Natural or Artificial? Habitat-Use by the Bull Shark,Carcharhinus leucas

Background

Despite accelerated global population declines due to targeted and illegal fishing pressure for many top-level shark species, the impacts of coastal habitat modification have been largely overlooked. We present the first direct comparison of the use of natural versus artificial habitats for the bull shark, Carcharhinus leucas, an IUCN ‘Near-threatened’ species - one of the few truly euryhaline sharks that utilises natural rivers and estuaries as nursery grounds before migrating offshore as adults. Understanding the value of alternate artificial coastal habitats to the lifecycle of the bull shark is crucial for determining the impact of coastal development on this threatened but potentially dangerous species.

Methodology/Findings

We used longline surveys and long-term passive acoustic tracking of neonate and juvenile bull sharks to determine the ontogenetic value of natural and artificial habitats to bull sharks associated with the Nerang River and adjoining canals on the Gold Coast, Australia. Long-term movements of tagged sharks suggested a preference for the natural river over artificial habitat (canals). Neonates and juveniles spent the majority of their time in the upper tidal reaches of the Nerang River and undertook excursions into adjoining canals. Larger bull sharks ranged further and frequented the canals closer to the river mouth.

Conclusions/Significance

Our work suggests with increased destruction of natural habitats, artificial coastal habitat may become increasingly important to large juvenile bull sharks with associated risk of attack on humans. In this system, neonate and juvenile bull sharks utilised the natural and artificial habitats, but the latter was not the preferred habitat of neonates. The upper reaches of tidal rivers, often under significant modification pressure, serve as nursery sites for neonates. Analogous studies are needed in similar systems elsewhere to assess the spatial and temporal generality of this research.     

How can the feeding habits of the sand tiger shark influence the success of conservation programs?

The feeding habits of the sand tiger shark Carcharias taurus , one of the most threatened sharks of the world, are poorly known. Sand tiger sharks are critically endangered in the South-west Atlantic. Since 2007, the law requires that all individuals caught in recreational fisheries off Argentina must be released. Using data from a north Patagonian recreational fishery ( n =164 stomachs with contents), we analyzed the diet of sand tiger sharks in relation with size, sex, maturity stage and season; assessed prey consumption patterns and hooking location; and estimated diet overlap with fishery landings. Sand tiger sharks consumed mainly teleosts (55.4% of the total prey number, N ) and elasmobranchs (41.84% N ), and ate more benthic elasmobranchs (batoids and angel sharks) as they become larger. Sharks swallowed prey mostly in one piece (93.7%) and were hooked mainly in internal organs (87.4%, n =175), causing occlusion and perforation of the esophagus and stomach, and lacerations to the pericardium, heart and liver. Sand tiger sharks fed on the most heavily landed species, overlapping almost completely (>90%) with fishery landings. Conservation plans should take into account that releasing hooked sharks could be insufficient to minimize fishing mortality and that competition for food with fisheries is likely to occur.     

A new elusive otodontid shark (Lamniformes: Otodontidae) from the lower Miocene,and comments on the taxonomy of otodontid genera,including the ‘megatoothed’ clade

We describe a new large otodontid lamniform shark, Megalolamna paradoxodon gen. nov. et sp. nov., chronostratigraphically restricted to the early Miocene (Aquitanian–Burdigalian). This new species is based on isolated teeth found from five globally distributed localities: the Jewett Sand in southern California, USA; the Pungo River Formation of North Carolina, USA; the Chilcatay Formation of Peru; the Oi Formation in Mie Prefecture, Japan; and the O’oshimojo Formation in Nagano Prefecture, Japan. Extrapolations based on available published data on modern macrophagous lamniforms suggest that the largest specimen of M. paradoxodon gen. nov. et sp. nov. possibly came from an individual that measured at least 3.7 m in total length. All specimens came from deposits in the mid-latitudinal zones representing shallow-water, shelf-type, coastal environments. Its dentition likely exhibited monognathic heterodonty suited for capturing and cutting relatively large prey (e.g. medium-sized fishes). We recommend the genus Otodus to include sharks of the ‘megatoothed’ (e.g. megalodon) lineage in order to avoid Otodus paraphyly. We also propose the following phylogenetic hypothesis: [Kenolamna?+?[Cretalamna?+?[Megalolamna + Otodus]]].

ZooBank LSID for the genus Megalolamna is: urn: lsid:zoobank.org:act:B4791DEF-4D96-4FEB-9B7B-0EF816B96079

ZooBank LSID for the species Megalolamna paradoxodon is: urn:lsid:zoobank.org:act:7D3D7442-53C6-43A2-9E8D-6339729565B6     

Functional significance of the shark Na,K-ATPase N-terminal domain. Is the structurally variable N-Terminus involved in tissue-specific regulation by FXYD proteins?

The proteolytic profile after mild controlled trypsin cleavage of shark rectal gland Na,K-ATPase was characterized and compared to that of pig kidney Na,K-ATPase, and conditions for achieving N-terminal cleavage of the alpha-subunit at the T(2) trypsin cleavage site were established. Using such conditions, the shark enzyme N-terminus was much more susceptible to proteolysis than the pig enzyme. Nevertheless, the maximum hydrolytic activity was almost unaffected for the shark enzyme, whereas it was significantly decreased for the pig kidney enzyme. The apparent ATP affinity was unchanged for shark but increased for pig enzyme after N-terminal truncation. The main common effect following N-terminal truncation of shark and pig Na,K-ATPase is a shift in the E(1)-E(2) conformational equilibrium toward E(1). The phosphorylation and the main rate-limiting E(2) --> E(1) step are both accelerated after N-terminal truncation of the shark enzyme, but decreased significantly in the pig kidney enzyme. Some of the kinetic differences, like the acceleration of the phosphorylation reaction, following N-terminal truncation of the two preparations may be due to the fact that under the conditions used for N-terminal truncation, the C-terminal domain of the FXYD regulatory protein of the shark enzyme, PLMS or FXYD10, was also cleaved, whereas the gamma or FXYD2 of the pig enzyme was not. In the shark enzyme, N-terminal truncation of the alpha-subunit abolished association of exogenous PLMS with the alpha-subunit and the functional interactions were abrogated. Moreover, PKC phosphorylation of the preparation, which relieves PLMS inhibition of Na,K-ATPase activity, exposed the N-terminal trypsin cleavage site. It is suggested that PLMS interacts functionally with the N-terminus of the shark Na,K-ATPase to control the E(1)-E(2) conformational transition of the enzyme and that such interactions may be controlled by regulatory protein kinase phosphorylation of the N-terminus. Such interactions are likely in shark enzyme where PLMS has been demonstrated by cross-linking to associate with the Na,K-ATPase A-domain.     

A review of shark agonistic displays: comparison of display features and implications for shark–human interactions

Agonistic displays in 23 species of sharks of six families are described and illustrated. These displays are reviewed in terms of ethological concepts and shark hydrodynamic models. Shark agonistic displays feature many common elements rendering them readily distinguishable from normal swimming and pseudodisplays caused by sharksucker irritation. Shark agonistic displays are most readily elicited by rapid, direct diver approach when food is absent and potential escape routes restricted. Such displays appear to be motivated by defence of self or the immediately surrounding space rather than defence of territory or resources. Costs and benefits of display versus attack in shark–shark and shark–diver contests are evaluated using payoff matrices and optimal strategies are identified. Shark–human interactions are modelled in terms of a system of nested critical approach distances. For divers faced with a displaying shark, responses which may decrease the likelihood of defensive attack are suggested. Recommendations for future work on shark agonistic behaviour are offered.     

Is the alkaline tide a signal to activate metabolic or ionoregulatory enzymes in the dogfish shark (Squalus acanthias)?

Experimental metabolic alkalosis is known to stimulate whole-animal urea production and active ion secretion by the rectal gland in the dogfish shark. Furthermore, recent evidence indicates that a marked alkaline tide (systemic metabolic alkalosis) follows feeding in this species and that the activities of the enzymes of the ornithine-urea cycle (OUC) for urea synthesis in skeletal muscle and liver and of energy metabolism and ion transport in the rectal gland are increased at this time. We therefore evaluated whether alkalosis and/or NaCl/volume loading (which also occurs with feeding) could serve as a signal for activation of these enzymes independent of nutrient loading. Fasted dogfish were infused for 20 h with either 500 mmol L(-1) NaHCO3 (alkalosis + volume expansion) or 500 mmol L(-1) NaCl (volume expansion alone), both isosmotic to dogfish plasma, at a rate of 3 mL kg(-1) h(-1). NaHCO3 infusion progressively raised arterial pH to 8.28 (control = 7.85) and plasma [HCO3-] to 20.8 mmol L(-1) (control = 4.5 mmol L(-1)) at 20 h, with unchanged arterial P(CO2), whereas NaCl/volume loading had no effect on blood acid-base status. Rectal gland Na+,K+-ATPase activity was increased 50% by NaCl loading and more than 100% by NaHCO3 loading, indicating stimulatory effects of both volume expansion and alkalosis. Rectal gland lactate dehydrogenase activity was elevated 25% by both treatments, indicating volume expansion effects only, whereas neither treatment increased the activities of the aerobic enzymes citrate synthase, NADP-isocitrate dehydrogenase, or the ketone body-utilizing enzyme beta-hydroxybutyrate dehydrogenase in the rectal gland or liver. The activity of ornithine-citrulline transcarbamoylase in skeletal muscle was doubled by NaHCO3 infusion, but neither treatment altered the activities of other OUC-related enzymes (glutamine synthetase, carbamoylphosphate synthetase III). We conclude that both the alkaline tide and salt loading/volume expansion act as signals to activate some but not all of the elevated metabolic pathways and ionoregulatory mechanisms needed during processing of a meal.     

Follicle cell processes: a shark thing?

Follicle cell processes (FCP) are identified in two species of carcharhinid shark (Selachii) but are absent in the little skate Leucoraja erinacea (Batoidea). This suggests that FCPs are either a unique structure that evolved in selachians or were lost by the batoids after their divergence, some 280 mya . The presence of FCPs in the selachians would be consistent with the evolution of large oocytes in this group of animals.     

Stable and radiogenic isotope analyses on shark teeth from the Early to the Middle Permian (Sakmarian–Roadian) of the southwestern USA

δ¹⁸O_P values and ⁸⁷Sr/⁸⁶Sr ratios were determined on disarticulated xenacanthiform, hybodontid and ctenacanthid shark tooth material from several Early Permian (Sakmarian–Kungurian) continental bone beds of northern Texas and southern Oklahoma as well as from the marine Middle Permian (Roadian) of northern Arizona. The δ¹⁸O_P values derived from the teeth of bone beds are in the range of 17.6–23.5‰ VSMOW, and are mostly depleted in ¹⁸O by 0.5–5‰ relative to proposed coeval marine δ¹⁸O_P values. This indicates an adaptation to freshwater habitats on the Early Permian coastal plain by several sharks. Distinctly higher δ¹⁸O_P values from two bone beds are attributed to significant evaporative enrichment in ¹⁸O in flood plain ponds. ⁸⁷Sr/⁸⁶Sr ratios of around 0.71077 are notably more radiogenic than ⁸⁷Sr/⁸⁶Sr of contemporaneous seawater. In contrast, the isotopic composition of teeth from the marine Kaibab Formation is characterised by low δ¹⁸O_P values in the range of 13.4–15.6‰ VSMOW while ⁸⁷Sr/⁸⁶Sr ratios of around 0.70821 are closer to the Roadian seawater value. The distinctly depleted δ¹⁸O_P values cannot be readily explained by fluvially affected freshening in a nearshore marine environment, so a diagenetic alteration of the Kaibab material seems to be more likely, excluding it from further interpretation.     

Orders out of chaos – molecular phylogenetics reveals the complexity of shark and stingray tapeworm relationships

Novel molecular data are presented to resolve the long-standing issue of the non-monophyly of the elasmobranch-hosted tapeworm order Tetraphyllidea relative to the other acetabulate eucestode orders. Bayesian inference analyses of various combinations of full ssrDNA, and full or partial lsrDNA (D1–D3), sequence data, which included 134 species representing 97 genera across the 15 eucestode orders, were conducted. New ssrDNA data were generated for 82 species, partial lsrDNA data for 53 species, and full lsrDNA data for 29 species. The monophyly of each of the elasmobranch-hosted orders Cathetocephalidea, Litobothriidea, Lecanicephalidea and Rhinebothriidea was confirmed, as was the non-monophyly of the Tetraphyllidea. Two relatively stable groups of tetraphyllidean taxa emerged and are hereby designated as new orders. The Onchoproteocephalidea n. ord. is established to recognise the integrated nature of one undescribed and 10 described genera of hook-bearing tetraphyllideans, previously placed in the family Onchobothriidae, with the members of the order Proteocephalidea. The Phyllobothriidea n. ord. is established for a subset of 12 non-hooked genera characterised by scoleces bearing four bothridia each with an anterior accessory sucker; most parasitise sharks and have been assigned to the Phyllobothriidae at one time or another. Tentative ordinal placements are suggested for eight additional genera; placements for the remaining tetraphyllidean genera have not yet emerged. We propose that these 17 genera remain in the “Tetraphyllidea”. Among these, particularly labile across analyses were Anthobothrium, Megalonchos, Carpobothrium, Calliobothrium and Caulobothrium. The unique association of Chimaerocestus with holocephalans, rather than with elasmobranchs, appears to represent a host-switching event. Both of the non-elasmobranch hosted clades of acetabulate cestodes (i.e. Proteocephalidea and Cyclophyllidea and their kin) appear to have had their origins with elasmobranch cestodes. Across analyses, the sister group to the clade of “terrestrial” cestode orders was found to be an elasmobranch-hosted genus, as was the sister to the freshwater fish- and tetrapod-hosted Proteocephalidea. Whilst further data are required to resolve outstanding nomenclatural and phylogenetic issues, the present analyses contribute significantly to an understanding of the evolutionary radiation of the entire Cestoda. Clearly, elasmobranch tapeworms comprise the backbone of cestode phylogeny.     

Grow fast,die young: Does compensatory growth reduce survival of juvenile blacktip sharks (Carcharhinus limbatus) in the western Gulf of Mexico?

Effective conservation and management necessitate an understanding of the ecological mechanisms that shape species life histories in order to predict how variability in natural and anthropogenic impacts will alter growth rates, recruitment, and survival. Among these mechanisms, the interaction between parturition timing and prey availability frequently influences offspring success, particularly when postnatal care is absent. Here, we assess how parturition timing and nursery conditions, including prey abundance and environmental conditions, influence the growth and potential survival of blacktip sharks (Carcharhinus limbatus) in western Gulf of Mexico (GOM) estuaries over their first year. Catch data from long‐term gillnet monitoring allowed for clear delineation of cohorts based on size frequency distribution plots, and showed that late parturition cohorts born in estuaries with fewer prey resources exhibited more rapid growth than early parturition cohorts that experienced more abundant prey. Compensatory behaviors that promoted accelerated growth led to reduced second year residency, likely due to reduced survival resultant from greater risk taking and potentially due to reduced site fidelity attributed to larger body size. Water temperatures influenced blacktip growth rates through physiological increases in metabolism and potential premigratory foraging cues associated with cooling temperatures. Gradual warming of the GOM (0.03°C year⁻¹) was also correlated with earlier parturition across the study period (1982–2017), similar to other migratory species. Considering current trends in climate and associated phenological shifts in many animals, testing hypotheses assessing compensatory growth‐risk trade‐offs is important moving forward to predict changes in life histories and associated recruitment in concert with current and future conservation actions, like wildlife management.     

Which alkylglycerols from shark liver oil have anti-tumour activities?

Alkylglycerols (alkyl-Gro) are ether lipids abundant in shark liver oil (SLO), and oral SLO or alkyl-Gro mix from this source have several in vivo biological activities including stimulation of haematopoiesis an immunological defences, or anti-tumour and anti-metastasis activities in vivo. Composition of natural alkyl-Gro mix contains several alkyl-Gro varying by chain length and unsaturation, and individual anti-tumour activity of each molecule present in natural mix remained unknown. We synthesized six prominent constituents of natural alkyl-Gro mix, namely 12:0, 14:0 16:0, 18:0, 16:1 n-7, and 18:1 n-9 alkyl-Gro. Using an in vivo model of grafted tumour in mice (3LL cells), we studied and compared the oral anti-tumour and anti-metastasis activities of each of these 6 alkyl-Gro. 16:1 and 18:1 alkyl-Gro showed strong activity in reducing lung metastasis number, while saturated alkyl-Gro had weaker (16:0) or no (12:0, 14:0, 18:0) effect. Spleen weights at day 20 after graft were also measured and showed tremendous variations depending on the treatment. Tumour graft resulted in a raise in spleen weight in control group, this raise was nearly abolished in 16:1 and 18:1 alkyl-Gro-treated mice, and was reduced in 14:0 and 16:0 alkyl-Gro-treated mice. Conversely, 18:0 alkyl-Gro-treated mice showed spleen weigh raise as compared with untreated grafted mice. These new data demonstrate a prominent role of unsaturation in the anti-tumour activities of alkyl-Gro.     

Do shark declines create fear‐released systems?

We illustrate the theoretical plausibility that fishery removal of sharks can indirectly alter predation pressure on different fish species via the behavioural responses of mesoconsumers released from predator intimidation. Our dynamic state variable model of foraging decisions by harbour seals, a mesopredator, predicted indirect effects of the removal of Pacific sleeper sharks on two species consumed by seals, Pacific herring and walleye pollock, as mediated by seal behaviour. Herring, a fatty fish, form near‐surface aggregations that often are ephemeral and widely dispersed. Pollock are found in the deeper strata preferred by sharks and have lower energy density than herring, but also are larger and their more continuous distribution potentially makes them the more predictable resource for seals. During simulations, predation risk from sharks produced an asymmetric trophic cascade mediated by the seal's underutilisation of deeper, riskier strata. Risk management by seals reduced mortality on pollock, which required riskier access in deep strata, while increasing mortality on herring, which could be accessed with less risk in shallow strata. This effect, however, attenuated if herring were scarcer and seal energy state was poor. During shark removal scenarios, seals shifted to deeper strata, increasing pollock consumption and substantially decreasing use of herring; the proportional change was greatest if seals were in good energy state. Prior studies have addressed how shark declines might affect community structure through density responses by species consumed by sharks; earlier models incorporating antipredator behaviour of the mesopredator (i.e. Ecosim/Ecospace) allow for activity reduction but not for the spatial shifts that altered the asymmetric trophic cascade in our simulations. Our results suggest that shark declines might have stronger ecological consequences than previously recognised if we account for spatial and diet shifts by mesoconsumers released from shark intimidation.     

Just keep swimming? Observations of resting behavior in gray reef sharks Carcharhinus amblyrhynchos (Bleeker, 1856)

Understanding the respiratory modes of sharks has important implications for studying the metabolism, energetics, and behavioral strategies of different species. Here we provide the first reported observations of resting behavior in the gray reef shark Carcharhinus amblyrhynchos, a species typically considered an obligate ram ventilator. Observations were made at several locations in the Republic of Seychelles, where sharks were found resting under reef ledges and were unresponsive to the presence of divers. These findings update our understanding of the respiratory mode of this species and have implications for future research.     

Is the tiger shark Galeocerdo cuvier a coastal species? Expanding its distribution range in the Atlantic Ocean using at‐sea observer data

The occurrence of tiger shark Galeocerdo cuvier in the Atlantic Ocean was assessed using at‐sea observer data from multiple pelagic longline fisheries. Geographic positions of 2764 G. cuvier recorded between 1992 and 2013 and covering a wide area of the Atlantic Ocean were compared with the currently accepted distribution ranges of the species. Most records fell outside those ranges in both the Southern and Northern Hemispheres, which strongly suggests that the distribution range of G. cuvier in the open ocean is considerably larger than previously described     

Human introduction or natural dispersion? Atlantic Ocean occurrence of the Indo‐Pacific whitetip reef shark Triaenodon obesus

Occurrence of multiple whitetip reef sharks Triaenodon obesus in the Atlantic Ocean is reported for the first time from near a sunken ferry off the Paraná coast in south‐eastern Brazil. This occurrence is hypothesized to have been caused by either a human introduction or a remarkably long oceanic displacement.