Responses of a coral reef shark acutely exposed to ocean acidification conditions

Anthropogenic ocean acidification (OA) is a threat to coral reef fishes, but few studies have investigated responses of high-trophic-level predators, including sharks. We tested the effects of 72-hr exposure to OA-relevant elevated partial pressures of carbon dioxide (pCO₂) on oxygen uptake rates, acid–base status, and haematology of newborn tropical blacktip reef sharks (Carcharhinus melanopterus). Acute exposure to end-of-century pCO₂ levels resulted in elevated haematocrit (i.e. stress or compensation of oxygen uptake rates) and blood lactate concentrations (i.e. prolonged recovery) in the newborns. Conversely, whole blood and mean corpuscular haemoglobin concentrations, blood pH, estimates of standard and maximum metabolic rates, and aerobic scope remained unaffected. Taken together, newborn blacktip reef sharks appear physiologically robust to end-of-century pCO₂ levels, but less so than other, previously investigated, tropical carpet sharks. Our results suggest peak fluctuating pCO₂ levels in coral reef lagoons could still physiologically affect newborn reef sharks, but studies assessing the effects of long-term exposure and in combination with other anthropogenic stressors are needed.

     

A novel pharyngeal expansion mechanism in the yellow-spotted fanray, Platyrhina tangi (Elasmobranchii: Batoidea), with special reference to the function of the fifth ceratobranchial cartilage in batoids

Expansion of the ‘pharynx’ during breathing or capturing prey in fishes generally involves posteroventral retraction of the hyoid arch. However, the hyoid arch structure of batoid fishes (skates, rays, guitarfishes, and sawfishes) is unique, and how they expand the pharyngeal cavity is poorly understood. To investigate the mechanism of pharyngeal expansion during breathing in the yellow-spotted fanray, Platyrhina tangi, we conducted anatomical and kinematic investigations of the pharyngeal region. Our study revealed that the yellow-spotted fanray and sharks have different skeletal linkage systems for pharyngeal expansion. During pharyngeal expansion in the yellow-spotted fanray, the hyoid bar and branchial apparatus rotate ventrally around the hinge joint between the fifth ceratobranchial cartilage and the pectoral girdle. This pharyngeal expansion mechanism appears to be widespread among batoid fishes and is unique among cartilaginous fishes (sharks, batoids, and holocephalans). Batoid fishes possibly developed this pharyngeal expansion mechanism during early batoid evolution.     

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.     

Serum steroid hormones including 11-ketotestosterone, 11-ketoandrostenedione, and dihydroprogesterone in juvenile and adult bonnethead sharks, Sphyrna tiburo.

Previous studies in the placental viviparous bonnethead shark, Sphyrna tiburo, have correlated 17 beta-estradiol, progesterone, testosterone, and dihydrotestosterone with reproductive events in both males and females. However, several key reproductive events, including implantation, maintenance of pregnancy, and parturition, did not correlate with these four steroid hormones. Therefore, the present study investigated three steroid hormones, 11-ketotestosterone, 11-ketoandrostenedione, and dihydroprogesterone, which have demonstrably important roles in the reproductive cycles of teleosts. It was hypothesized that one or more of these three hormones would correlate with specific reproductive events in S. tiburo. Concurrently, developmental (growth and/or maturation) analyses of these three steroids plus 17 beta-estradiol, progesterone, testosterone, and dihydrotestosterone were investigated in juvenile bonnethead sharks. Serum dihydroprogesterone concentrations were highest in mature females and 11-ketotestosterone concentrations were highest in mature males. In mature females, 11-ketoandrostenedione levels were elevated from the time of mating, through six months of sperm storage and another four months of gestation. At parturition concentrations became significantly lower and remained lower until mating occurred again in another two to three months. Serum 11-ketotestosterone concentrations were the highest at implantation though not significant. In mature males, significantly elevated serum levels of dihydroprogesterone occurred in April and May, near the start of annual testicular development. During growth in males, testosterone and dihydrotestosterone increased progressively and in females, testosterone increased progressively. At maturity in males, significant increases occurred in testosterone and 11-ketotestosterone concentrations while, in females, dihydroprogesterone, 11-ketotestosterone, 17 beta-estradiol, progesterone, testosterone, and dihydrotestosterone concentrations increased. This study shows that although testosterone may be the primary androgen in the bonnethead shark, other derived androgens may have important functions in growth, maturation, and reproduction. J. Exp. Zool. 284:595-603, 1999.     

Review: Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas.

Elasmobranchs and bony fishes have evolved independently for more than 400 million years. However, two Recent groups, the lamnid sharks (Family Lamnidae) and tunas (Family Scombridae), display remarkable similarities in features related to swimming performance. Traits separating these two groups from other fishes include a higher degree of body streamlining, a shift in the position of the aerobic, red, locomotor muscle that powers sustained swimming to a more anterior location in the body and nearer to the vertebral column, the capacity to conserve metabolic heat (i.e. regional endothermy), an increased gill surface area with a decreased blood-water barrier thickness, a higher maximum blood oxygen carrying capacity, and greater muscle aerobic and anaerobic enzyme activities at in vivo temperatures. The suite of morphological, physiological, and biochemical specializations that define "high-performance fishes" have been extensively characterized in the tunas. This review examines the convergent features of lamnid sharks and tunas in order to gain insight into the extent that comparable environmental selection pressures have led to the independent origin of similar suites of functional characteristics in these two distinctly different taxa. We propose that, despite differences between teleost and elasmobranch fishes, lamnid sharks and tunas have evolved morphological and physiological specializations that enhance their swimming performance relative to other sharks and most other high performance pelagic fishes.     

New insights on the trophic ecology of blue (Prionace glauca) and shortfin mako sharks (Isurus oxyrinchus) from the oceanic eastern South Pacific

The blue shark (Prionace glauca) and the shortfin mako shark (Isurus oxyrinchus) are two large and highly migratory sharks distributed in most oceans. Although they are often caught in the south Pacific Ocean long-line fisheries, their trophic ecology is poorly understood. Stable isotopes with Bayesian mixing and dependence concentration models were performed to determine the diet and trophic differences between the two species in the South-eastern Pacific Ocean. According to the mixing models, fishes are the most important prey of these sharks. Dolphin calves and remains were found in the stomachs of both species, which represents a novel finding in trophic ecology of South Pacific sharks. Intra-specific differences were found in P. glauca, but not in specimens of I. oxyrinchus. The two sharks showed a high degree of diet overlap (73%), primarily over mackerel and dolphin carcasses. Our results indicate that blue and shortfin mako sharks have a generalist feeding strategy in the eastern Pacific Ocean, with a strong preference for teleost fishes and also for dolphin carcasses. Therefore, trophic studies are useful to understand energy flow through the food web, and the trophic position of key species.     

Osmoregulatory Functions of Neurohypophysial Hormones in Fishes and Amphibians

The renal effects of neurohypophysial hormones in fishes andamphibians are discussed. Injections of arginine vasotocin (AVT)elicit diuresis in fishes, but antidiuresis in amphibians. However,the physiological significance of these hormonal responses remainsto be demonstrated. Studies with bioassays and radio-immunoassayson circulating levels of AVT indicate that hypovolemia may bea very potent stimulus for the release of the hormone. Hyperosmoticstimuli may not be as important. In anurans, mesotocin has aglomerular diuretic effect. This neurohypophysial hormone appearsto dilate, while AVT constricts, the afferent glomerular circulationin bullfrogs, Rana catesbeiana.     

Ontogeny of head and caudal fin shape of an apex marine predator: The tiger shark (Galeocerdo cuvier)

How morphology changes with size can have profound effects on the life history and ecology of an animal. For apex predators that can impact higher level ecosystem processes, such changes may have consequences for other species. Tiger sharks (Galeocerdo cuvier) are an apex predator in tropical seas, and, as adults, are highly migratory. However, little is known about ontogenetic changes in their body form, especially in relation to two aspects of shape that influence locomotion (caudal fin) and feeding (head shape). We captured digital images of the heads and caudal fins of live tiger sharks from Southern Florida and the Bahamas ranging in body size (hence age), and quantified shape of each using elliptical Fourier analysis. This revealed changes in the shape of the head and caudal fin of tiger sharks across ontogeny. Smaller juvenile tiger sharks show an asymmetrical tail with the dorsal (upper) lobe being substantially larger than the ventral (lower) lobe, and transition to more symmetrical tail in larger adults, although the upper lobe remains relatively larger in adults. The heads of juvenile tiger sharks are more conical, which transition to relatively broader heads over ontogeny. We interpret these changes as a result of two ecological transitions. First, adult tiger sharks can undertake extensive migrations and a more symmetrical tail could be more efficient for swimming longer distances, although we did not test this possibility. Second, adult tiger sharks expand their diet to consume larger and more diverse prey with age (turtles, mammals, and elasmobranchs), which requires substantially greater bite area and force to process. In contrast, juvenile tiger sharks consume smaller prey, such as fishes, crustaceans, and invertebrates. Our data reveal significant morphological shifts in an apex predator, which could have effects for other species that tiger sharks consume and interact with. J. Morphol. 277:556–564, 2016. © 2016 Wiley Periodicals, Inc.     

Is there a hormonal network in Tetrahymena? A systematic investigation of hormonal effects on the hormone content

The effect of six hormones (histamine, serotonin, insulin, epidermal growth factor (EGF), oxytocin and gonadotropin) was studied on the hormone (histamine, serotonin, adrenocorticotropic hormone [ACTH], endorphin and triiodothyronine [T(3)]) content of Tetrahymena. The hormones were given in 10(-9) or 10(-12) M concentrations or as 0.1 and 0.001 I.U. ml(-1) (in the case of oxytocin and gonadotropin) for 1 h. The hormones in picomolar concentration, i.e. at levels which can be present also in natural conditions, influence the amount of other hormones inside the cell. Their effect is not a general one: it is individual, the level of one of the hormones was elevated, while that of the others diminished under the effect of the same hormonal stimulus. Insulin was the only hormone, which influenced the concentration of other hormones in one direction, elevating them. This effect could have a role in the life-saving property of this hormone in Tetrahymena, but the hormones were not studied from this point of view. Usually there is no difference between the effect of the two concentrations used, but there are situations when the effect of the two concentrations is opposite. This means that there is a possible concentration dependence and this could influence differently the cells which are far from or near to the secretor cell. Considering earlier observations, the duration of the treatment can also influence the result. The results give new data to the hormonal regulation at unicellular level (which can be the base of regulation at higher evolutionary levels) and point to the possibility of a hormonal network.     

Thyroid hormone levels in the peripheral blood of the ground squirrel Citellus parryi during winter hibernation

In the Arctic ground squirrel Citellus parryi, thyroxine and triiodothyronine concentrations in the peripheral blood have been determined by RIA in various seasons and during a short hibernation period. It was shown that during hibernation (December-February), hormonal concentration is higher than during homoiothermal period (August-October). The highest concentration of the thyroid hormones was found in hibernating animals in January. The data obtained indicate that thyroid hormones are involved in control of hibernation of the species investigated.     

The fish tail as a derivation from axial musculoskeletal anatomy: an integrative analysis of functional morphology

The adult morphology of the tail varies greatly among extant fishes despite sharing both ontogenetic similarities and the functional need to propel the body through a fluid medium. Both sharks (Chondrichthyes) and ray-finned fishes (Actinopterygii) control caudal fin musculature independently of axial body myomere activity to modify the stiffness and shape of their tails. For example, sharks and bony fishes possess different structural elements and muscles and move their tails in different ways, resulting in different locomotory hydrodynamic effects and a range of performance variables including speed and maneuverability. The stiffness of the heterocercal, lobate tail of the shark can be modulated during the tail beat resulting in nearly continuous thrust production. In contrast, the highly flexible tail of ray-finned fishes can be manipulated into many different shape conformations enabling increased maneuverability for these fishes. Consequently, the developmental, morphological, and functional derivation of the tail from the axial trunk has resulted in a diversity of form, the attributes of which may be of ecological and evolutionary significance.     

The endocrinology of pregnancy and fetal loss in wild baboons

An impressive body of research has focused on the mechanisms by which the steroid estrogens (E), progestins (P), and glucocorticoids (GC) ensure successful pregnancy. With the advance of non-invasive techniques to measure steroids in urine and feces, steroid hormones are routinely monitored to detect pregnancy in wild mammalian species, but hormone data on fetal loss have been sparse. Here, we examine fecal steroid hormones from five groups of wild yellow baboons (Papio cynocephalus) in the Amboseli basin of Kenya to compare the hormones of successful pregnancies to those ending in fetal loss or stillbirth. Using a combination of longitudinal and cross-sectional data, we analyzed three steroid hormones (E, P, GC) and related metabolites from 5 years of fecal samples across 188 pregnancies. Our results document the course of steroid hormone concentrations across successful baboon pregnancy in the wild and demonstrate that fecal estrogens predicted impending fetal loss starting 2 months before the externally observed loss. By also considering an additional 450 pregnancies for which we did not have hormonal data, we determined that the probability for fetal loss for Amboseli baboons was 13.9%, and that fetal mortality occurred throughout gestation (91 losses occurred in 656 pregnancies; rates were the same for pregnancies with and without hormonal data). These results demonstrate that our longstanding method for early detection of pregnancies based on observation of external indicators closely matches hormonal identification of pregnancy in wild baboons.     

Plasma steroid hormone profiles and reproductive biology of the epaulette shark, Hemiscyllium ocellatum.

Examination of the reproductive biology of the oviparous epaulette shark, Hemiscyllium ocellatum, was conducted on a wild population. Male sharks were found to reach maturity at between 55-60 cm total length (TL) and female sharks mature around 55 cm TL. Blood samples collected from mature male and female sharks were analyzed for sex steroid hormones to examine seasonal hormone patterns. Plasma samples were analyzed via radioimmunoassay techniques with female samples measured for estradiol, progesterone, and androgen concentrations, and male samples measured for androgen concentrations. Male androgen concentrations showed a single broad peak from July to October with maximum hormone concentrations (60 ng/ml) occurring in August. Male androgen concentrations were lowest in December-February (<20 ng/ml), and appeared to correlate with reproductive activity and water temperature. Female androgen concentrations were an order of magnitude lower than those for males and showed peaks in June (6 ng/ml) and December (8 ng/ml). Estradiol concentrations in females peaked during the months of September-November (0.5 ng/ml) coinciding with the egg laying period. Progesterone concentrations ranged up to 0.5 ng/ml prior to the mating season. Observations of ova size and egg production showed eggs develop in pairs and ova are ovulated at a size of 25-27 mm. Females lay eggs from August to January. Males were observed with swollen claspers from July through December, with the highest amount of sperm storage in the epididymis occurring between August through November. Our observations indicate that epaulette sharks in the waters near Heron Island mate from July through December. J. Exp. Zool. 284:586-594, 1999.     

Mammary gland differentiation in hypophysectomized, pregnant mice treated with corticosterone and thyroxine.

Swiss Webster mice were hypophysectomized or sham-operated on Day 11 of pregnancy. The animals were fitted s.c. with osmotic minipumps containing either corticosterone (B) dissolved in Molecusol (Pharmatec, Alachua, FL) or the vehicle alone immediately after they were hypophysectomized. Animals in some of the experimental groups also received thyroxine (T4) in their drinking water. The mice were killed on Day 18 of gestation, and mammary tissue was homogenized and extracted for assessment of DNA, RNA, alpha-lactalbumin, and alpha-casein. Serum was assayed for placental lactogen-I (PL-I), and placental lactogen-II (PL-II), B, and T4. The concentration of PL-II in serum was elevated in the hypophysectomized mice, whereas the PL-I concentration did not differ among experimental groups. Hypophysectomy decreased both T4 and B concentrations in serum, and administration of these hormones restored their serum concentrations to normal or, in some cases, somewhat higher than normal levels. Hypophysectomy reduced the total RNA content and RNA/DNA ratio of the mammary gland, but treatment with B alone or with B and T4 restored RNA levels to those of sham-operated animals. T4 alone was ineffective in restoring RNA levels. Sham-operated animals that received hormonal treatment (B and T4) had the highest levels of RNA in the mammary tissue. Hypophysectomized animals had reduced content and concentration of alpha-lactalbumin in the mammary gland as compared to all other experimental groups.(ABSTRACT TRUNCATED AT 250 WORDS)     

Feeding habits of Scymnorhinus licha in Catalan waters

A study has been made of the diet of Scymnorhinus licha in Catalan coastal waters by means of the analysis of the stomach contents of 97 specimens caught at depths ranging from 300 to 600 metres during a 12 month survey. The annual coefficient of repletion is 80%. Bony fishes form the basic group in the diet for all seasons: they are followed by sharks, crustaceans and cephalopods, which are secondary. As the size of G. licha increases, there is an increase in the frequency of crustaceans and sharks in the stomach contents and a drop in the frequency of cephalopods. Bony fishes are slightly more frequent in the larger specimens. The males have a higher coefficient of repletion and a higher average of prey per stomach and show a greater preference for sharks and bony fishes.     

How type of parturition and health status influence hormonal and metabolic profiles in newborn foals

Thyroid hormones, insulin growth factor I (IGF-I) and non-esterified fatty acids (NEFA) represent important hormonal and metabolic factors associated with perinatal growth and maturation. Their action could be influenced by the type of parturition and the health status of the foal and therefore the aim of this work is to evaluate their plasma concentrations in newborn foals during the first 2 wks of life. Three groups of subjects were enrolled: 15 healthy foals born by spontaneous parturition, 24 healthy foals born by induced parturition and 26 pathologic foals. From each of the healthy foals, blood was collected at 10, 20 and 30 minutes, 3 and 12 hours from birth, daily from Day 1 to Day 7, and at Day 10 and 14 of life. In pathologic foals samples were collected twice a day from the day of admission at the hospital until the day of discharge or death. Thyroid hormones (T3 and T4) and IGF-I were analyzed by radioimmunoassay and NEFA by enzymatic-colorimetric methods. In all the three groups a declining trend of T3 and T4 plasma concentrations was detectable, with lower levels in the pathologic group compared to healthy foals. Spontaneous foals showed higher levels of T3 at 7 d compared to induced foals, while T4 levels were higher in spontaneous vs. induced foals before 6 h of life, at three and seven days. IGF-I showed increasing plasma concentrations in all three considered groups. No differences were found between healthy and pathologic foals. NEFA in spontaneous and induced healthy foals showed a declining trend with higher levels during the first hours of life. Pathologic foals presented higher levels compared to spontaneous foals only at 24 h and 10 d. These data suggest that the type of foaling could influence the reference ranges for thyroid hormones. Moreover, pathologic foals showed some hormonal and metabolic differences related to their health status. Above all changes of thyroid hormones levels, early in postnatal life, could be a cause, and not only a consequence, of the diseased condition of these foals.     

Expression of sex steroid receptors and IGF-1 mRNA in breast tissue--effects of hormonal treatment

The mechanisms behind increased breast tissue proliferation and a possibly increased breast cancer risk in women using hormonal contraception (HC) and hormonal replacement therapy (HRT) are incompletely understood. We analyzed breast tissue from 20 premenopausal and seven postmenopausal women undergoing reduction mammoplasties for estrogen receptor (ER) and progesterone receptor (PR) content as well as mRNA levels for ER, PR and insulin-like growth factor-1 (IGF-1). The receptor values were correlated to IGF-1 mRNA concentrations and levels of steroid and peptide hormones and SHBG. In women using HC, we found significantly lower ER values (p=0.02) but non-significantly lower ER mRNA levels compared to those in naturally cycling women. PR and PR mRNA were no different. Women on HC displayed a higher breast tissue proliferation (p=0.05) expressed as Ki-67, MIB-1 positivity, which was correlated with IGF-1 mRNA (r_s=0.82, p=0.04). Since the concentration of sex steroid receptors in breast tissue is comparatively low and steroid receptors are down-regulated during hormonal treatment, mechanisms other than direct sex steroid receptor action are likely to be present. Our results suggest a role for IGF-1 in the proliferative response of breast tissue during exogenous hormonal treatment.     

Paternity, parental behavior and circulating steroid hormone concentrations in nest-tending male bluegill

Like many teleost fishes, bluegill (Lepomis macrochirus) are characterized by sole male parental care of offspring. In addition, bluegill parental males experience cuckoldry by specialized parasitic male morphs. This cuckoldry has previously been shown to influence the expression of parental care behavior. To better understand some of the proximate mechanisms mediating parental behavior, we examined the relationships between circulating steroid hormones, paternity, and parental behavior during the egg and fry stages of care in parentals that spawned during the first third of the breeding season. During the egg stage of care, we found that males with higher paternity had lower levels of testosterone, but there was no relationship between paternity and either 11-ketotestosterone or cortisol. There also was no relationship between the hormones and care behavior comprising fanning of the eggs, nest rim circles, chases of brood predators, or pecking at the eggs (indicative of egg cannibalism), except for a negative relationship between cortisol and pecking behavior. During the fry stage of care, we conversely found that males with higher paternity had higher levels of testosterone and 11-ketotestosterone. There also was a negative relationship between the concentrations of these two androgens and the defensive behavior of males when exposed to a potential brood predator (a pumpkinseed, Lepomis gibbosus). We discuss these results in relation to previous work in fishes and other vertebrate taxa. Overall, our data suggest a complex relationship between circulating steroid hormone levels, paternity and parental behavior.     

The existence during gestation of an immunological buffer zone at the interface between maternal and foetal tissues.

In mammalian pregnancy the trophoblast normally constitutes an uninterrupted boundary of foetal tissue in immediate contact with maternal tissue, including blood in some species, and is the decisive immunological barrier to rejection of the foetus as an allograft. The ability of the trophoblast to function as a barrier evidently results from its capacity to resist immunological attack by either alloantibody or alloimmune cells and to prevent immunocompetent cells from reaching and damaging the foetus but, as yet, there is no general agreement regarding the means by which it exercises these functions. In view of the dramatic hormonal changes that occur during pregnancy and the undisputed involvement of trophoblast in these endocrine events, the possibility exists of an interaction between the hormones of pregnancy and the immunological phenomena. The present account furnishes evidence that endocrine activity at the maternal surface of the trophoblast, the presumptive site of the immunological frontier between foetus and mother, may be a factor in its local survival at implantation. The placental hormones so far known that are capable of blocking the antigen receptor sites of the mother's lymphocytes and thus preventing the latter from reacting with the foetal antigens are the glycoprotein, human chorionic gonadotrophin (HCG) and the polypeptide hormone, human chorionic somatomammotrophin (HCS) or human placental lactogen (HPL), both of which are specific to the human placenta. The origin of these hormones, their spatial distribution and their probable interaction with placental steroid hormones are discussed. It is argued that the place of highest concentration of these hormones is on the surface of the syncytial microvilli and the adjacent caviolae of the apical plasma membrane, as well as on the surfaces of the persisting cytotrophoblastic cells of the basal plate (cytotrophoblastic shell), the cell islands and the septa-precisely where the immunological challenge of the foetal allograft to the maternal host occurs. An explanation is offered for the continuing production of the voluminous quantities of these hormones during human pregnancy.