bull shark Carcharhinus leucas in the Brisbane River

Pillans, Richard David (2006). The physiological ecology of the bull shark Carcharhinus leucas in the Brisbane River PhD Thesis, School of Integrative Biology , University of Queensland.

       
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Author Pillans, Richard David
Thesis Title The physiological ecology of the bull shark Carcharhinus leucas in the Brisbane River
School, Centre or Institute School of Integrative Biology
Institution University of Queensland
Publication date 2006
Thesis type PhD Thesis
Supervisor Assoc Pr Craig Franklin
Abstract/Summary The bull shark, Carcharhinus leucas is one of few elasmobranchs capable of living in, and moving freely between, freshwater (FW) and seawater (SW). Despite this remarkable ability, very little is known about the osmoregulatory physiology and ecology of this species. Bull sharks are common in the Brisbane River, a tidal river in subtropical Australia that has about 90 km of habitable water and salinity gradient from 33‰ (seawater) at the mouth to 0 ‰ (freshwater) in the upper reaches. The presence of bull sharks in the Brisbane River, and the accessibility of this system, provides a unique opportunity to investigate how this species osmoregulatory ability allows it to utilise freshwater, estuarine and marine environments. The distribution, size structure and movement patterns of bull sharks in the river and surrounding marine environment were investigated by capture, tagging and acoustic tracking. A total of 712 bull sharks were captured in Brisbane River and Moreton Bay. Juvenile bull sharks showed a strong preference for the upper FW reaches with the catch per unit effort (CPUE) in upper FW reaches (1.18 sharks per hr) significantly higher than Moreton Bay and the river mouth (0.08 and 0.09 sharks per hour) Presence of open umbilical scars indicate that bull sharks are born at 65 – 83 cm Total length (TL). Size composition in the river was strongly skewed towards juveniles, with neonates contributing 68% to the riverine population. Although neonates dominated the catches, animals between 85 – 130 cm were not uncommon and this together with tag recapture data indicates that bull sharks remain in the Brisbane River from birth until approximately 140 cm when they move to a marine environment. Six animals were tracked using acoustic tags. Three juvenile animals tagged in freshwater reaches showed very similar movement patterns remaining in the upper reaches and did not encounter any changes in environmental salinity. Two out of three animals tagged in the estuarine reaches moved upstream and downstream and were exposed to large and rapid fluctuations in environmental salinity resulting in a need to osmoregulate in hyper and hypo-ionic environments. Plasma osmolality of bull sharks captured along a salinity gradient from FW to SW was always hyperosmotic to the environment, ranging from 642 ± 7 mOsm.kg¯¹ (FW animals) to 1067 ± 21 mOsm.kg¯¹(SW animals). In FW animals, sodium, chloride and urea were 208 ± 3, 203 ± 3 and 192 ± 2 mmol.l¯¹ , respectively. Plasma sodium, chloride and urea in SW-captured C. leucas were 289 ± 3, 296 ± 6 and 370 ± 10 mmol.l¯¹, respectively. This osmoregulatory strategy necessitates active Na+ and Cl- secretion by the rectal gland in SW and active conservation of these ions in FW. Despite the increased importance of the rectal gland in hyper-ionic environments, there was no difference in the rectal gland mass of C. leucas captured in FW and estuarine environments (20–28‰) of the Brisbane River. Juvenile C. leucas captured in freshwater (FW) (3 mOsm) were acclimated to seawater (SW) (980 – 1000 mOsm) over sixteen days. A freshwater group was maintained in captivity over a similar time period. In SW, juvenile sharks regulated all plasma osmolytes to the same degree as adults captured in SW showing that juveniles are capable of osmoregulation in SW and that preference for FW is due to behaviour rather than a physiological constraint. Gill, rectal gland, kidney and intestinal tissue were analysed for maximal Na+/K+- ATPase activity. Na+/K+-ATPase activity in the gills and intestine was less than 1 mmol Pi.mg¯¹ protein.h¯¹ and there was no difference in activity between FW and SW acclimated animals. In SW, rectal gland Na+/K+-ATPase activity (9.2 ± 0.6 mmol Pi.mg¯¹ protein.h¯¹) was significantly higher than FW animals (5.6 ± 0.8 and 9.2 ± 0.6 mmol Pi.mg¯¹protein. h¯¹). Na+/K+-ATPase activity in the kidney of FW acclimated animals (8.4 ± 1.1 Pi.mg¯¹ protein.h¯¹) was significantly higher than SW animals (3.3 ± 1.1 Pi.mg¯¹ protein.h¯¹). These differences were attributed to the increased importance of the rectal gland to secretion of Na+ and Cl- in SW and the need for the kidney to actively reabsorb Na+ and Cl- in freshwater. Despite large biochemical changes in the rectal gland, structural changes were less obvious. There was no difference in rectal gland cross sectional area, lumen area, rectal gland vein area, number of secretory tubules or secretory cells per secretory tubule in FW and SW acclimated animals. At a cellular level, there was no difference between the degree of basolateral and lateral folding, number of mitochondria or number of desmosomes per tight junction. Tight junction width was significantly greater in SW acclimated animals. The number of red blood cells in the interstitial tissue was also significantly higher in SW acclimated animals reflecting an increased perfusion of the capillaries of the rectal gland. The lack of large morphological changes reflects the small amount of FW habitat in the Brisbane River and the fact that animals are exposed to increasing salinity when they move downstream. Results of acoustic tracking showed that animals were capable of moving rapidly between salinity gradients. Do determine the extend and timing of plasma and erythrocyte solute properties, animals captured in freshwater (FW) were acutely acclimated to 75% seawater (SW), and 100% SW. Blood samples were taken at 0, 12 and 96 h following transfer to 75% SW and 24 h and 72 h after transfer to 100% SW. A control group in FW was subjected to the same sampling regime. Upon transfer of C. leucas to 75% and 100% SW, plasma Na+, Cl-, K+, Mg²+, Ca²+, urea and TMAO concentrations all increased significantly but disproportionately. Plasma Na+ and Cl- increased immediately, followed by an increase in plasma urea. Erythrocyte urea and TMAO concentrations increased significantly following transfer to 75% and 100% SW, however changes in erythrocyte inorganic ion concentrations were insignificant. Haematocrit, haemoglobin and mean cell haematocrit did not differ significantly after transfer to seawater, however, plasma water was slightly reduced after 24 h and 72 h in 100% SW. Red blood cell (RBC) water content was elevated 24 h after transfer to 100% SW but returned to FW levels after 72 h. Juvenile bull sharks tolerated rapid and significant increases in salinity by rapidly increasing plasma osmolality to be hyperosmotic to the environment whilst maintaining a tight regulation of their intracellular fluid environment. Results from this research indicate the juvenile bull sharks spend several years in the Brisbane River before moving to a marine environment. Despite a preference for the FW reaches, juveniles are capable of living in both FW and SW and osmoregulate equally well in both environments. The bull sharks ability to live and move between FW and SW is due to their rapid control of plasma and erythrocyte ion and water content via the action of the rectal gland, gills and kidney.

 
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