The Effects of Hypoxia on Three Sympatric Shark Species: Physiological and Behavioral Responses

Behavioral and physiological responses to hypoxia were examined in three sympatric species of sharks: bonnethead shark Sphyrna tiburo, blacknose shark, Carcharhinus acronotus, and Florida smoothhound shark, Mustelus norrisi, using closed system respirometry. Sharks were exposed to normoxic and three levels of hypoxic conditions. Under normoxic conditions (5.5–6.4mg l^–1), shark routine swimming speed averaged 25.5 and 31.0cm s^–1 for obligate ram-ventilating S. tiburo and C. acronotus respectively, and 25.0cm s^–1 for buccal-ventilating M. norrisi. Routine oxygen consumption averaged about 234.6 mg O₂kg^–1h^–1 for S. tiburo, 437.2mg O₂kg^–1h^–1 for C. acronotus, and 161.4mg O₂ kg^–1 h^–1 for M. norrisi. For ram-ventilating sharks, mouth gape averaged 1.0cm whereas M. norrisi gillbeats averaged 56.0 beats min^–1. Swimming speeds, mouth gape, and oxygen consumption rate of S. tiburo and C. acronotus increased to a maximum of 37–39cm s^–1, 2.5–3.0cm and 496 and 599mg O₂ kg^–1 h^–1 under hypoxic conditions (2.5–3.4mg l^–1), respectively. M. norrisi decreased swimming speeds to 16cm s^–1 and oxygen consumption rate remained similar. Results support the hypothesis that obligate ram-ventilating sharks respond to hypoxia by increasing swimming speed and mouth gape while buccal-ventilating smoothhound sharks reduce activity.     

Vertebral size-at-age heterogeneity in gummy shark harvested off southern Australia

Stochastic parametrization of growth heterogeneity was applied to investigate the distribution of vertebral band radius-at-age in three populations of gummy shark Mustelus antarcticus Günther harvested with very different fishing effort and different mesh-sizes of gillnet. Three examples of four parameter growth models were developed where the random von Bertalanffy growth rate K is represented alternatively by three positive distributions to avoid negative tails in size-at-age distribution. Models with gamma and log-normal distributions of K fitted the data equally well and both fitted better than a model with the Weibull distribution. Various results are presented from the model developed with the gamma distribution of K. Heterogeneity in vertebral growth is presented as a series of quantiles of distribution of band radius-at-age. Probability density functions of band radius are presented for sharks at four selected ages, and cross-sections of these probability densities against age are presented for three selected values of band radius. Heterogeneity of growth rate K in a population is presented as tables of 10% quantiles and as graphs of probability densities. The differences in the patterns of vertebral growth for male and female sharks separately, between Bass Strait during 1973–1976, Bass Strait during 1986–1987 and South Australia during 1986–1987 are generally consistent with those determined from shark length-at-age in other published studies. However, the stochastic modelling approach adopted in the present study avoids having to make any assumptions about vertebral growth patterns of individual sharks and embraces heterogeneity in vertebral radius-at-age in the models which allows for better evaluation of alternative hypotheses for explaining the observed differences in growth patterns.     

Species identification and comparative population genetics of four coastal houndsharks based on novel NGS‐mined microsatellites

The common smooth‐hound (Mustelus mustelus ) is the topmost bio‐economically and recreationally important shark species in southern Africa, western Africa, and Mediterranean Sea. Here, we used the Illumina HiSeq? 2000 next‐generation sequencing (NGS ) technology to develop novel microsatellite markers for Mustelus mustelus . Two microsatellite multiplex panels were constructed from 11 polymorphic loci and characterized in two populations of Mustelus mustelus representative of its South African distribution. The markers were then tested for cross‐species utility in Galeorhinus galeus , Mustelus palumbes , and Triakis megalopterus , three other demersal coastal sharks also subjected to recreational and/or commercial fishery pressures in South Africa. We assessed genetic diversity (N _A, A _R, H _O, H _E, and PIC) and differentiation (F _ST and D _est) for each species and also examined the potential use of these markers in species assignment. In each of the four species, all 11 microsatellites were variable with up to a mean N _A of 8, A _R up to 7.5, H _E and PIC as high as 0.842. We were able to reject genetic homogeneity for all species investigated here except for T . megalopterus . We found that the panel of the microsatellite markers developed in this study could discriminate between the study species, particularly for those that are morphologically very similar. Our study provides molecular tools to address ecological and evolutionary questions vital to the conservation and management of these locally and globally exploited shark species.     

The survey of ectoparasites on two species of Triakids (Mustelus mustelus and M. punctulatus) sharks from Tunisian coasts

Between 2018 and 2020, 696 fish belonging to two species of sharks from the Family Triakidae (Mustelus mustelus and M. punctulatus) were collected from the coasts of Tunisia and inspected for parasites. Six copepod taxa (Perissopus dentatus Steenstrup & Lütken, 1861, Eudactylinella alba Wilson, 1932, Kroyeria lineata Van Beneden, 1853, Nesippus orientalis Heller, 1865 and Lernaeopoda galei Krøyer, 1837, Kroyeria sp.), four isopod species (Anilocra physodes (Linnaeus, 1758), Emetha audouini (H. Milne Edwards, 1840), Ceratothoa parallela (Otto, 1828) and Ceratothoa oestroides (Risso, 1816)) and two monogenean species (Erpocotyle sp1. And Erpocotyle sp2) were collected. A large number of global host records was reported, including the occurrence of E. audouini on M. mustelus and of Erpocotyle sp.2 on M. punctulatus. The study of the diversity of parasites per host species revealed that M. mustelus had a higher parasitic richness compared to M. punctulatus. In this study, it was provided for the first records on ectoparasites on Triakidae sharks from Tunisian coasts and their infection indices.     

Immunocytochemical localization of S-100 protein in the hypophysis and saccus vasculosus of the elasmobranchs Mustelus manazo and Scyliorhinus torazame

Summary S-100 protein-immunoreactive cells were demonstrated by immunocytochemical procedures in the hypophysis and saccus vasculosus of two species of elasmobranchs (Mustelus manazo and Scyliorhinus torazame). In the saccus vasculosus of M. manazo, immunoreactivity was detectable exclusively in the fibrous portions interposed between the epithelial layer and the blood vessels. In the neurohypophysis, tanycytes and astrocytes of the median eminence were immunostained, but only a few labeled cells were found in the neurointermediate lobe. In S. torazame, the neurohypophysis displayed a similar distribution of immunoreactivity, but there were no labeled cells in the saccus vasculosus. In both species, none of the glandular cells of the hypophysis displayed immunoreactivity. Electron-microscopic examination showed that the immunostained cells in the saccus vasculosus correspond to astrocytes.     

Microscopic organization of the sperm storage tubules in the oviducal gland of the female gummy shark (Mustelus antarcticus), with observations on sperm distribution and storage

Oviducal gland morphology, the microscopic organization of the terminal zone, and sperm storage were described in the female gummy shark (Mustelus antarcticus). Mustelus antarcticus is a nonplacental viviparous hound shark, which displays minimal histotrophy during embryonic development. The animals examined represented all stages of maturity and gestation. The oviducal gland was found to have the same fundamental zonation as in most chondrichthyans. Using recent terminology, the oviducal gland of chondrichthyans has an anterior club zone, followed by a papillary zone, both of which produce jelly that surrounds the egg, a baffle zone that elaborates the tertiary egg envelope and a terminal zone, where sperm storage occurs. Each zone is composed of simple tubular glands that connect to transverse grooves, which extend the full width of the gland. The exception is the terminal zone, which does not have transverse grooves but consists of individual tubules. The microscopic organization and histochemical nature of the zones display similar patterns to those of other chondrichthyan genera. Tubules of the terminal zone contain four types of cell: ciliated cells, alcian blue‐positive secretory cells, periodic acid‐Schiff and alcian blue‐negative secretory cells, and secretory columnar cells. These tubules end in recesses, the sperm storage tubules, which extend beyond the periphery of the baffle zone. Sperm were stored in the sperm storage tubules of all maturing and mature animals examined. Of note is the observation of stored sperm in an animal 1 year prior to first ovulation. Sperm were also observed throughout the uterine sphincter, body of the uterus, isthmus, and oviduct of maturing and mature animals, and in the uterine sphincter of an immature animal. These sperm represent immediately postcopulation aggregations of sperm and sperm in the process of migrating to the site of storage or to the site of fertilization. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Reproductive biology of the brown smoothhound shark Mustelus henlei,in the northern Gulf of California,México

Female brown smoothhound sharks Mustelus henlei were found to reproduce annually. A mature female carried both developing oocytes in the ovary and developing embryos in the uteri concurrently for c. 1 year. A great variability in the size of embryos was recorded each month, and the maximum embryo sizes were found from late January to mid‐March. The largest oocytes in mature females were observed in mid‐March. Gestation lasted c. 10 months. A linear relationship between maternal total length (L_T) and the number of pups per litter (litter size one to 21) was estimated. Birth L_T was reached in c. 280 mm. Females and males matured at 570–660 and 550–560 mm L_T, respectively. Difference in the litter size among Californian coast (one to 10) and northern Gulf of California (one to 21) populations existed for this smoothhound shark.     

Reproductive biology of the smooth-hound shark Mustelus mustelus (L.) in the Gulf of Gabès (south-central Mediterranean Sea)

The reproductive biology of the smooth-hound shark Mustelus mustelus was studied in the Gulf of Gabès (southern Tunisia). Females were found to mature between 1075 and 1230 mm total length ( L _T) whereas males matured between 880 and 1120 mm L _T. The L _T at which 50% of the population reached maturity was 971 and 1172 mm for males and females, respectively. Male gonads were symmetrical in terms of mass and both functional, whereas in females only the right ovary was functional. The seasonal changes in the oocytes and testes development, embryo length and the occurrence of near-term and post-partum females showed that this species displayed a clearly defined annual reproductive cycle with parturition occurring during late April and early May, after a gestation period of 10–11 months. Mating took place during May and early June and fertilization occurred from early June to early July. The embryo sex ratio was not significantly different from unity. Litter size varied from four to 18 embryos and was positively correlated with maternal L _T. The young were born with a L _T of 340–420 mm.     

Granulated peripolar epithelial cells in the renal corpuscle of marine elasmobranch fish

Summary Granulated epithelial cells at the vascular pole of the renal corpuscle, peripolar cells, have been found in the kidneys of five species of elasmobranchs, the little skate (Raja erinaced), the smooth dogfish shark (Mustelus canis), the Atlantic sharpnose shark (Rhizoprionodon terraenovae), the scalloped hammerhead shark (Sphryna lewini), and the cow-nosed ray (Rhinoptera bonasus). In a sixth elasmobranch, the spiny dogfish shark (Squalus acanthias), the peripolar cells could not be identified among numerous other granulated epithelial cells. The peripolar cells are located at the transition between the parietal epithelium of Bowman's capsule and the visceral epithelium (podocytes) of the glomerulus, thus forming a cuff-like arrangement surrounding the hilar vessels of the renal corpuscle. These cells may have granules and/or vacuoles. Electron microscopy shows that the granules are membrane-bounded, and contain either a homogeneous material or a paracrystalline structure with a repeating period of about 18 nm. The vacuoles are electron lucent or may contain remnants of a granule. These epithelial cells lie close to the granulated cells of the glomerular afferent arteriole. They correspond to the granular peripolar cells of the mammalian, avian and amphibian kidney. The present study is the first reported occurrence of peripolar cells in a marine organism or in either bony or cartilagenous fish.     

Odor tracking in sharks is reduced under future ocean acidification conditions

Recent studies show that ocean acidification impairs sensory functions and alters the behavior of teleost fishes. If sharks and other elasmobranchs are similarly affected, this could have significant consequences for marine ecosystems globally. Here, we show that projected future CO₂ levels impair odor tracking behavior of the smooth dogfish (Mustelus canis). Adult M. canis were held for 5 days in a current‐day control (405 ± 26 μatm) and mid (741 ± 22 μatm) or high CO₂ (1064 ± 17 μatm) treatments consistent with the projections for the year 2100 on a ‘business as usual’ scenario. Both control and mid CO₂‐treated individuals maintained normal odor tracking behavior, whereas high CO₂‐treated sharks significantly avoided the odor cues indicative of food. Control sharks spent >60% of their time in the water stream containing the food stimulus, but this value fell below 15% in high CO₂‐treated sharks. In addition, sharks treated under mid and high CO₂ conditions reduced attack behavior compared to the control individuals. Our findings show that shark feeding could be affected by changes in seawater chemistry projected for the end of this century. Understanding the effects of ocean acidification on critical behaviors, such as prey tracking in large predators, can help determine the potential impacts of future ocean acidification on ecosystem function.