Freshwater to seawater acclimation of juvenile bull sharks ( Carcharhinus leucas): plasma osmolytes and Na +/K +-ATPase activity in gill, rectal gland, kidney and intestine

This study examined the osmoregulatory status of the euryhaline elasmobranch Carcharhinus leucas acclimated to freshwater (FW) and seawater ( SW). Juvenile C. leucas captured in FW ( 3 mOsm l(-1) kg(-1)) were acclimated to SW ( 980 - 1,000 mOsm l(-1) kg(-1)) over 16 days. A FW group was maintained in captivity over a similar time period. In FW, bull sharks were hyper-osmotic regulators, having a plasma osmolarity of 595 mOsm l(-1) kg(-1). In SW, bull sharks had significantly higher plasma osmolarities ( 940 mOsm l(-1) kg(-1)) than FW-acclimated animals and were slightly hypoosmotic to the environment. Plasma Na+, Cl-, K+, Mg2+, Ca2+, urea and trimethylamine oxide (TMAO) concentrations were all significantly higher in bull sharks acclimated to SW, with urea and TMAO showing the greatest increase. Gill, rectal gland, kidney and intestinal tissue were taken from animals acclimated to FW and SW and 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 contrast Na+/ K+-ATPase activity in the rectal gland and kidney were significantly higher than gill and intestine and showed significant differences between the FW- and SW-acclimated groups. In FW and SW, rectal gland Na+/ K+-ATPase activity was 5.6 +/- 0.8 and 9.2 +/- 0.6 mmol Pi mg(-1) protein h(-1), respectively. Na+/ K+-ATPase activity in the kidney of FW and SW acclimated animals was 8.4 +/- 1.1 and 3.3 +/- 1.1 Pi mg(-1) protein h(-1), respectively. Thus juvenile bull sharks have the osmoregulatory plasticity to acclimate to SW; their preference for the upper reaches of rivers where salinity is low is therefore likely to be for predator avoidance and/or increased food abundance rather than because of a physiological constraint.

Hepatic urea biosynthesis in the euryhaline elasmobranch Carcharhinus leucas

Plasma urea levels and hepatic urea production in the euryhaline bull shark, Carcharhinus leucas, acclimated to freshwater and seawater environments were measured. It was found that plasma urea concentration increased with salinity and that this increase was, in part, the result of a significant increase in hepatic production of urea. This study provides direct evidence that hepatic production of urea plays an important role in the osmoregulatory strategy of C. leucas.

Sequence, circulating levels, and expression of C-type natriuretic peptide in a euryhaline elasmobranch, Carcharhinus leucas

The present study has examined expression and circulating levels of C-type natriuretic peptide (CNP) in the euryhaline bull shark, Carcharhinus leucas. Complementary DNA and deduced amino acid sequence for CNP in C leucas were determined by RACE methods. Homology of CNP amino acid sequence in C. leucas was high both for proCNP and for mature CNP when compared with previously identified elasmobranch CNPs. Mature CNP sequence in C. leucas was identical to that in Triakis seyllia and Seyliorhinus canicula. Levels of expression of CNP mRNA were significantly decreased in the atrium but did not change in either the brain or ventricle following acclimation to a SW environment. However, circulating levels of CNP significantly increased from 86.0 +/- 7.9 fmol ml(-1) in FW to 144.9 +/- 19.5 fmol ml(-1) in SW. The results presented demonstrate that changes in environmental salinity influences both synthesis of CNP from the heart and also circulating levels in C. leucas. Potential stimulus for release and modes of action are discussed. (c) 2005 Elsevier Inc. All rights reserved.

The effects of freshwater to seawater transfer on circulating levels of angiotensin II, C-type natriuretic peptide and arginine vasotocin in the euryhaline elasmobranch, Carcharhinus leucas

This study examined the effect of transfer to increased environmental salinity on the circulating levels of angiotensin II (ANG II), C-type natriuretic peptide (CNP), and arginine vasotocin (AVT) in the euryhaline elasmobranch, Carcharhinus letteas. Plasma levels of ANG 11 and CNP were significantly increased in C. leucas chronically acclimated to seawater (SW) in comparison to freshwater (FW) acclimated fish. There was no difference in plasma AVT levels. Acute transfer of FW fish to 75% SW induced an increase in plasma ANG II levels within 12 h, and subsequent transfer from 75 to 100% SW further increased plasma ANG 11 levels at both 24 and 72 h. No change in plasma CNP was observed during acute transfer to increased salinity. However, a significant increase in plasma AVT levels was observed following 96 h in 75% SW and 24 h in 100% SW. In chronically SW acclimated C leucas plasma osmolality, sodium, chloride, and Urea were all significantly higher than FW acclimated fish but there was no difference in haematocrit. Acute transfer of C letteas to 75% SW induced a significant increase in plasma osmolality, sodium and urea concentrations within 96 h of transfer. Subsequent transfer from 75 to 100% SW induced a further increase in these variables within 24 h in addition to a significant increase in plasma chloride above control levels. Haematocrit did not differ between the experimental and control groups throughout the acute study. Circulating levels of ANG 11 were significantly correlated to plasma, sodium, chloride, and urea concentrations during acclimation to SW. Conversely, circulating levels of CNP and AVT did not correlate to plasma osmolytes, however, CNP was significantly correlated to haematocrit during acclimation to seawater. (c) 2005 Elsevier Inc. All rights reserved.

Fatty acids and stable isotopes as indicators of early-life feeding and potential maternal resource dependency in the bull shark Carcharhinus leucas

The degree of reliance of newborn sharks on energy reserves from maternal resource allocation and the timescales over which these animals develop foraging skills are critical factors towards understanding the ecological role of top predators in marine ecosystems. We used muscle tissue stable carbon isotopic composition and fatty acid analysis of bull sharks Carcharhinus leucas to investigate early-life feeding ecology in conjunction with maternal resource dependency. Values of δ13C of some young-of-the-year sharks were highly enriched, reflecting inputs from the marine-based diet and foraging locations of their mothers. This group of sharks also contained high levels of the 20:3ω9 fatty acid, which accumulates during periods of essential fatty acid deficiency, suggesting inadequate or undeveloped foraging skills and possible reliance on maternal provisioning. A loss of maternal signal in δ13C values occurred at a length of approximately 100 cm, with muscle tissue δ13C values reflecting a transition from more freshwater/estuarine-based diets to marine-based diets with increasing length. Similarly, fatty acids from sharks >100 cm indicated no signs of essential fatty acid deficiency, implying adequate foraging. By combining stable carbon isotopes and fatty acids, our results provided important constraints on the timing of the loss of maternal isotopic signal and the development of foraging skills in relation to shark size and imply that molecular markers such as fatty acids are useful for the determination of maternal resource dependency.

Size-based variation in intertissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier)

Stable isotopes are important tools for understanding the trophic roles of elasmobranchs. However, whether different tissues provide consistent stable isotope values within an individual are largely unknown. To address this, the relationships among carbon and nitrogen isotope values were quantified for blood, muscle, and fin from juvenile bull sharks (Carcharhinus leucas) and blood and fin from large tiger sharks (Galeocerdo cuvier) collected in two different ecosystems. We also investigated the relationship between shark size and the magnitude of differences in isotopic values between tissues. Isotope values were significantly positively correlated for all paired tissue comparisons, but R2 values were much higher for δ13C than for δ15N. Paired differences between isotopic values of tissues were relatively small but varied significantly with shark total length, suggesting that shark size can be an important factor influencing the magnitude of differences in isotope values of different tissues. For studies of juvenile sharks, care should be taken in using slow turnover tissues like muscle and fin, because they may retain a maternal signature for an extended time. Although correlations were relatively strong, results suggest that correction factors should be generated for the desired study species and may only allow coarse-scale comparisons between studies using different tissue types.

Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator, Carcharhinus leucas

The frequency of extreme environmental events is predicted to increase in the future. Understanding the short- and long-term impacts of these extreme events on large-bodied predators will provide insight into the spatial and temporal scales at which acute environmental disturbances in top-down processes may persist within and across ecosystems. Here, we use long-term studies of movements and age structure of an estuarine top predator—juvenile bull sharks Carcharhinus leucas—to identify the effects of an extreme ‘cold snap’ from 2 to 13 January 2010 over short (weeks) to intermediate (months) time scales. Juvenile bull sharks are typically year-round residents of the Shark River Estuary until they reach 3 to 5 yr of age. However, acoustic telemetry revealed that almost all sharks either permanently left the system or died during the cold snap. For 116 d after the cold snap, no sharks were detected in the system with telemetry or captured during longline sampling. Once sharks returned, both the size structure and abundance of the individuals present in the nursery had changed considerably. During 2010, individual longlines were 70% less likely to capture any sharks, and catch rates on successful longlines were 40% lower than during 2006−2009. Also, all sharks caught after the cold snap were young-of-the-year or neonates, suggesting that the majority of sharks in the estuary were new recruits and several cohorts had been largely lost from the nursery. The longer-term impacts of this change in bull shark abundance to the trophic dynamics of the estuary and the importance of episodic disturbances to bull shark population dynamics will require continued monitoring, but are of considerable interest because of the ecological roles of bull sharks within coastal estuaries and oceans.

To Madagascar and back: long-distance, return migration across open ocean by a pregnant female bull shark Carcharhinus leucas

A large, pregnant, female bull shark Carcharhinus leucas was tracked migrating from Seychelles across open ocean to south-east Madagascar, c. 2000 km away, and back again. In Madagascar, the shark spent a prolonged period shallower than 5 m, consistent with entering estuarine habitat to pup, and upon return to Seychelles the shark was slender and no longer gravid. This represents an unprecedented return migration across the open ocean for a C. leucas and highlights the need for international collaboration to manage the regional C. leucas population sustainably.

To Madagascar and back: long-distance, return migration across open ocean by a pregnant female bull shark Carcharhinus leucas

A large, pregnant, female bull shark Carcharhinus leucas was tracked migrating from Seychelles across open ocean to south-east Madagascar, c. 2000 km away, and back again. In Madagascar, the shark spent a prolonged period shallower than 5 m, consistent with entering estuarine habitat to pup, and upon return to Seychelles the shark was slender and no longer gravid. This represents an unprecedented return migration across the open ocean for a C. leucas and highlights the need for international collaboration to manage the regional C. leucas population sustainably.

Mitochondrial DNA supports the identification of two endangered river sharks (Glyphis glyphis and Glyphis garricki) across northern Australia

The river sharks (genus Glyphis) are a small group of poorly known sharks occurring in tropical rivers and estuarine waters across northern Australia, south-east Asia and the subcontinent. The taxonomy of the genus has long been unclear due to very few individuals having been caught and examined, resulting in a paucity of data regarding their distribution, biology and ecology. Only recently has attention focussed on the two Australian species, G. glyphis and G. garricki. This study is a result of a rare opportunity to collate the few samples that have been collected from these species and the bull shark Carcharhinus leucas, which shares an overlapping range. These samples were analysed using the DNA barcoding approach (cox1 mitochondrial gene), compared with six other species of carcharhinids and evaluated in light of the current taxonomic classification. Nine species-specific nucleotide differences were found between G. glyphis and G. garricki and no intra-specific variation provides strong support for the separation into distinct species. Significant differences were also observed at the inter-generic level, with Glyphis forming a distinct clade from Carcharhinus. This study provides the basis for future molecular studies required to better address conservation issues confronting G. glyphis and G. garricki in Australia.

The status of shark and ray fishery resources in the Gulf of California: applied research to improve management and conservation

Seasonal surveys were conducted during 1998–1999 in Baja California, Baja California Sur, Sonora, and Sinaloa to determine the extent and activities of artisanal elasmobranch fisheries in the Gulf of California. One hundred and forty–seven fishing sites, or camps, were documented, the majority of which (n = 83) were located in Baja California Sur. Among camps with adequate fisheries information, the great majority (85.7%) targeted elasmobranchs during some part of the year. Most small, demersal sharks and rays were landed in mixed species fisheries that also targeted demersal teleosts, but large sharks were usually targeted in directed drift gillnet or, to a lesser extent, surface longline fisheries. Artisanal fishermen were highly opportunistic, and temporally switched targets depending on the local productivity of teleost, invertebrate, and elasmobranch fishery resources. Major fisheries for small sharks (< 1.5 m, “cazón”) were documented in Baja California during spring, in Sonora during autumn–spring, and in Sinaloa during winter and spring. Triakid sharks (Mustelus spp.) dominated cazón landings in the northern states, whereas juvenile scalloped hammerheads (Sphyrna lewini) primarily supported the fishery in Sinaloa. Large sharks (> 1.5 m, “tiburón”) were minor components of artisanal elasmobranch fisheries in Sonora and Sinaloa, but were commonly targeted during summer and early autumn in Baja California and Baja California Sur. The pelagic thresher shark (Alopias pelagicus) and silky shark (Carcharhinus falciformis) were most commonly landed in Baja California, whereas a diverse assemblage of pelagic and large coastal sharks was noted among Baja California Sur landings. Rays dominated summer landings in Baja California and Sinaloa, when elevated catch rates of the shovelnose guitarfish (Rhinobatos productus, 13.2 individuals/vessel/trip) and golden cownose ray (Rhinoptera steindachneri, 11.1 individuals/vesse/trip) primarily supported the respective fisheries. The Sonoran artisanal elasmobranch fishery was the most expansive recorded during this study, and rays (especially R. productus) dominated spring and summer landings in this state. Seasonal catch rates of small demersal sharks and rays were considerably greater in Sonora than in other surveyed states. Many tiburón populations (e.g., C. leucas, C. limbatus, C. obscurus, Galeocerdo cuvier) have likely been overfished, possibly shifting effort towards coastal populations of cazón and rays. Management recommendations, including conducting demographic analyses using available life history data, determining and protecting nursery areas, and enacting seasonal closures in areas of elasmobranch aggregation (e.g., reproduction, feeding), are proposed. Without effective, enforceable management to sustain or rebuild targeted elasmobranch populations in the Gulf of California, collapse of many fisheries is a likely outcome. (PDF contains 243 pages)

El estado actual de los tiburones y rayas sujectos a explotación comercial en el Golfo de California: una investigación aplicada al mejoramiento de su manejo pesquero y conservación

Se realizaron prospecciones estacionales durante 1998–1999 en Baja California, Baja California Sur, Sonora y Sinaloa para determinar la dimensión y las actividades de las pesquerías artesanales de elasmobranquios dentro del Golfo de California. Ciento cuarenta y siete campamentos o sitios pesqueros fueron documentados, la mayoría de los cuales (n= 83) fueron localizados en Baja California Sur. Entre los campamentos con información pesquera adecuada, la gran mayoría (85.7%) pescaron elasmobranquios en algún momento del año. La mayoría de los pequeños tiburones y rayas demersales fueron capturados en pesquerías multiespecíficas, las cuales también tienen como objetivo teleósteos, pero los grandes tiburones fueron capturados generalmente por pesquerías de redes agalleras a la deriva dirigidas a ellos, o en menor grado, por pesquerías de palangre de superficie. Los pescadores artesanales presentaron un comportamiento altamente oportunístico y temporalmente cambiaban de especie objetivo dependiendo de la productividad de los recursos pesqueros locales de especies de escama, invertebrados y elasmobranquios. Las mayores pesquerías de pequeños tiburones (≤1.5 m, “cazón”) se documentaron en Baja California, Sonora, y Sinaloa durante la primavera y adicionalmente durante otoño e invierno en Sonora. Los tiburones del genero Mustelus (Mustelus spp) dominaron los desembarques de cazón en los estados norteños, mientras que los tiburones martillo juveniles (Sphyrna lewini) sostuvieron la pesquería en Sinaloa. Los grandes tiburones (> 1.5 m, “tiburón”) fueron componente menor de las pesquerías artesanales de elasmobranquios en Sonora y Sinaloa, pero comúnmente fueron capturados en verano y principios de otoño en Baja California y Baja California Sur. El tiburón zorro pelágico (Alopias pelagicus) y el tiburón piloto (Carcharhinus falciformis) fueron comúnmente desembarcados en Baja California, mientras que un diverso ensamble de tiburones pelágicos y grandes costeros fueron observados en los desembarques de Baja California Sur. Las rayas dominaron los desembarques en verano en Baja California y Sinaloa, sostenidas principalmente por elevadas tasas de captura de la guitarra común (Rhinobatos productus, 13.2 individuos/embarcación/viaje) y del tecolote (Rhinoptera steindachneri, 11.1 individuos/embarcación/viaje). La pesquería de rayas de Sonora fue la más extensamente documentada durante este estudio y las rayas (especialmente R. productus) dominaron los desembarques en primavera y verano en este estado. Las tasas de captura estacionales de pequeños tiburones demersales y rayas fueron considerablemente mayores en Sonora que en los otros estados prospectados. Numerosas poblaciones de tiburón (p. ej. C. leucas, C. limbatus, C. obscurus, Galeocerdo cuvier) han sido probablemente sobreexplotados, lo que posiblemente este causando un cambio en el esfuerzo hacia las poblaciones de cazón y rayas costeros. Se proponen recomendaciones de manejo, incluyendo conducir análisis demográficos empleando la información de historias de vida disponible, localizando y protegiendo áreas de crianza e implementando temporadas de veda estacional en las áreas de mayor concentración de elasmobranquios (p. ej. alimentación, reproducción). Sin un manejo pesquero efectivo, vigilado, para sostener o reconstruir las poblaciones de elasmobranquios sujetas a explotación comercial dentro del Golfo de California, el colapso de las pesquerías es un evento probable. (PDF contains 261 pages)

Multidirectional movements of sportfish species between an estuarine no-take zone and surrounding waters of the Indian River Lagoon, Florida

We examined movement patterns of sportfish that were tagged in the northern Indian River Lagoon, Florida, between 1990 and 1999 to assess the degree of fish exchange between an estuarine no-take zone (NTZ) and surrounding waters. The tagged f ish were from seven species: red drum (Sciaenops ocellatus); black drum (Pogonias cromis); sheepshead (Archosargus probatocephalus); common snook (Centropomus undecimalis); spotted seatrout (Cynoscion nebulosus); bull shark (Carcharhinus leucas); and crevalle jack (Caranx hippos). A total of 403 tagged fish were recaptured during the study period, including 65 individuals that emigrated from the NTZ and 16 individuals that immigrated into the NTZ from surrounding waters of the lagoon. Migration distances between the original tagging location and the sites where emigrating fish were recaptured were from 0 to 150 km, and these migration distances appeared to be influenced by the proximity of the NTZ to spawning areas or other habitats that are important to specific life-history stages of individual species. Fish that immigrated into the NTZ moved distances ranging from approximately 10 to 75 km. Recapture rates for sportfish species that migrated across the NTZ boundary suggested that more individuals may move into the protected habitats than move out. These data demonstrated that although this estuarine no-take reserve can protect species from fishing, it may also serve to extract exploitable individuals from surrounding fisheries; therefore, if the no-take reserve does function to replenish surrounding fisheries, then increased egg production and larval export may be more important mechanisms of replenishment than the spillover of excess adults from the reserve into fishable areas.

Opportunistic visitors : long-term behavioural response of bull sharks to food provisioning in Fiji

Shark-based tourism that uses bait to reliably attract certain species to specific sites so that divers can view them is a growing industry globally, but remains a controversial issue. We evaluate multi-year (2004–2011) underwater visual (n = 48 individuals) and acoustic tracking data (n = 82 transmitters; array of up to 16 receivers) of bull sharks Carcharhinus leucas from a long-term shark feeding site at the Shark Reef Marine Reserve and reefs along the Beqa Channel on the southern coast of Viti Levu, Fiji. Individual C. leucas showed varying degrees of site fidelity. Determined from acoustic tagging, the majority of C. leucas had site fidelity indexes >0.5 for the marine reserve (including the feeding site) and neighbouring reefs. However, during the time of the day (09:00–12:00) when feeding takes place, sharks mainly had site fidelity indexes <0.5 for the feeding site, regardless of feeding or non-feeding days. Site fidelity indexes determined by direct diver observation of sharks at the feeding site were lower compared to such values determined by acoustic tagging. The overall pattern for C. leucas is that, if present in the area, they are attracted to the feeding site regardless of whether feeding or non-feeding days, but they remain for longer periods of time (consecutive hours) on feeding days. The overall diel patterns in movement are for C. leucas to use the area around the feeding site in the morning before spreading out over Shark Reef throughout the day and dispersing over the entire array at night. Both focal observation and acoustic monitoring show that C. leucas intermittently leave the area for a few consecutive days throughout the year, and for longer time periods (weeks to months) at the end of the calendar year before returning to the feeding site.

Urea-based osmoregulation in the developing embryo of oviparous cartilaginous fish (Callorhinchus milii) : contribution of the extraembryonic yolk sac during the early developmental period

Marine cartilaginous fish retain a high concentration of urea to maintain the plasma slightly hyperosmotic to the surrounding seawater. In adult fish, urea is produced by hepatic and extrahepatic ornithine urea cycles (OUCs). However, little is known about the urea retention mechanism in developing cartilaginous fish embryos. In order to address the question as to the mechanism of urea-based osmoregulation in developing embryos, the present study examined the gene expression profiles of OUC enzymes in oviparous holocephalan elephant fish (Callorhinchus milii) embryos. We found that the yolk sac membrane (YSM) makes an important contribution to the ureosmotic strategy of the early embryonic period. The expression of OUC enzyme genes was detectable in the embryonic body from at least stage 28, and increased markedly during development to hatching, which is most probably due to growth of the liver. During the early developmental period, however, the expression of OUC enzyme genes was not prominent in the embryonic body. Meanwhile, we found that the mRNA expression of OUC enzymes was detected in the extra-embryonic YSM; the mRNA expression of cmcpsIII in the YSM was much higher than that in the embryonic body during stages 28-31. Significant levels of enzyme activity and the existence of mitochondrial-type cmgs1 transcripts in the YSM supported the mRNA findings. We also found that the cmcpsIII transcript is localized in the vascularized inner layer of the YSM. Taken together, our findings demonstrate for the first time that the YSM is involved in urea-based osmoregulation during the early to mid phase of development in oviparous cartilaginous fish.