First evidence of multiple paternity in the blue shark (Prionace glauca)

Multiple paternity (MP) is defined as the behaviour in which females successfully mate with multiple males leading to offspring from different sires within the same litter. MP seems to be frequent and an evolutionary advantage in elasmobranchs. Here the authors report for the first time the occurrence of MP in the cosmopolitan blue shark Prionace glauca L. The evidence, gathered via microsatellite genotyping of pregnant females and their embryos, suggests that MP is very frequent in this species. Knowledge of MP in P. glauca should help describe more precisely its reproductive biology and contribute to the management of its populations.     

The fine structure of the intra-uterine epithelium during late gestation in the blue shark,Prionace glauca

The fine structure of the intra-uterine epithelium of the pregnant blue shark,Prionace glauca, was examined. The intra-uterine epithelium was bilaminar and the underlying epithelial cell was extremely reduced in cytoplasm. Two cytological characteristics were shown in the outer epithelial cell; open inter-cellular spaces closed in the apical portion by a junction complex and, numerous mitochondria distributed in the basal and lateral portions of the cytoplasm. Secretive characteristics were not recognized in the outer epithelial cell, although few regions composed only of mucous cells were seen. The flattened endothelium of the capillary lay closely beneath the epithelium. These structures are thought to facilitate the water-solute transport and gaseous exchange. It suggests that the intra-uterine epithelium is involved in the osmoregulation of the uterine fluid and the exchange of respiratory gases between mother and fetus.     

Mating scars reveal mate size in immature female blue shark Prionace glauca

The objective of this study was to determine the size and maturity status of the male blue sharks Prionace glauca attempting to mate with small, immature females in the north‐west Atlantic Ocean. The relationship between male curved fork length (L_FC) and jaw gape was used in conjunction with the diameter of the mating scar to estimate the L_FC and infer the maturity status of the male shark that produced the mating scar. The results indicate that mature males with a mean ± s.d . L_FC of 218 cm ± 23 cm were attempting to mate with sexually immature females.     

Isolation of enamelinlike proteins from blue shark (Prionace glauca) enameloid

A sequential dissociative extraction scheme was used to extract proteins from developing Blue Shark enameloid. The first extraction solution (4 M guanidine HC1) solubilized the polypeptides, mainly collagenous, not closely associated with the hydroxyapatite. The next extraction solution (4 M guanidine HC1, 0.5 M ethylenediaminetetraacedic acid (EDTA] solubilized the proteins more closely associated with the tooth mineral component. After extraction, the proteins were separated and isolated with gel electrophoresis. Protein molecular weights were determined and selected proteins were isolated for amino acid composition analysis. The two proteins isolated were tested for mammalian enamel protein antigenic determinants by a "Dot" immunobinding assay. The isolated proteins were enamelinlike by extraction criteria and amino acid composition. Further, the two proteins share antigenic determinants with mammalian enamel proteins.     

The abundance of the blue shark,Prionace glauca,in the western English Channel

Synopsis Since 1952, a sport fishery for the blue shark,Prionace glauca, has existed off the south coast of Cornwall in England. Annual catches from this fishery have ranged from < 200 to>6000 sharks. The fishery was based on a previously unexploited stock in the 1950s. The abundance of the species in the English Channel declined in the early 1960s and again in the mid-1970s. The declining abundance was investigated in relation to sea surface temperature (SST), prey abundance, and fishing pressure. Short-term fluctuations in SST were found to be responsible for changes in the distribution of the population, but not for changes in abundance. The abundance of prey species in the Channel was observed to be inversely related to the abundance of blue sharks. The reduced abundance of blue sharks lowered the level of effective predation on the prey populations, allowing their abundance to increase. It was concluded that the nature of the fishing practice off the Cornish coast was responsible for a significant part of the decrease in shark abundance. By killing large numbers of sub-adult females, the reproductive capacity of the population was lowered. Continued fishing pressure prevented the population from recovering; and as of 1987, the abundance of the species in the Channel is still declining. Various conservation measures have been proposed.     

Identification and characterization of polymorphic microsatellite loci in the blue shark Prionace glauca, and cross-amplification in other shark species

Two to 14 alleles were found to be segregating per locus (mean 5·2), with observed and expected heterozygosities ranging from 0·08 to 0·78 and 0·08 to 0·94, respectively. Cross-amplification of six of these microsatellite loci indicated that they are also polymorphic in three species of Carcharhiniformes and two species of Lamniformes. The newly developed primers reported here constitute a useful tool for genetic population analyses on Prionace glauca and, potentially, other related species.     

Presence of new disulphide-bonded collagens in shark Prionace glauca muscle

• 1.1. Two new collagenous fragments were detected in great blue shark myocommata.
• 2.2. The fragments, isolated from pepsin digests, were shown to be sensitive to disulphide bond cleaving agents. The higher molecular weight fragment (designated HMW) of about 250 kDa gave rise to a 40 kDa fragment following reduction. The second fragment with a molecular weight of about 53 kDa (designated LMW) produced a major fragment of about 29 kDa after reduction with disulphide bond cleaving agents.
• 3.3. Type I collagen, a type I-like collagen and type V collagen were also detected in the myocommata.

     

Development of an alternative ageing technique for blue shark (Prionace glauca) using the vertebra

Accurate determination of age is essential for the comprehensive assessment and management of exploited shark populations. Enhancement of growth bands is necessary to accurately and efficiently determine age. However, most traditional techniques do not describe an efficiency of a series of procedures and the detailed protocol for different‐sized sharks. We describe a simple and highly successful technique for ageing vertebrae of blue shark (Prionace glauca) that we refer to as “burn method”, derived from the “break and burn method” and “shadowing method”—a simple procedure requiring an alkaline treatment to clean the vertebral centra and a burning treatment to enhance growth band visualization. We described optimal times for sharks of precaudal length of 50, 100, 150, and 200 cm as 44.9, 88.7, 134.0, 183.5 s of alkaline treatment, and 6.8, 8.9, 10.2, and 11.5 min of burning treatment; both longer and shorter exposure times resulted in higher failed sample frequencies. Using our burn method, it is possible to do ageing a sample from a wide angle, with the reader able to obtain information on growth bands from different perspectives. To critique different technique efficiencies, the index of average percent error (IAPE) and mean coefficient of variation (CV) are compared for independent readers using the burn method and other techniques (silver nitrate impregnation and the unstained shadowing methods). The precision of the burn method (IAPE, 4.1%; CV, 5.7%) was similar to that of silver nitrate impregnation (IAPE, 5.8%; CV, 8.2%) and unstained shadowing method (IAPE, 8.3%; CV, 11.8%). For younger specimens, the IAPE and CV of the burn method were lower than those of the other techniques, but, compared with other ageing methods, precision decreased for older sharks. We demonstrate that the burn method to be accurate for age determination of blue sharks, especially for specimens with less than 10 bands, but recommend simultaneous use of other methods, such as thin sectioning (the most common for structure‐based ageing) and bomb carbon dating, to accurately determine the age of older individuals.     

Morphological abnormalities in a blue shark Prionace glauca (Chondrichthyes: Carcharhinidae) foetus from southern Brazil

This study records the occurrence of a blue shark Prionace glauca foetus, with morphological abnormalities in the trunk and cephalic region, from a female caught by a pelagic longline in October 2003, in southern Brazil.     

World without borders—genetic population structure of a highly migratory marine predator,the blue shark (Prionace glauca)

Highly migratory, cosmopolitan oceanic sharks often exhibit complex movement patterns influenced by ontogeny, reproduction, and feeding. These elusive species are particularly challenging to population genetic studies, as representative samples suitable for inferring genetic structure are difficult to obtain. Our study provides insights into the genetic population structure one of the most abundant and wide‐ranging oceanic shark species, the blue shark Prionace glauca, by sampling the least mobile component of the populations, i.e., young‐of‐year and small juveniles (<2 year; N = 348 individuals), at three reported nursery areas, namely, western Iberia, Azores, and South Africa. Samples were collected in two different time periods (2002–2008 and 2012–2015) and were screened at 12 nuclear microsatellites and at a 899‐bp fragment of the mitochondrial control region. Our results show temporally stable genetic homogeneity among the three Atlantic nurseries at both nuclear and mitochondrial markers, suggesting basin‐wide panmixia. In addition, comparison of mtDNA CR sequences from Atlantic and Indo‐Pacific locations also indicated genetic homogeneity and unrestricted female‐mediated gene flow between ocean basins. These results are discussed in light of the species' life history and ecology, but suggest that blue shark populations may be connected by gene flow at the global scale. The implications of the present findings to the management of this important fisheries resource are also discussed.     

Feeding habits of the blue shark, Prionace glauca, and salmon shark, Lamna ditropis, in the transition region of the Western North Pacific

We describe the feeding habits of 70 blue sharks (Prionace glauca) and 39 salmon sharks (Lamna ditropis) caught at 0–7 m depth at night by research drift gillnets in the transition region of the western North Pacific during April–May of 1999 and 2000. Blue sharks of 50–175 cm total length fed on a large variety of prey species, consisting of 24 species of cephalopods and 16 species of fishes. Salmon sharks of 69–157 cm total length fed on a few prey species, consisting of 10 species of cephalopods and one species of fish. Important prey for the blue sharks were large, non-active, gelatinous, meso- to bathypelagic cephalopods (e.g., Chiroteuthis calyx, Haliphron atlanticus, Histioteuthis dofleini and Belonella borealis) and small myctophid fishes. Important prey for the salmon sharks were mid-sized, active, muscular, epi- to mesopelagic squids (e.g. Gonatopsis borealis, Onychoteuthis borealijaponica and Berryteuthis anonychus). Our results suggest that blue sharks feed on cephalopods mainly during the daytime when they descend to deep water. Salmon sharks may feed opportunistically with no apparent diurnal feeding period. Blue sharks and salmon sharks have sympatric distribution in the transition region in spring; they have different feeding habits and strategies that reduce competition for food resources.     

Isolation and characterization of Cu,Zn superoxide dismutase of the shark Prionace glauca

A Cu,Zn superoxide dismutase was purified for the first time from an elasmobranch species (Prionace glauca) and showed the following differences with respect to other animal superoxide dismutases. The enzyme displays a low isoelectric point. The enzyme activity is unusually independent of ionic strength. The isolated enzyme has 30% of its copper in the reduced state.     

Oxidative stress indicators and trace elements in the blue shark (Prionace glauca) off the east coast of the Mexican Pacific Ocean

Trace element concentrations and oxidative stress indicators (including production of reactive oxygen species (ROS), antioxidant enzyme activities and oxidative damage) were measured in muscle of blue sharks collected along the west coast of Baja California Sur to determine potential differences by sex and maturity cohorts. Mercury (Hg) concentration in muscle samples from larger sharks (>200 cm LT) exceeded the permissible limit (>1 ppm wet weight) for human consumption set by numerous international agencies. Significant differences were found in Hg concentrations (mature>immature; males>females), and in protein carbonyl concentrations (male>female); however, except for carbonyl protein levels, no significant differences by sex or maturity stage were found in the oxidative stress indicators. Differences between sexes and maturity stages in trace element concentration and carbonyl protein levels in blue shark muscle may be related to variations in diet within different cohorts.     

Distribution of Kroeyerina elongata (Kroyeriidae: Siphonostomatoida, Copepoda) in the olfactory sacs of the blue shark, Prionace glauca

The infection pattern of Kroeyerina elongata (Kroyeriidae, Copepoda) in the olfactory sacs of the blue shark, Prionace glauca, was investigated using 4,722 copepods from 54 olfactory sacs. Copepod prevalence and mean intensity of infection per olfactory sac were 94.0 and 91.1%, respectively, and the most intensely infected olfactory sac and shark hosted 218 and 409 copepods, respectively. There were significant linear relationships between the number of female and total copepods per left olfactory sac and shark fork length as well as between the numbers of female, male, and total copepods per shark and mean olfactory sac width and cumulative olfactory sac width. Female copepods typically outnumbered males within olfactory sacs (mean intensity = 65.7 and 26.3, respectively), and no statistical differences were detected between the numbers of copepods inhabiting the left and right olfactory sacs. Copepods were not evenly distributed within olfactory sacs. Typically, female copepods occupied olfactory chambers located centrally along the length of the olfactory sac, while males infected lateral olfactory chambers nearest the naris. The orientation of most copepods (84.6%) suggested positive rheotaxis relative to the path of water through the olfactory sac. Within olfactory chambers, most mature females (68.2%) infected the first third of the peripheral excurrent channel and the adjacent fringe of olfactory lamellae, while most males (91.7%) infected the olfactory lamellae, and the 4 larval females collected were attached within the lamellar field and grasped by males. Based on the observed infection patterns and the pattern of water flow throughout the olfactory sac, a hypothesis regarding the life cycle of K. elongata is advanced wherein infective copepodids are swept into the olfactory sac from the surrounding sea and initially colonize the olfactory lamellae. Copepodids feed and mature among the olfactory lamellae, and adult males search for mates and copulate with young females among the olfactory lamellae. Inseminated females move to the peripheral excurrent channels to mature and produce ovisacs. Hatching ovisacs release free-swimming nauplii into the excurrent water flow to be swept into the milieu, where they can molt into infective copepodids that may infect new hosts.     

Blue shark Prionace glauca fin-to-carcass-mass ratios in Spain and implications for finning ban enforcement

This study examines the processing of fins from blue sharks Prionace glauca caught by the Spanish longline fleet and landed in Vigo, Spain, and implications of these practices for enforcing the E.U. ban on shark finning, which relies on a maximum fin-to-carcass-mass ratio. Two major sources of variability in fin-to-carcass ratios are quantified and discussed: (1) the fin set (type and number of fins retained from each shark) and (2) the cutting method used to separate fins from carcasses. The significant differences in fin-to-carcass-mass ratios between fin sets or cutting procedure demonstrates that the ratio limit is problematic and, conclusively, in order to facilitate proper enforcement, fishermen should be required to land all sharks with the fins still naturally attached to the bodies.     

Testicular degeneration during spermatogenesis in the blue shark,Prionace glauca: Nonconformity with expression as seen in the diametric testes of other carcharhinids

The elasmobranch testis consists of spherical spermatocysts, each housing a single germ cell stage and its own clone of Sertoli cells. Because of the simple diametrical arrangement of cysts in maturational order, the testes of Squalus acanthias, Scyliorhinus canicula, and Prionace glauca are classified as the diametric shark testis type. The aim of this study was to document histologically the spermatocyst composition in the blue shark stage‐by‐stage and to establish whether the diametric testis type confers any uniformity regarding the expression of spermatogenesis in all sharks with this testis type. Analysis of the testes of blue sharks breeding in summer revealed extensive cyst degeneration of various forms and degrees, cyst shrinkage, and cyst disorganization with or without evidence of cell death, initially at the spermatogonia—spermatocyte transition but predominantly in spermatocyte and spermatid cysts. Animals could be grouped into two categories based on the major degenerative phenomena observed, namely those with extensive multinucleate cell (MNC) formation, and those with pronounced vacuolation in cysts. A major finding was the significant (P < 0.001) predominance of MNC formation and vacuolation in late‐stage spermatogonial cysts in the respective categories of sharks. Spermatocyte cysts showed varying degrees of germ cell depletion, with or without evidence of degeneration. Normal‐looking, but clearly subnormal‐sized primary and secondary spermatocyte cysts with no evidence of degeneration were significantly the dominant spermatocyte cyst types in both categories. It is proposed that these subnormal‐sized spermatocyte cysts could proceed into spermiogenesis. Because neighboring spermatid cysts lacked ordered bundling of spermatid heads (disorganized), a morphology significantly correlated with the vacuolation category of sharks, these results suggest that further progression into spermiogenesis was halted in such cysts. Thus, testicular degeneration in the diametric testis type is species specific in quantity and quality. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Quantifying the impact of environmental variables upon catch per unit effort of the blue shark Prionace glauca in the western English Channel

The effect of environmental variables on blue shark Prionace glauca catch per unit effort (CPUE) in a recreational fishery in the western English Channel, between June and September 1998–2011, was quantified using generalized additive models (GAMs). Sea surface temperature (SST) explained 1·4% of GAM deviance, and highest CPUE occurred at 16·7° C, reflecting the optimal thermal preferences of this species. Surface chlorophyll a concentration (CHL) significantly affected CPUE and caused 27·5% of GAM deviance. Additionally, increasing CHL led to rising CPUE, probably due to higher productivity supporting greater prey biomass. The density of shelf‐sea tidal mixing fronts explained 5% of GAM deviance, but was non‐significant, with increasing front density negatively affecting CPUE. Time‐lagged frontal density significantly affected CPUE, however, causing 12·6% of the deviance in a second GAM and displayed a positive correlation. This outcome suggested a delay between the evolution of frontal features and the subsequent accumulation of productivity and attraction of higher trophic level predators, such as P. glauca.     

Development and microstructure of tooth histotypes in the blue shark,Prionace glauca (Carcharhiniformes: Carcharhinidae) and the great white shark,Carcharodon carcharias (Lamniformes: Lamnidae)

Elasmobranchs exhibit two distinct arrangements of mineralized tissues in the teeth that are known as orthodont and osteodont histotypes. Traditionally, it has been said that orthodont teeth maintain a pulp cavity throughout tooth development whereas osteodont teeth are filled with osteodentine and lack a pulp cavity when fully developed. We used light microscopy, scanning electron microscopy, and high‐resolution micro‐computed tomography to compare the structure and development of elasmobranch teeth representing the two histotypes. As an example of the orthodont histotype, we studied teeth of the blue shark, Prionace glauca (Carcharhiniformes: Carcharhinidae). For the osteodont histotype, we studied teeth of the great white shark, Carcharodon carcharias (Lamniformes: Lamnidae). We document similarities and differences in tooth development and the microstructure of tissues in these two species and review the history of definitions and interpretations of elasmobranch tooth histotypes. We discuss a possible correlation between tooth histotype and tooth replacement and review the history of histotype differentiation in sharks. We find that contrary to a long held misconception, there is no orthodentine in the osteodont teeth of C. carcharias. J. Morphol. 276:797–817, 2015. © 2015 Wiley Periodicals, Inc.