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1.
Article in English | MEDLINE | ID: mdl-32717287

ABSTRACT

Marine elasmobranchs are nitrogen-limited owing to the requirement of nitrogen for both somatic growth and urea-based osmoregulation, and due to the loss of urea across the gills and kidney as nitrogenous waste. In this study we used in vitro stomach and intestinal gut sacs to investigate the effects of consuming a urea-rich meal (700 mM within a 2% body-mass ration of food-slurry) on nitrogen movement across the gastrointestinal (GI) tract of North Pacific spiny dogfish (Squalus acanthias suckleyi). Plasma urea concentrations did not differ between fasted (359 ± 19 mM), urea-poor fed (340 ± 16 mM), and urea-rich fed (332 ± 24 mM) dogfish. Interestingly, in vitro gut sacs of urea-rich fed dogfish showed no net urea absorption from the lumen over 3 h incubation, which contrasts previously published data on urea-poor fed dogfish that absorb urea from the lumen. In addition, ammonium (NH4+) concentration within the gut sac intestinal lumen significantly increased from 0.62 to 4.35 mM over 3 h. This is likely due to a combination of tissue production and microbial urease activity in the intestine. The overall results highlight the ability of S. a. suckleyi to regulate and maintain internal nitrogen concentrations despite the addition of excess dietary urea.


Subject(s)
Animal Feed , Homeostasis , Squalus acanthias/physiology , Urea/metabolism , Ammonia/metabolism , Animals , Chlorides/metabolism , Gastrointestinal Tract/metabolism , Gills/physiology , Intestines/physiology , Male , Nitrogen/metabolism , Osmoregulation , Stomach/physiology , Urease/metabolism , Water-Electrolyte Balance/physiology
2.
Sci Rep ; 9(1): 14317, 2019 10 04.
Article in English | MEDLINE | ID: mdl-31586144

ABSTRACT

Pivotal life history traits concerning age structure and reproduction of the spiny dogfish (Squalus acanthias, Linnaeus 1758) were investigated in the Adriatic Sea from mid February 2012 to mid July 2013 and in 2016. The whole sample consisted of 176 females and 150 males, ranging between 217-1025 mm and 219-875 mm, respectively. The individual age, which was estimated using a cross-sectioning technique of the second dorsal-fin spine, ranged from 0 to 13+ years for females and from 0 to 9+ years for males. Based on the length-at-age estimates, the Gompertz growth parameters were L∞ = 1130 mm, k = 0.18 and L∞ = 920 mm, k = 0.24 for females and males, respectively. The size at sexual maturity (L50) was 659 mm for females and 575 mm for males, corresponding to 7.5 and 5.5 years of age (A50), respectively. Mean biennial fecundity was approximately 11 embryos/female and 12 ripe oocytes/female. Mature males occurred during much of the sampling period, while mature females with nearly full-term embryos were exclusively recorded in May 2013 and July 2016. Monitoring of catches conducted in a sample port of the north Adriatic (Chioggia) over the past 20 years has shown fluctuating trends in landings, with peaks during the summer reproductive season.


Subject(s)
Life History Traits , Spine/anatomy & histology , Squalus acanthias/physiology , Anatomy, Cross-Sectional , Animals , Body Size , Female , Male , Reproduction , Seasons , Sexual Maturation , Squalus acanthias/anatomy & histology
3.
Anat Rec (Hoboken) ; 302(5): 837-844, 2019 05.
Article in English | MEDLINE | ID: mdl-30312010

ABSTRACT

Vertebrates utilize six extraocular muscles that attach to a tough, protective sclera to rotate the eye. The goal of the study was to describe the maximum tetanic forces, as well as the torques produced by the six extraocular muscles of the piked dogfish Squalus acanthias to understand the forces exerted on the eye. The lateral rectus extraocular muscle of Squalus acanthias was determined to be parallel fibered with the muscle fibers bundled into discrete fascicles. The extraocular muscles attach to the sclera by muscular insertions. The total tensile forces generated by the extraocular muscles ranged from 1.18 N to 2.21 N. The torques of the extraocular muscles ranged from 0.39 N to 2.34 N. The torques were greatest in the principal direction of movement for each specific muscle. The lateral rectus produced the greatest total tensile force, as well as the greatest torque force component, while the medial rectus produced the second greatest. This is likely due to the constant rotational movement of the eye anteriorly and posteriorly to stabilize the visual image, as well as increase the effective visual field during swimming. Rotational forces in dimensions other than the primary direction of movement may contribute to motion in directions other than the principal direction during multi-muscle contraction that occurs in the vertebrate eye. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:837-844, 2019. © 2018 Wiley Periodicals, Inc.


Subject(s)
Eye Movements/physiology , Models, Biological , Muscle Contraction/physiology , Oculomotor Muscles/physiology , Squalus acanthias/physiology , Animals , Muscle Fibers, Skeletal/physiology , Oculomotor Muscles/anatomy & histology , Vision, Ocular/physiology
4.
J Exp Biol ; 220(Pt 21): 3967-3975, 2017 11 01.
Article in English | MEDLINE | ID: mdl-28883085

ABSTRACT

A key feature of fish functional design is the presence of multiple fins that allow thrust vectoring and redirection of fluid momentum to contribute to both steady swimming and maneuvering. A number of previous studies have analyzed the function of dorsal fins in teleost fishes in this context, but the hydrodynamic function of dorsal fins in freely swimming sharks has not been analyzed, despite the potential for differential functional roles between the anterior and posterior dorsal fins. Previous anatomical research has suggested a primarily stabilizing role for shark dorsal fins. We evaluated the generality of this hypothesis by using time-resolved particle image velocimetry to record water flow patterns in the wake of both the anterior and posterior dorsal fins in two species of freely swimming sharks: bamboo sharks (Chiloscyllium plagiosum) and spiny dogfish (Squalus acanthias). Cross-correlation analysis of consecutive images was used to calculate stroke-averaged mean longitudinal and lateral velocity components, and vorticity. In spiny dogfish, we observed a velocity deficit in the wake of the first dorsal fin and flow acceleration behind the second dorsal fin, indicating that the first dorsal fin experiences net drag while the second dorsal fin can aid in propulsion. In contrast, the wake of both dorsal fins in bamboo sharks displayed increased net flow velocity in the majority of trials, reflecting a thrust contribution to steady swimming. In bamboo sharks, fluid flow in the wake of the second dorsal fin had higher absolute average velocity than that for first dorsal fin, and this may result from a positive vortex interaction between the first and second dorsal fins. These data suggest that the first dorsal fin in spiny dogfish has primarily a stabilizing function, while the second dorsal fin has a propulsive function. In bamboo sharks, both dorsal fins can contribute thrust and should be considered as propulsive adjuncts to the body during steady swimming. The function of shark dorsal fins can thus differ considerably among fins and species, and is not limited to a stabilizing role.


Subject(s)
Animal Fins/physiology , Sharks/physiology , Swimming , Animals , Female , Hydrodynamics , Male , Squalus acanthias/physiology
5.
J Morphol ; 278(8): 1075-1090, 2017 08.
Article in English | MEDLINE | ID: mdl-28470783

ABSTRACT

Musculo-skeletal morphology is an indispensable source for understanding functional adaptations. Analysis of morphology of the branchial apparatus of Hexanchiform sharks can provide insight into aspects of their respiration that are difficult to observe directly. In this study, I compare the structure of the musculo-skeletal system of the gill apparatus of Heptranchias perlo and Squalus acanthias in respect to their adaptation for one of two respiratory mechanisms known in sharks, namely, the active two-pump (oropharyngeal and parabranchial) ventilation and the ram-jet ventilation. In both species, the oropharyngeal pump possesses two sets of muscles, one for compression and the other for expansion. The parabranchial pump only has constrictors. Expansion of this pump occurs only due to passive elastic recoil of the extrabranchial cartilages. In Squalus acanthias the parabranchial chambers are large and equipped by powerful superficial constrictors. These muscles and the outer walls of the parabranchial chambers are much reduced in Heptranchias perlo, and thus it likely cannot use this pump. However, this reduction allows for vertical elongation of outer gill slits which, along with greater number of gill pouches, likely decreases branchial resistance and, at the same time, increases the gill surface area, and can be regarded as an adaptation for ram ventilation at lower speeds.


Subject(s)
Gills/anatomy & histology , Musculoskeletal System/anatomy & histology , Sharks/anatomy & histology , Sharks/physiology , Animals , Bone and Bones/anatomy & histology , Head/anatomy & histology , Muscles/anatomy & histology , Squalus acanthias/anatomy & histology , Squalus acanthias/physiology
6.
J Fish Biol ; 88(5): 1758-75, 2016 May.
Article in English | MEDLINE | ID: mdl-27020803

ABSTRACT

The objective of this study was to estimate reproductive and population parameters of the spiny dogfish Squalus acanthias for the south-western Atlantic Ocean. In total, 2714 specimens (1616 males and 1098 females) were collected from surveys carried out using research vessels. Males ranged from 225 to 861 mm total length (LT ) and females from 235 to 925 mm LT . The size at maturity of females (651 mm) was significantly greater than that of males (565 mm). The maximum proportion of mature individuals (Pmax ) of the gestation ogive was <1, which indicates that a proportion of mature females was not in gestation. This inactivity may be explained by the occurrence of resting periods between cycles or by the asynchrony of the reproductive cycle. The estimated Pmax for the maternity ogive suggested that about one third of mature females were in the maternity stage (i.e. with embryos >156 mm). The temporal and spatial co-occurrence of non-gravid adult females at different stages of ovarian development, as well as gravid females at all embryonic development stages would indicate that the female reproductive cycle in the south-western Atlantic Ocean is asynchronous. The results indicate that S. acanthias is susceptible to fishing pressure on account of its length at maturity, extended reproductive cycles and low fecundity.


Subject(s)
Reproduction , Squalus acanthias/physiology , Animals , Atlantic Ocean , Female , Fertility , Male , Population Density , Sex Characteristics , Sexual Maturation , Squalus acanthias/anatomy & histology
7.
J Comp Physiol B ; 185(5): 511-25, 2015 Jul.
Article in English | MEDLINE | ID: mdl-25794843

ABSTRACT

Although they are ureotelic, marine elasmobranchs express Rh glycoproteins, putative ammonia channels. To address questions raised by a recent study on high environmental ammonia (HEA) exposure, dogfish were intravascularly infused for 24 h at 3 ml kg(-1) h(-1) with isosmotic NaCl (500 mmol l(-1), control), NH4HCO3 (500 mmol l(-1)), NH4Cl (500 mmol l(-1)), or HCl (as 125 mmol l(-1) HCl + 375 mmol l(-1) NaCl). While NaCl had no effect on arterial acid-base status, NH4HCO3 caused mild alkalosis, NH4Cl caused strong acidosis, and HCl caused lesser acidosis, all predominantly metabolic in nature. Total plasma ammonia (T(Amm)) and excretion rates of ammonia (J(Amm)) and urea-N (J(Urea-N)) were unaffected by NaCl or HCl. However, despite equal loading rates, plasma T(Amm) increased to a greater extent with NH4Cl, while J(Amm) increased to a greater extent with NH4HCO3 due to much greater increases in blood-to-water PNH3 gradients. As with HEA, both treatments caused large (90%) elevations of J(Urea-N), indicating that urea-N synthesis by the ornithine-urea cycle (OUC) is driven primarily by ammonia rather than HCO3(-). Branchial mRNA expressions of Rhbg and Rhp2 were unaffected by NH4HCO3 or NH4Cl, but v-type H(+)-ATPase was down-regulated by both treatments, and Rhbg and Na(+)/H(+) exchanger NHE2 were up-regulated by HCl. In the kidney, Rhbg was unresponsive to all treatments, but Rhp2 was up-regulated by HCl, and the urea transporter UT was up-regulated by HCl and NH4Cl. These responses are discussed in the context of current ideas about branchial, renal, and OUC function in this nitrogen-limited predator.


Subject(s)
Acid-Base Equilibrium/drug effects , Ammonium Chloride/adverse effects , Bicarbonates/adverse effects , Gene Expression Regulation/drug effects , Nitrogen/metabolism , Squalus acanthias/physiology , Acid-Base Equilibrium/physiology , Ammonia/blood , Ammonium Chloride/administration & dosage , Analysis of Variance , Animals , Bicarbonates/administration & dosage , DNA Primers/genetics , Hydrochloric Acid , Membrane Glycoproteins/metabolism , Polymerase Chain Reaction , Sodium Chloride , Spectrophotometry, Atomic , Squalus acanthias/metabolism , Urea/metabolism
8.
Physiol Biochem Zool ; 87(5): 623-39, 2014.
Article in English | MEDLINE | ID: mdl-25244375

ABSTRACT

The effects of acute moderate (20% air O2 saturation; 6-h exposure) and severe (5% air O2 saturation; 4-h exposure) hypoxia on N-waste, acid-base, and ion balance in dogfish sharks (Squalus acanthias suckleyi) were evaluated. We predicted that the synthesis and/or retention of urea, which are active processes, would be inhibited by hypoxia. Exposure to moderate hypoxia had negligible effects on N-waste fluxes or systemic physiology, except for a modest rise in plasma lactate. Exposure to severe hypoxia led to a significant increase in urea excretion (Jurea), while plasma, liver, and muscle urea concentrations were unchanged, suggesting a loss of urea retention. Ammonia excretion (Jamm) was elevated during normoxic recovery. Moreover, severe hypoxia led to disruptions in acid-base balance, indicated by a large increase in plasma [lactate] and substantial decreases in arterial pHa and plasma [Formula: see text], as well as loss of ionic homeostasis, indicated by increases in plasma [Mg(2+)], [Ca(2+)], and [Na(+)]. We suggest that severe hypoxia in dogfish sharks leads to a reduction in active gill homeostatic processes, such as urea retention, acid-base regulation and ionoregulation, and/or an osmoregulatory compromise due to increased functional gill surface area. Overall, the results provide a comprehensive picture of the physiological responses to a severe degree of hypoxia in an ancient fish species.


Subject(s)
Oxygen/metabolism , Squalus acanthias/physiology , Urea/metabolism , Water-Electrolyte Balance , Anaerobiosis , Animals , Hydrogen-Ion Concentration , Male , Squalus
9.
Physiol Biochem Zool ; 87(5): 652-62, 2014.
Article in English | MEDLINE | ID: mdl-25244377

ABSTRACT

Chemical and molecular chaperones are organic compounds that protect and stabilize proteins from damage and aggregation as a result of cellular stress. Using the dogfish (Squalus acanthias) red blood cell (RBC) as a model, we examined whether elasmobranch cells with naturally high concentrations of the chemical chaperone trimethylamine oxide (TMAO) would induce the molecular chaperone heat shock protein 70 (HSP70) when exposed to an acute thermal stress. Our hypothesis was that TMAO is itself capable of preventing damage and preserving cellular function during thermal stress and thus that the heat shock response would be inhibited/diminished. We incubated RBCs in vitro with and without physiologically relevant concentrations of TMAO at 13°C and then exposed cells to a 1-h acute heat shock at 24°C. HSP70 protein expression was elevated in dogfish RBCs after the acute heat stress, but this induction was inhibited by extracellular TMAO. Regardless of the presence of TMAO and/or HSP70, we did not observe any cell damage, as indicated by changes in caspase 3/7 activity, protein carbonyls, membrane viability, or levels of ubiquitin. We also saw no change in RBC cell function, as determined by hemoglobin oxygen affinity or carrying capacity, in cells lacking the heat shock response but protected by TMAO. This study demonstrates that there is cellular coordination between chemical and molecular chaperones in response to an acute thermal stress in dogfish RBCs and suggests that TMAO has a thermoprotective role in these cells, thus eliminating the need for a heat shock response.


Subject(s)
Erythrocytes/metabolism , HSP70 Heat-Shock Proteins/genetics , Heat-Shock Response , Methylamines/metabolism , Squalus acanthias/physiology , Animals , Female , HSP70 Heat-Shock Proteins/metabolism , Male , Squalus acanthias/genetics
10.
PLoS One ; 9(7): e103384, 2014.
Article in English | MEDLINE | ID: mdl-25068584

ABSTRACT

Spiny dogfish (Squalus acanthias) are assumed to be a highly migratory species, making habitual north-south migrations throughout their northwestern Atlantic United States (U.S.) range. Also assumed to be a benthic species, spiny dogfish stock structure is estimated through Northeast Fisheries Science Center (NEFSC) bottom-trawl surveys. Recent anomalies in population trends, including a recent four-fold increase in estimated spawning stock biomass, suggest alternative movement patterns could exist for this shark species. To obtain a better understanding of the horizontal and vertical movement dynamics of this species, Microwave Telemetry pop-up satellite archival X-Tags were attached to forty adult spiny dogfish at the northern (Gulf of Maine) and southern (North Carolina) extents of their core U.S. geographic range. Reconstructed geolocation tracks ranging in lengths from two to 12 months suggest that the seasonal migration patterns appear to be local in nature to each respective northern and southern deployment site, differing from previously published migration paradigms. Differences in distance and direction traveled between seasonal geolocations possibly indicate separate migratory patterns between groups. Kernel utilization distribution models also suggest strong separate core home ranges. Significant differences in seasonal temperature and depths between the two regions further substantiate the possibility of separate regional movement patterns between the two groups. Vertical utilization also suggests distinct diel patterns and that this species may not utilize the benthos as previously thought, potentially decreasing availability to benthic gear.


Subject(s)
Animal Identification Systems/methods , Fisheries/methods , Satellite Communications , Squalus acanthias/physiology , Swimming/physiology , Animal Identification Systems/instrumentation , Animal Migration/physiology , Animals , Atlantic Ocean , Female , Geography , Homing Behavior/physiology , Maine , Male , Massachusetts , Models, Biological , Movement/physiology , North Carolina , Seasons , Temperature , Time Factors , Virginia
11.
J Morphol ; 274(11): 1288-98, 2013 Nov.
Article in English | MEDLINE | ID: mdl-23907951

ABSTRACT

Stability and procured instability characterize two opposing types of swimming, steady and maneuvering, respectively. Fins can be used to manipulate flow to adjust stability during swimming maneuvers either actively using muscle control or passively by structural control. The function of the dorsal fins during turning maneuvering in two shark species with different swimming modes is investigated here using musculoskeletal anatomy and muscle function. White-spotted bamboo sharks are a benthic species that inhabits complex reef habitats and thus have high requirements for maneuverability. Spiny dogfish occupy a variety of coastal and continental shelf habitats and spend relatively more time cruising in open water. These species differ in dorsal fin morphology and fin position along the body. Bamboo sharks have a larger second dorsal fin area and proportionally more muscle insertion into both dorsal fins. The basal and radial pterygiophores are plate-like structures in spiny dogfish and are nearly indistinguishable from one another. In contrast, bamboo sharks lack basal pterygiophores, while the radial pterygiophores form two rows of elongated rectangular elements that articulate with one another. The dorsal fin muscles are composed of a large muscle mass that extends over the ceratotrichia overlying the radials in spiny dogfish. However, in bamboo sharks, the muscle mass is divided into multiple distinct muscles that insert onto the ceratotrichia. During turning maneuvers, the dorsal fin muscles are active in both species with no differences in onset between fin sides. Spiny dogfish have longer burst durations on the outer fin side, which is consistent with opposing resistance to the medium. In bamboo sharks, bilateral activation of the dorsal in muscles could also be stiffening the fin throughout the turn. Thus, dogfish sharks passively stiffen the dorsal fin structurally and functionally, while bamboo sharks have more flexible dorsal fins, which result from a steady swimming trade off.


Subject(s)
Animal Fins/anatomy & histology , Muscle, Skeletal/anatomy & histology , Sharks/anatomy & histology , Squalus acanthias/anatomy & histology , Animal Fins/physiology , Animals , Biomechanical Phenomena , Muscle Contraction , Muscle, Skeletal/physiology , Sharks/physiology , Squalus acanthias/physiology , Swimming/physiology
12.
J Fish Biol ; 80(5): 2089-111, 2012 Apr.
Article in English | MEDLINE | ID: mdl-22497417

ABSTRACT

Two of the most commonly used elasmobranch experimental model species are the spiny dogfish Squalus acanthias and the little skate Leucoraja erinacea. Comparative biology and genomics with these species have provided useful information in physiology, pharmacology, toxicology, immunology, evolutionary developmental biology and genetics. A wealth of information has been obtained using in vitro approaches to study isolated cells and tissues from these organisms under circumstances in which the extracellular environment can be controlled. In addition to classical work with primary cell cultures, continuously proliferating cell lines have been derived recently, representing the first cell lines from cartilaginous fishes. These lines have proved to be valuable tools with which to explore functional genomic and biological questions and to test hypotheses at the molecular level. In genomic experiments, complementary (c)DNA libraries have been constructed, and c. 8000 unique transcripts identified, with over 3000 representing previously unknown gene sequences. A sub-set of messenger (m)RNAs has been detected for which the 3' untranslated regions show elements that are remarkably well conserved evolutionarily, representing novel, potentially regulatory gene sequences. The cell culture systems provide physiologically valid tools to study functional roles of these sequences and other aspects of elasmobranch molecular cell biology and physiology. Information derived from the use of in vitro cell cultures is valuable in revealing gene diversity and information for genomic sequence assembly, as well as for identification of new genes and molecular markers, construction of gene-array probes and acquisition of full-length cDNA sequences.


Subject(s)
Cell Line , Primary Cell Culture , Skates, Fish/genetics , Squalus acanthias/genetics , Animals , Cells, Cultured , Conserved Sequence , Gene Library , Genomics , Molecular Biology , RNA, Messenger/genetics , Skates, Fish/physiology , Squalus acanthias/physiology , Transcriptome
13.
Cell Tissue Res ; 349(3): 703-15, 2012 Sep.
Article in English | MEDLINE | ID: mdl-22314845

ABSTRACT

A common observation in the vertebrate testis is that new germ cell clones enter spermatogenesis proper before previously formed clones have completed their development. The extent to which the developmental advance of any given germ cell clone in any phase of spermatogenesis is dependent on that of neighboring clones and/or on the coordinating influence of associated Sertoli cells in the immediate vicinity or of others further away remains unclear. This review presents an overall synthesis of findings in an ancient vertebrate, the spiny dogfish shark and shows that, even at this phyletic level, the developmental advance of a given germ cell clone is the outcome of various processes emanating from its spatiotemporal relationship with (1) its own complement of Sertoli cells in the anatomically distinct spermatocyst and (2) Sertoli cells associated with other germ cell clones that lie upstream or downstream in the spermatogenic progression and that secrete, among others, androgen and estrogen destined for target sites upstream. Analysis of the protracted spermatogenic cycle shows the coordination in space and time of spermatogenic and steroidogenic events. Furthermore, the natural withdrawal of pituitary gonadotropin support in the dogfish causes a distinct and highly ordered gradient of apoptosis among the spermatogonial generations; this in turn is a major contributing factor to the cyclic nature of sperm production observed in this lower vertebrate. Because of the simplicity of their testicular organization, their cystic spermatogenesis and their phylogenetic position, cartilaginous fishes constitute a valid vertebrate reference system for comparative analysis with higher vertebrates.


Subject(s)
Spermatogenesis/physiology , Squalus acanthias/physiology , Testis/cytology , Animals , Germ Cells/cytology , Male , Sertoli Cells/cytology
14.
J Fish Biol ; 79(7): 2060-6, 2011 Dec.
Article in English | MEDLINE | ID: mdl-22141905

ABSTRACT

Three lipid correction models were evaluated for liver and white dorsal muscle from Squalus acanthias. For muscle, all three models performed well, based on the Akaike Information Criterion value corrected for small sample sizes (AIC(c) ), and predicted similar lipid corrections to δ(13) C that were up to 2.8 ‰ higher than those predicted using previously published models based on multispecies data. For liver, which possessed higher bulk C:N values compared to that of white muscle, all three models performed poorly and lipid-corrected δ(13) C values were best approximated by simply adding 5.74 ‰ to bulk δ(13) C values.


Subject(s)
Carbon Isotopes/metabolism , Models, Biological , Squalus acanthias/physiology , Animals , Carbon Isotopes/analysis , Diet , Lipids , Liver/metabolism , Muscle Fibers, Fast-Twitch/metabolism , Predatory Behavior , Species Specificity , Squalus acanthias/metabolism
15.
Am J Physiol Regul Integr Comp Physiol ; 296(5): R1547-56, 2009 May.
Article in English | MEDLINE | ID: mdl-19176885

ABSTRACT

Hypoxia and increased temperature alter venous blood pressures in teleosts through active changes in venous tone. Elasmobranchs possess a capacious venous system but have limited adrenergic vascular innervation and subambient central venous pressure (P(cv)). In this study, we explored venous hemodynamic responses to acute temperature increase and moderate (6.9 kPa) and severe (2.5 kPa) hypoxia in the dogfish (Squalus acanthias). Normoxic dogfish at 10 degrees C had a P(cv) between -0.08 and -0.04 kPa and a mean circulatory filling pressure (P(mcf)) of approximately 0.12 kPa. At 16 degrees C, heart rate (f(H)), cardiac output (Q), and P(mcf) increased but P(cv) and plasma epinephrine and norepinephrine levels were unchanged. In contrast, moderate and severe hypoxia increased P(cv) and decreased Q and stroke volume (V(S)). f(H) decreased in severe hypoxia, whereas P(mcf) was unaffected despite elevated catecholamine levels. Atropine abolished hypoxic reductions in Q, V(S), and f(H), but P(cv) still increased. In contrast to the response in teleosts, this study on dogfish suggests that venous capacitance changes associated with warming and hypoxia are minimal and likely not mediated by circulating catecholamines. Thus hemodynamic status of the capacious elasmobranch venous circulation is potentially regulated by blood volume shifts from passive flow-mediated events and possibly through myogenic mechanisms.


Subject(s)
Catecholamines/blood , Heart Rate/physiology , Hypoxia/physiopathology , Squalus acanthias/physiology , Temperature , Veins/physiology , Animals , Cardiac Output/physiology , Female , Hot Temperature , Male , Models, Animal , Venous Pressure/physiology
16.
Physiol Biochem Zool ; 81(3): 278-87, 2008.
Article in English | MEDLINE | ID: mdl-18419554

ABSTRACT

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.


Subject(s)
Alkalosis/metabolism , Energy Metabolism/physiology , L-Lactate Dehydrogenase/metabolism , Sodium-Potassium-Exchanging ATPase/metabolism , Squalus acanthias/physiology , Animals , Energy Metabolism/drug effects , Fish Proteins/metabolism , Food Deprivation , Hydrogen-Ion Concentration , L-Lactate Dehydrogenase/blood , Male , Seawater/chemistry , Sodium Bicarbonate/blood , Sodium Bicarbonate/pharmacology , Sodium Chloride/blood , Sodium Chloride/pharmacology , Sodium-Potassium-Exchanging ATPase/blood , Squalus acanthias/blood , Water-Electrolyte Balance
17.
J Exp Biol ; 210(Pt 8): 1335-49, 2007 Apr.
Article in English | MEDLINE | ID: mdl-17401117

ABSTRACT

In order to study the physiological consequences of voluntary feeding in the gastrointestinal tract of a ureotelic marine elasmobranch, dogfish (fasted for 96 h) were sampled at various times up to 360 h after consuming a 5-6% ration of teleost fish (hake) under natural feeding conditions. Digestion and absorption were completed between 120 and 360 h post-feeding. The tissue masses of different segments of the gastrointestinal tract increased and decreased markedly as the chyme moved through, mainly because of fluid engorgement rather than hyperplasia. In fasted dogfish, the cardiac and pyloric stomachs contained only small volumes of highly acidic fluid (pH 1.77+/-1.12, 2.05+/-0.08) similar in composition to seawater. Feeding resulted in gastric pHs of 3.20+/-0.31 and 3.95+/-0.40 at 6 h, followed by slow declines through 60 h. An alkaline tide in the blood also occurred at 6 h. In the face of large changing masses of highly acidic chyme in the stomachs, the pH (6.50+/-0.10), ionic composition and volume of chyme in the intestine (spiral valve) were precisely regulated from 6 to 60 h post-feeding at very different values from those in the stomachs, and intestinal HCO3(-) remained low (5.12+/-0.83 mmol l(-1)). The colon was usually empty and its pH constant at 7.20+/-0.16 at all times. Despite the ingestion of strongly hypo-osmotic teleost tissue, the osmolality of the chyme remained in equilibrium with that of the blood plasma in all segments at all times after feeding. Much of the osmotic equilibration was because of the secretion of urea into the chyme, particularly in the intestine. After feeding, gastric fluid concentrations of Na(+) and Mg(2+) declined, K(+) and Ca(2+) increased, whereas Cl(-) exhibited little change, indicating that additional drinking of seawater was minimal. Na(+), K(+), water and especially Cl(-) were absorbed in the intestine, whereas Mg(2+) and Ca(2+) were largely excluded. Our results illustrate the complex integration of digestive and ionoregulatory function in the elasmobranch digestive tract, and marked differences from the teleost pattern.


Subject(s)
Acid-Base Equilibrium/physiology , Gastrointestinal Tract/physiology , Postprandial Period/physiology , Squalus acanthias/physiology , Water-Electrolyte Balance/physiology , Analysis of Variance , Animals , Chlorides/analysis , Gastrointestinal Contents/chemistry , Hydrogen-Ion Concentration , Potassium/analysis , Sodium/analysis , Time Factors
18.
Article in English | MEDLINE | ID: mdl-17208025

ABSTRACT

We recently cloned an NHE3 orthologue from the gills of the euryhaline Atlantic stingray (Dasyatis sabina), and generated a stingray NHE3 antibody to unequivocally localize the exchanger to the apical side of epithelial cells that are rich with Na(+)/K(+)-ATPase (A MRC). We also demonstrated an increase in NHE3 expression when stingrays are in fresh water, suggesting that NHE3 is responsible for active Na(+) absorption. However, the vast majority of elasmobranchs are only found in marine environments. In the current study, immunohistochemistry with the stingray NHE3 antibody was used to localize the exchanger in the gills of the stenohaline marine spiny dogfish shark (Squalus acanthias). NHE3 immunoreactivity was confined to the apical side of cells with basolateral Na(+)/K(+)-ATPase and was excluded from cells with high levels of vacuolar H(+)-ATPase. Western blots detected a single protein of 88 kDa in dogfish gills, the same size as NHE3 in stingrays and mammals. These immunological data demonstrate that the putative cell type responsible for active Na(+) absorption in euryhaline elasmobranchs is also present in stenohaline marine elasmobranchs, and suggest that the inability of most elasmobranchs to survive in fresh water is not due to a lack of the gill ion transporters for Na(+) absorption.


Subject(s)
Gills/physiology , Sodium/metabolism , Squalus acanthias/physiology , Animals , Blotting, Western , Immunohistochemistry , Sodium-Hydrogen Exchanger 3 , Sodium-Hydrogen Exchangers/immunology , Sodium-Hydrogen Exchangers/metabolism , Sodium-Potassium-Exchanging ATPase/metabolism
19.
Zebrafish ; 4(4): 261-75, 2007.
Article in English | MEDLINE | ID: mdl-18284333

ABSTRACT

The multidrug resistance-associated protein 3 (MRP3/Mrp3) is a member of the ATP-binding cassette (ABC) protein family of membrane transporters and related proteins that act on a variety of xenobiotic and anionic molecules to transfer these substrates in an ATP-dependent manner. In recent years, useful comparative information regarding evolutionarily conserved structure and transport functions of these proteins has accrued through the use of primitive marine animals such as cartilaginous fish. Until recently, one missing tool in comparative studies with cartilaginous fish was cell culture. We have derived from the embryo of Squalus acanthias, the spiny dogfish shark, the S. acanthias embryo (SAE) mesenchymal stem cell line. This is the first continuously proliferating cell line from a cartilaginous fish. We identified expression of Mrp3 in this cell line, cloned the molecule, and examined molecular and cellular physiological aspects of the protein. Shark Mrp3 is characterized by three membrane-spanning domains and two nucleotide-binding domains. Multiple alignments with other species showed that the shark Mrp3 amino acid sequence was well conserved. The shark sequence was overall 64% identical to human MRP3, 72% identical to chicken Mrp3, and 71% identical to frog and stickleback Mrp3. Highest identity between shark and human amino acid sequence (82%) was seen in the carboxyl-terminal nucleotide-binding domain of the proteins. Cell culture experiments showed that mRNA for the protein was induced as much as 25-fold by peptide growth factors, fetal bovine serum, and lipid nutritional components, with the largest effect mediated by a combination of lipids including unsaturated and saturated fatty acids, cholesterol, and vitamin E.


Subject(s)
Embryo, Nonmammalian/physiology , Gene Expression Regulation, Developmental/physiology , Mesenchymal Stem Cells/metabolism , Multidrug Resistance-Associated Proteins/biosynthesis , Squalus acanthias/physiology , Amino Acid Sequence , Animals , Base Sequence , Cell Line , Cloning, Molecular , Culture Media , DNA/chemistry , Embryo, Nonmammalian/cytology , Insulin/physiology , Intercellular Signaling Peptides and Proteins/physiology , Lipids/physiology , Mesenchymal Stem Cells/cytology , Molecular Sequence Data , Multidrug Resistance-Associated Proteins/chemistry , Multidrug Resistance-Associated Proteins/genetics , Mutation , Polymorphism, Genetic , Sequence Alignment , Sequence Homology, Amino Acid , Squalus acanthias/embryology
20.
Am J Physiol Regul Integr Comp Physiol ; 291(5): R1465-73, 2006 Nov.
Article in English | MEDLINE | ID: mdl-16825417

ABSTRACT

Subambient central venous pressure (Pven) and modulation of venous return through cardiac suction (vis a fronte) characterizes the venous circulation in sharks. Venous capacitance was estimated in the dogfish Squalus acanthias by measuring the mean circulatory filling pressure (MCFP) during transient occlusion of cardiac outflow. We tested the hypothesis that venous return and cardiac preload can be altered additionally through adrenergic changes of venous capacitance. The experiments involved the surgical opening of the pericardium to place a perivascular occluder around the conus arteriosus. Another control group was identically instrumented, but lacked the occluder, and was subjected to the same pharmacological protocol to evaluate how pericardioectomy affected cardiovascular status. Routine Pven was negative (-0.08+/-0.02 kPa) in control fish but positive (0.09+/-0.01 kPa) in the pericardioectomized group. Injections of 5 microg/kg body mass (Mb) of epinephrine and phenylephrine (100 microg/kg Mb) increased Pven and MCFP, whereas isoproterenol (1 microg/kg Mb) decreased both variables. Thus, constriction and relaxation of the venous vasculature were mediated through the respective stimulation of alpha- and beta-adrenergic receptors. Alpha-adrenergic blockade with prazosin (1 mg/kg Mb) attenuated the responses to phenylephrine and decreased resting Pven in pericardioectomized animals. Our results provide convincing evidence for adrenergic control of the venous vasculature in elasmobranchs, although the pericardium is clearly an important component in the modulation of venous function. Thus active changes in venous capacitance have previously been underestimated as an important means of modulating venous return and cardiac performance in this group.


Subject(s)
Blood Circulation/physiology , Central Venous Pressure/physiology , Pericardium/physiology , Receptors, Adrenergic/physiology , Squalus acanthias/physiology , Vascular Capacitance/physiology , Adrenergic Agonists/pharmacology , Adrenergic Antagonists/pharmacology , Animals , Cardiac Output/drug effects , Cardiac Output/physiology , Epinephrine/pharmacology , Female , Male , Myocardial Contraction/drug effects , Myocardial Contraction/physiology , Pericardiectomy , Pericardium/surgery , Phenylephrine/pharmacology , Prazosin/pharmacology , Receptors, Adrenergic/drug effects , Stroke Volume/drug effects , Stroke Volume/physiology
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