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.     

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.     

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.     

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.     

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.     

Biological observations on the broadfin shark Lamiopsis temminckii (Carcharhiniformes: Carcharhinidae)

Biological information was collected from 214 individuals of the broadfin shark Lamiopsis temminckii measuring 418 to 1782 mm total length, L_T. Size at maturity (L₅₀) for females and males was estimated at 1430 and 1368 mm L_T, respectively, while mature and gravid females were observed from 1350 mm L_T with litter sizes 2–8 and size at birth 418–650 mm L_T. Analysis of stomach contents revealed a variety of prey, primarily crustaceans (54·0%), teleosts (42·7%) and cephalopods.     

Panbiogeographical analysis of the shark genus Rhizoprionodon (Chondrichthyes,Carcharhiniformes, Carcharhinidae)

The distributional patterns of the seven species of Rhizoprionodon were analysed using the panbiogeographical method of track analysis. The individual tracks of Rhizoprionodon suggest that the genus is mainly an Indian–Atlantic Ocean group. Five generalized tracks were found: (1) Caribbean, defined by R. porosus and R. terraenovae; (2) eastern coast of South America, defined by R. porosus and R. lalandei; (3) Indian Ocean, defined by R. acutus and R. oligolinx; (4) north‐western Australia, defined by R. acutus, R. oligolinx and R. taylori; (5) north‐north‐eastern Australia, defined by R. acutus and R. taylori. Only R. longurio was not included in any generalized track, and its distribution is restricted to the eastern Pacific Ocean. Two biogeographical nodes were found at the intersection of the generalized tracks 1 and 2 (Caribbean Sea) and generalized tracks 4 and 5 (north Australia). The generalized tracks overlap with those found in several unrelated marine taxa. Overall, the generalized tracks are associated with warm currents. The biogeographical nodes found (Caribbean and Australian) are coincident with the global distribution of mangroves.     

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.     

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.     

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.     

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.     

Marine biodiversity of Costa Rica, the microcrustacea: Copepoda (Crustacea: Maxillopoda)

This report is part of a series that summarizes the species and localities of Costa Rican marine taxa. A review of the literature on copepods, both pelagic and benthic for the Pacific and Caribbean coast of Costa Rica, includes eighty species. Sixty seven pelagic species have been found, distributed between sixteen calanoid, one cyclopoid, three harparticoid and four poecilostomatoid families. Moreover, thirteen benthonic species distributed into six families, all harparticoids, are reported. Among the pelagic families, Pontellidae has six species, while Paracalanidae and Eucalanidae had five each. Other families, like Calanidae, Pseudodiaptomidae and Acartiidae had four species and most families only one. Forty five species are reported only for the Pacific coast, thirteen for the Caribbean coast, only nine species occurred in both coasts; being a direct consequence of the more intensive research effort in the Pacific. Pelagic copepod biodiversity reflects different oceanographic conditions in both coasts. Typical estuarine species were found in the lower region of the Gulf of Nicoya, while a mixture of estuarine and oceanic species were found in Golfo Dulce. Diversity in the Caribbean, specially at the Cahuita coral reef is lower in comparison with the copepod diversity found in other regions in the Caribbean sea. This may be due to the high sediment resuspension rate characteristic of the Cahuita coral reef, which could affect the reproduction of many holozooplankters, specially copepods. Although sixty seven pelagic copepod species appears to be in low numbers, in terms of specific biodiversity it is as high when compared to numbers found in other tropical areas. Thirteen species are reported in the literature, all harparticoids. Five species, three sub-species and one genera were new to science. Balacopsylla is reported for the first time from a neotropical regions, while the genus Karllangia, represented by two coexisting species in the Caribbean coast, belong to a few circumtropical-subtropical genera. The most diverse family was Tetragonicipitidae. This is the first effort to summarize the available information about the biodiversity of marine copepods for Costa Rica's coasts.     

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.     

Diversity of the free-living marine and freshwater Copepoda (Crustacea) in Costa Rica: a review

The studies on marine copepods of Costa Rica started in the 1990’s and focused on the largest coastal-estuarine systems in the country, particularly along the Pacific coast. Diversity is widely variable among these systems: 40 species have been recorded in the Culebra Bay influenced by upwelling, northern Pacific coast, only 12 in the Gulf of Nicoya estuarine system, and 38 in Golfo Dulce, an anoxic basin in the southern Pacific coast of the country. Freshwater environments of Costa Rica are known to harbor a moderate diversity of continental copepods (25 species), which includes 6 calanoids, 17 cyclopoids and only two harpacticoids. Of the +100 freshwater species recorded in Central America, six are known only from Costa Rica, and one appears to be endemic to this country. The freshwater copepod fauna of Costa Rica is clearly the best known in Central America. Overall, six of the 10 orders of Copepoda are reported from Costa Rica. A previous summary by 2001 of the free-living copepod diversity in the country included 80 marine species (67 pelagic, 13 benthic). By 2009, the number of marine species increased to 209: 164 from the Pacific (49% of the copepod fauna from the Eastern Tropical Pacific) and 45 from the Caribbean coast (8% of species known from the Caribbean Basin). Both the Caribbean and Pacific species lists are growing. Additional collections of copepods at Cocos Island, an oceanic island 530 km away of the Pacific coast, have revealed many new records, including five new marine species from Costa Rica. Currently, the known diversity of marine copepods of Costa Rica is still in development and represents up to 52.6% of the total marine microcrustaceans recorded in the country. Future sampling and taxonomic efforts in the marine habitats should emphasize oceanic environments including deep waters but also littoral communities. Several Costa Rican records of freshwater copepods are likely to represent undescribed species. Also, the biogeographic relevance of the inland copepod fauna of Costa Rica requires more detailed surveys.     

The freshwater Copepoda (Crustacea) of Costa Rica with notes on some species

Sixteen species of Copepoda were recorded in this first detailed study of Costa Rican zooplankton. Two of these species are halophile. Notes are given on some of the species and their distribution. One new species found will be described elsewhere. The Costa Rican fauna resembles in composition the fauna of other Central American and Caribbean regions. Relatively few species were recorded. This is partly due to a low intensity of sampling but also to the paucity of lentic habitats. The occurrence of two circumtropical species of Mesocyclops is interesting.

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Résumé 16 espèces de Copépodes ont été inventoriées au cours d'une première étude détaillée du zooplankton dulcaquicole de Costa Rica. Deux des espèces trouvées sont halophiles. Des remarques sont faites a propos de quelques espèces et de leur répartition. Une nouvelle espèce est nouvelle — elle sera décrite par ailleurs. La fauna de Costa Rica ressemble par sa composition à celle des autres pays d'Amérique centrale et des îles caraibes. Relativement peu d'espèces sont notées. La faible intensité de l'échantillonnage mais aussi la pauvreté en habitats limniques en sont responsables. La présence de deux espèces circumtropicales de Mesocyclops est intéressante.

     

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.     

On the role of dense aggregations of males and juveniles in the functional structure of the range of the blue shark Prionace glauca

Analysis of the quantitative distribution and size composition indicated a high extent of the differentiation of the range of the blue shark Prionace glauca. This most abundant and widely distributed species in the oceanic epipelagial of the entire World Ocean remains for the first years of its life in coastal and neritic waters at depths of 80 m. At the earliest age, at a length under 70 cm, sexes separate into individual schools; females stay nearer to the coast. In the eastern Atlantic, two regions of juvenile habitats are recorded: to the north and to the south of the equator, with a typical gap between them in tropical waters. On reaching a length of 160–190 cm, sharks leave for oceanic waters; immature females follow dense aggregations of adult males situated in oceanic waters where their first mating takes place with a delayed fertilization until reaching sexual maturity. A similar pattern of distribution is traced in the eastern Pacific and other regions of the World Ocean. Under conditions of an increased demand and high prices of shark fins, such aggregations of juveniles and adult males where density exceeds average values dozens of times, can easily lead to overfishing and endanger the species existence and the stability of the structure of the oceanic biota as a whole. The necessity of introducing international protection measures with respect to such aggregations is substantiated.     

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.