Mustelus Research Articles

Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species

Although an understanding of mating systems is thought to be an important component of long-term population management, these life history characteristics are poorly known in sharks. Here, we employ polymorphic microsatellite markers to test for the occurrence and prevalence of multiple paternity in a population of the brown smoothhound shark, Mustelus henlei. We analyzed litters from 14 females sampled from the Pacific coast of Baja California Sur. The minimum number of sires ranged from one to three with an average of 2.3 sires per litter. Regression analyses did not indicate a relationship between female body size and number of sires, or female body size and size of the litter. A review of the existing literature on genetic mating systems in sharks suggests that polyandry may be common and that reproductive behavior may have evolved from conflicting selection pressures between the sexes.

Isolation and characterization of microsatellite markers for the dusky smoothhound shark, Mustelus canis

A total of 32 nuclear-encoded microsatellites, including 15 polymorphic and 13 monomorphic microsatellites, isolated from an enriched genomic library of the triakid shark, Mustelus canis (dusky smoothhound), and four microsatellites previously isolated from two other triakid sharks were characterized in 91 individuals of M. canis. Polymorphic repeat motifs included 12 dinucleotide, two trinucleotide and one pentanucleotide repeat(s). Mustelus canis supports both commercial and recreational fisheries throughout its range in the western Atlantic Ocean from Maine (USA) to southern Argentina. The microsatellites characterized will be useful in studies of population structure of M. canis and other triakid sharks.

Characterization of 11 microsatellite loci for the brown smooth-hound shark, Mustelus henlei (Triakidae), discovered with next-generation sequencing

The brown smooth-hound shark, Mustelus henlei (Triakidae), is an endemic member of the eastern Pacific shark assemblage considered both commercially and recreationally important. Here, microsatellite loci for M. henlei discovered by next-generation sequencing (Roche 454 pyrosequencing) are described. All loci were polymorphic (3–10 alleles) with observed heterozygosities between 0.24 and 0.89 and expected heterozygosities between 0.23 and 0.86. These loci are the first to be characterized explicitly for M. henlei and should be useful for the investigation of population structure and gene flow in this species and for other members of the Triakidae.

Five new species of Acanthobothrium van Beneden, 1849 (Cestoda: Tetraphyllidea) in elasmobranchs from the northwest Atlantic and Gulf of Mexico with first records from smooth-hound sharks and guitarfish

Five new species of Acanthobothrium van Beneden, 1849 are described from elasmobranchs from Atlantic coastal waters of the United States and western Gulf of Mexico. Acanthobothrium cairae sp. nov., a category 3 species, from the roughtail stingray Dasyatis centroura (Mitchill), from New England coastal waters of Narragansett Bay, Rhode Island is differentiated from congeners by a combination of characteristics including hook lengths, testis number (82–166) and distribution, bilobed ovary and 8 large muscle fascicles symmetrically encircling the reproductive organs. Four new category 1 species of Acanthobothrium from four new host species from the Gulf of Mexico are Acanthobothrium lentiginosum sp. nov. from the rhinobatid (guitarfish), Rhinobatos lentiginosus Garman; Acanthobothrium schalli sp. nov. from two species of triakid sharks, Mustelus canis canis Mitchill and M. norrisi Springer; and Acanthobothrium ulmeri sp. nov. and A. westi sp. nov., both from the skate Raja texana Chandler (Rajidae). Acanthobothrium floridensis Goldstein, 1964 is reported from a new host, R. texana off the Texas coast in the western Gulf of Mexico, a new locality for this species. These species are differentiated by a combination of characters including size, bothridial size, total hook length, ratio of total hook length to bothridium length, ratio of bothridial length to cephalic peduncle length, ovarian shape, position of the genital pore, testis number and distribution. Biogeographically these records from sharks and the guitarfish are new for Acanthobothrium and add two new host families to the distribution of Acanthobothrium in coastal waters of the western Atlantic Ocean. Acanthobothrium is now known to occur in six families of elasmobranchs in the Gulf of Mexico: skates (Rajidae), rays (Dasyatidae, Gymnuridae, Myliobatidae), sharks (Triakidae) and guitarfish (Rhinobatidae) making it the most diverse geographical region for these cestodes in the eastern coastal waters of North America.

Habitat use, movements and site fidelity of the gray smooth-hound shark ( Mustelus californicus Gill 1863) in a newly restored southern California estuary

It is thought that some elasmobranchs use shallow temperate estuaries during warmer months because these habitats may provide thermal physiological advantages. However, extensive loss and degradation of southern California bays and estuaries has reduced coastal species access to estuarine habitats. While restoration of southern California estuaries has increased over the last two decades, little is known about the recovery of ecological function. Top predators are thought to be important indicators of restoration of ecological function in many ecosystems, including estuarine habitats. In this study, abundance surveys and acoustic telemetry were employed to examine how gray smooth-hound sharks (GSH) use the newly restored Full Tidal Basin (FTB) of Bolsa Chica. GSH were most abundant inside the FTB during the spring and summer, and numbers decreased during the winter. Over 83% of all individuals (n = 336) caught were immature juveniles and were most abundant when water temperatures were between 20 and 22 °C. Sharks fitted with acoustic transmitters ( n = 22) were continuously detected for 6–153 days (August 2008–December 2009). Forays into coastal waters were uncommon until individuals left for the season. GSH selected warmer habitats within the middle FTB; however, they also exhibited diel movements along the basin. GSH were most often found associated with mud and eelgrass at night, presumably for feeding. Since its restoration, population and behavioral data suggest that the FTB may provide juvenile GSH with a suitable seasonal environment for feeding and growth.

Characterization of 13 microsatellite loci for the tope shark, Galeorhinus galeus, discovered with next-generation sequencing and their utility for eastern Pacific smooth-hound sharks (Mustelus)

The tope shark, Galeorhinus galeus, is a commercially important member of the Triakidae that has been exploited globally for the past 80 years. Here we describe 13 microsatellite loci for G. galeus discovered by next-generation sequencing (Roche 454 pyrosequencing) and their utility for eastern Pacific smooth-hound sharks (Mustelus). These loci were polymorphic (3–12 alleles) with observed heterozygosity between 0.11 and 0.86 and expected heterozygosity between 0.24 and 0.87. Several loci (7 of 13) amplified consistently for Mustelus californicus and M. henlei. These loci are the first to be characterized explicitly for G. galeus and should be useful in the investigation of population structure of this vulnerable elasmobranch.

Concentration of DL-PCBs in fish from market of Parma city (north Italy): Estimated human intake

The concentrations of 12 congeners of non-ortho and mono-ortho dioxin-like polychlorinated biphenyls (ΣDL-PCB) were measured in 30 fish samples from Parma markets by GC/MS technique. The samples were randomly purchased, choosing the species commonly found in supermarkets. The concentration of DL-PCBs estimated remained under the fixed Italian limit of 4 pg g −1 ww WHO-TEQ (World Health Organization–Toxic Equivalent) in the major part of the samples, so the situation seems to be not at a level sufficient to pose a risk to human health of the Parma population. The medium daily intake for DL-PCBs for Italian consumers (Parma) was also estimated. This value generally resulted minor than 2 pg g −1 ww WHO-TEQ kg −1 body weight, exceeding only in four cases: eel, smooth hound, starry smooth hound and tuna.

Ontogenetic habitat preferences of the narrownose smooth-hound shark, Mustelus schmitti, in two Southwestern Atlantic coastal areas

The aim of this study was to determine the ontogenetic habitat preferences of the narrownose smooth-hound shark, Mustelus schmitti, in Rio de la Plata and El Rincon coastal areas. There, canonical correspondence analyses of fishery research survey data showed that M. schmitti ontogenetic stages were differentially affected by depth, temperature and salinity. Neonates and juveniles were more abundant and remain in nearshore waters, suggesting the presence of nursery areas in which food availability and environmental conditions allow a faster growth. Adults M. schmitti presented different environmental associations mainly associated with depth and temperature. During non-reproductive season they were associated with deeper coastal waters. With the arrival of the reproductive season, adults migrate from deep to nearshore waters and show sexual segregation associated with pre- or post-mating behaviors. Hence, the year-round presence of neonates and juveniles and the seasonal occurrence of adults in nearshore waters make this habitat essential to M. schmitti population dynamics since key ontogenetic stages will be vulnerable if a direct impact occurs there.

Catch and size selectivity of small-scale fishing gear for the smooth-hound shark Mustelus mustelus (Linnaeus, 1758) (Chondrichthyes: Triakidae) from the Aegean Turkish coast

Catch rate, CPUE, biomass ratios and size selectivity from traditional longline and trammel nets of Turkish coastal small-scale fisheries were investigated in order to describe the Smooth-hound shark (Mustelus mustelus) fishery. The SELECT method was used to estimate the selectivity parameters of a variety of models for the trammel nets inner panel of 150 and 170 mm mesh sizes. Catch composition and proportion of the species were significantly different in longline and trammel nets. While mean CPUE of longline was 119.2±14.3 kg/1000 hooks, these values for 150 and 170 mm trammel nets were 5.3±1.2 kg/1000 m of net and 12.7±3.9 kg/1000 m of net, respectively. Biomass ratios of the by catch to Smooth-hound catch were found to be 1:0.32 for 150 mm trammel net, 1:0.65 for longline and 1:0.73 for 170 mm trammel net. The estimated modal lengths and spreads were found to be 91.1 and 16.2 cm for 150 mm and 103.2 and 18.4 cm for 170 mm, respectively. The modal lengths of the species as well as the spread values increased with mesh size.

Low genetic diversity and population structure of the narrownose shark ( Mustelus schmitti)

The narrownose smooth-hound shark Mustelus schmitti is a coastal species endemic to the Southwest Atlantic Ocean. As this species is an important fishery resource, there is interest in knowing its genetic population structure. In this study, we used mitochondrial cytochrome b gene sequences to examine the genetic structure of the narrownose smooth-hound populations within the Río de la Plata and its Maritime Front in the SW Atlantic Ocean. We found no evidence for genetic structure in the analyzed samples. Low levels of pairwise Φ ST values indicated high connectivity and suggested genetic homogeneity at this geographic range. Additionally, notably low nucleotide and haplotype diversities found in this species could indicate that M. schmitti experienced a population bottleneck, recent expansion or selection. The results presented here indicate that M. schmitti exists as a single demographic unit in the Río de la Plata and its Maritime Front. The low genetic diversity values found in the present study, together with the low resilience to exploitation of this species, raise considerable concern over the conservation status of M. schmitti.

Extraction and functional properties of gelatin from the skin of cuttlefish (Sepia officinalis) using smooth hound crude acid protease-aided process

The characteristics and functional properties of gelatin from skin cuttlefish (Sepia officinalis) were investigated and compared to those of halal bovine gelatin (HBG). The gelatin extraction efficiency was improved by an acid-swelling process in the presence of smooth hound crude acid protease extract (SHCAP). The yields of gelatins from cuttlefish skin after 48h with acid and with crude acid protease (15units/g alkaline-treated skin) were 2.21% and 7.84%, respectively. The gelatin from skin cuttlefish had high protein (91.35%) but low fat (0.28%) contents. Compared to HBG, the cuttlefish-skin gelatin (CSG) has different amino acids composition than halal bovine gelatin. CSG contained slightly low hydroxyproline and proline (180‰) than HBG (219‰), whereas the content of serine was higher (49‰ versus 29‰). The gel strength of the gelatin gel from CSG (181g) was lower than that of HBG (259g) (p<0.05) possibly due to lower hydroxyproline content. Cuttlefish-skin gelatin exhibited a similar emulsifying activity but greater emulsifying and foam stability than the halal bovine gelatin (p<0.05). Foam formation ability, foam stability and water-holding capacity of CSG were slightly lower than those of the HBG, but fat-binding capacity was higher in the cuttlefish gelatin.

Rapid isolation of the first set of polymorphic microsatellite loci from the Australian gummy shark, Mustelus antarcticus and their utility across divergent shark taxa

The development of genetic markers for studies of population structure and genetic diversity can be applied to improving management and monitoring of commercially fished species. Here we report on the use of high-throughput (454) sequencing to develop a panel of 12 novel polymorphic microsatellite markers for the commercially harvested gummy shark, Mustelus antarcticus. This constitutes the first suite of microsatellites developed for the genus Mustelus, a group which features in commercial fisheries around the world. We demonstrate the successful amplification of these markers in other species of Mustelus and test their utility in species from an additional nine genera of shark.

First record of Polyonyx gibbesi (Anomura: Porcellanidae) in the Argentine Sea

The present paper reports the occurrence of Polyonyx gibbesi in Argentinean shelf waters and extends its distribution southwards in the western Atlantic. Forty-four specimens of P. gibbesi were found in stomach contents of the narrownose smoothhound shark Mustelus schmitti during November 2008.

Distribution of trace elements in the tissues of smooth hound Mustelus mustelus (Linnaeus, 1758) from the southern–eastern waters of Mediterranean Sea (Italy)

Trace element concentrations (Hg, Cd, Pb, Cr, Ni, Cu, Zn) were determined in the muscle, gonads, skin, and brain of smooth hound Mustelus mustelus in order to define the metal distribution patterns. The data indicated that metal accumulation depended on the tissues probably as a consequence of metabolic needs, physiochemical properties, and detoxification processes specific for each element. Metal concentrations were higher in gonads (Hg 0.10-0.70 μg g(-1); Cd 0.02-0.10 μg g(-1); Pb 0.08-0.39 μg g(-1); Cr 0.06-0.36 μg g(-1); Ni 1.37-3.00 μg g(-1); Zn 9.15-16.30 μg g(-1); Cu 1.95-21.62 μg g(-1)) and skin (Hg 0.16-0.66 μg g(-1); Cd 0.01-0.04 μg g(-1); Pb 0.10-0.62 μg g(-1); Cr 0.15-0.68 μg g(-1); Ni 1.60-7.20 μg g(-1); Zn 9.00-16.00 μg g(-1); Cu 0.78-6.80 μg g(-1)) than brain (Hg 0.04-0.34 μg g(-1); Cd 0.01-0.05 μg g(-1); Pb 0.03-0.59 μg g(-1); Cr 0.08-0.48 μg g(-1); Ni 5.59-9.69 μg g(-1); Zn 5.90-7.35 μg g(-1); Cu 0.90-4.02 μg g(-1)), while muscle always exhibited the lowest levels (Hg 1.03-2.58 μg g(-1); Cd 0.01-0.06 μg g(-1); Pb 0.02-0.16 μg g(-1); Cr 0.05-0.28 μg g(-1); Ni 1.13-2.48 μg g(-1); Zn 2.64-5.06 μg g(-1); Cu 0.33-2.23 μg g(-1)). Ni and Hg took exception having the highest concentrations in brain and muscle, respectively. An assessment of the risk for human due to the consumption of these marine organisms was also undertaken. Regarding Cd and Pb intakes, consumption did not guide to any concerns, while it should be extremely moderate when considering Hg intake. The comparative analyses revealed that Mediterranean sharks were exposed to higher Hg levels than biota inhabiting open ocean.

Biochemical Properties of Anionic Trypsin Acting at High Concentration of NaCl Purified from the Intestine of a Carnivorous Fish: Smooth Hound (Mustelus mustelus)

Trypsin from the intestine of smooth hound (Mustelus mustelus) was purified by fractionation with ammonium sulfate, Sephadex G-75 gel filtration, and DEAE-cellulose ion exchange chromatography, with a 65-fold increase in specific activity and 15% recovery. The molecular weight of the purified trypsin was estimated to be 24 kDa using size exclusion chromatography and sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE). The purified enzyme showed esterase-specific activity on N(alpha)-p-tosyl-L-arginine methyl ester hydrochloride (TAME) that was four times greater than its amidase-specific activity on Nalpha-benzoyl-DL-arginine-p-nitroanilide (BAPNA). The optimum pH and temperature for the trypsin activity were pH 8.5 and 50 degrees C, respectively, using TAME as a substrate. The enzyme was extremely stable in the pH range of 7.0-9.0 and highly stable up to 40 degrees C after 1 h of incubation. The purified enzyme was strongly inhibited by soybean trypsin inhibitor (SBTI) and N-p-tosyl-1-lysine chloromethyl ketone (TLCK), specific inhibitors for trypsin. In addition, smooth hound trypsin showed higher proteolytic activity at high NaCl concentration, demonstrating its potential for protein hydrolysis at high salt content. The N-terminal amino acid sequence of the first 12 amino acids of the purified trypsin was IVGGYECKPHSQ. This sequence showed high homology with trypsins from marine vertebrates and invertebrates. Purified trypsin had a Michaelis-Menten constant (K(m)) and catalytic constant (K(cat)) of 0.387 +/- 0.02 mM and 2.62 +/- 0.11 s(-1), respectively, when BAPNA was used as a substrate. For the hydrolysis of TAME, K(m) and K(cat) were 0.156 +/- 0.01 mM and 59.15 +/- 2.2 s(-1), respectively.

Evaluation of angiotensin I-converting enzyme (ACE) inhibitory activities of smooth hound (Mustelus mustelus) muscle protein hydrolysates generated by gastrointestinal proteases: identification of the most potent active peptide

In this study, smooth hound protein hydrolysates (SHPHs), obtained by treatment with various gastrointestinal proteases, were analyzed for their angiotensin I-converting enzyme (ACE) inhibitory activities. Protein hydrolysates were obtained by treatment with crude alkaline enzyme extract, low molecular weight (LMW) alkaline protease, trypsin-like protease and pepsin from Mustelus mustelus, and bovine trypsin. All hydrolysates exhibited inhibitory activity toward ACE. Hydrolysate generated with alkaline protease extract displayed the highest ACE inhibitory activity, and the higher inhibition activity (82.6% at 2 mg/mL) was obtained with a hydrolysis degree of 18.8%. This hydrolysate was then fractionated by size exclusion chromatography on a Sephadex G-25 into five major fractions (P1–P5). ACE inhibitory activities of all fractions were assayed, and P3 was found to display a high ACE inhibitory activity (62.24% at 1 mg/mL). P3 was then fractionated by reversed-phase high-performance liquid chromatography (RP-HPLC) and ten fractions of ACE inhibitors were found (F1–F10). Sub-fraction F3 showed the strongest ACE inhibitory activity, being able to suppress more than 60% of initial enzyme activity at a concentration of 100 μg/mL. The amino acid sequence of peptide F3 was determined by ESI/MS and ESI–MS/MS as Ala-Gly-Ser, and the IC50 value for ACE inhibitory activity was 0.13 ± 0.03 mg/mL. Further, purified peptide F3 maintained inhibitory activity even after in vitro digestion with gastrointestinal proteases in order to demonstrate gastrointestinal stability digestion to enable oral application. These results indicate that smooth hound protein hydrolysate possesses potent antihypertensive activity.

Evidence of in vivo satietogen effect and control of food intake of smooth hound ( Mustelus mustelus) muscle protein hydrolysate in rats

Protein hydrolysates are of a significant interest, due to their potential application as a source of bioactive peptides in nutraceutical and pharmaceutical domains. The present study was focused on the effect of protein hydrolysate from smooth hound ( Mustelus mustelus) (SHPH) in the regulation of components of the food intake control such as satiety. SHPH was produced by intestinal digestive proteases from the same species. The amino acid analysis by GC/MS showed that the hydrolysate was rich in leucine, alanine, glycine, threonine, serine, lysine and glutamate. The molecular weights of peptides in SHPH were estimated by ESI-MS to be between 200 and 2500 Da. Biological in vivo capacities of SHPH in rats were evaluated by determination of the CCK-like peptides and insulin content using a clinical human radioimmunoassay. The food intake and the body weight of rats were measured during the period of treatment. Rats treated with SHPH showed a significant decrease in body weight at the end of treatment, as well as a decrease of food intake. Our findings revealed a possible mechanism of the beneficial effects of SHPH in appetite regulation, and this might be important to prevent the risk of a number of medical conditions including type II diabetes.

Demographic structure of broadnose seven-gill shark, Notorynchus cepedianus, caught by anglers in southern Patagonia, Argentina

Between 2004 and 2007, tournament editions and the recreational fishery for the broadnose seven-gill shark, Notorynchus cepedianus, were monitored in Natural Reserves of Ría Deseado (RD, a breeding area for the Patagonian smooth hound) and Peninsula de San Julian (SJ), southern Patagonia, Argentina. Sharks' catch composition by sex; total length (TL) and weight (W) were recorded. Reproductive status was assessed from the literature. Juvenile females dominated the catches in both areas during the 4-year period.

Diet composition of smooth-hound shark,Mustelus mustelus(Linnaeus, 1758), in the Gulf of Gabès, southern Tunisia

Summary The diet of the smooth-hound shark, Mustelus mustelus, from the Gulf of Gabes (southern Tunisia, central Mediterranean Sea) was investigated with respect to fish size and season. Stomach contents were analyzed from 540 specimens with total lengths ranging from 34 to 158.5 cm. Of the total number of stomachs examined, 63 were empty (11.67%). Smooth-hound shark fed mainly on crustaceans, fishes and cephalopods. Sipunculids, polychaetes and echinoderms were occasional preys. No differences were found between the diets of males and females. Ontogenetic changes in diet of M. mustelus were apparent, with crustaceans forming a greater proportion of the diet of smaller sharks. Both teleosts and molluscs increased in importance with increasing shark size. Consumptions of polycheates, sipunculids and echinoderms were not related to predator size. Prey diversity also increased with size, with large and mobile prey species found more commonly in the diet of larger sharks. The limited overlap in the dietary compositions of juveniles, subadults and adults suggests the possibility of resource partitioning. Seasonality in food habits was in accordance with the dynamics of the predator and the prey species.

Cuttlefish use startle displays, but not against large predators

Prey animals can survive a predatory encounter if they communicate unprofitability to an approaching predator. Otherwise undefended prey often use conspicuous deimatic (frightening) displays to intimidate closely approaching predators into delaying or aborting an attack. The ‘startle’ displays of several insect groups are the best-known example: comprising a sudden size increase coupled with a conspicuous ‘eyespot’ pattern, these displays can effectively deter highly dangerous avian predators, although they are often unsuccessful. Cephalopods perform remarkably similar visual displays that are presumed to function in the same way, although evidence for this is lacking. Unlike large insects, cephalopods possess rapid escape responses, and seem unlikely to benefit from predator hesitation. Moreover, field and laboratory-based observations with cuttlefish suggest that what has previously been labelled the Deimatic Display may be directed towards small teleosts that pose little or no direct predation risk. In staged encounters between cuttlefish, Sepia officinalis , and large predatory fish (sea bass, Dicentrarchus labrax and smooth hound Mustelus mustelus ), naïve cuttlefish did not perform their Deimatic Display towards large predators, even when spatially constrained and unable to flee. Cuttlefish also discriminated between large predators, selectively using a different visual signal (previously termed the Flamboyant Display) towards the more dangerous teleost fish. These results strongly suggest that, although superficially similar, cephalopod deimatic displays are functionally different to insect displays: large brains and keen senses allow cuttlefish to discriminate between species, and selectively signal to small and only indirectly threatening teleost intruders, rather than highly dangerous predators.