Placentation and associated aspects of gestation in the bonnethead shark, Sphyrna tiburo

The left ovary of the bonnethead shark, Sphyrna tiburo, is rudimentary, and the right ovary supplies both oviducts which share a common ostium situated in the falciform ligament. Preceding ovulation the nidamental gland of each oviduct hypertrophies and the caudal two-thirds of each oviduct is modified to form a uterus. In the Florida-Caribbean area Sphyrna tiburo probably mates in March and 3–7 eggs are fertilized in the vicinity of the nidamental gland of each oviduct. The developing embryo is nourished during the first 3–4 months of gestation by yolk stored in its extensive yolk sac. Approximately three and one-half months after fertilization, the distal portion of the yolk sac becomes convoluted and interdigitates with deep folds in the uterine wall to form a yolk-sac placenta. As the placenta develops, the maternal uterine epithelium is reduced from columnar cells to squamous cells, and the foetal yolk-sac epithelium is reduced from columnar and cuboidal cells to squamous cells. Exchange between the maternal and foetal blood systems takes place through maternal endothelium, reduced maternal epithelium, egg-case membrane, reduced foetal epithelium, and foetal endothelium.     

Calcitonin-like immunoreactivity in serum and tissues of the bonnethead shark,Sphyrna tiburo

Calcitonin is a 32-amino acid peptide hormone that is best known for its actions in maintaining skeletal integrity and calcium homeostasis in mammals. Calcitonin also appears to function in regulating certain aspects of animal reproduction, but the nature of this role remains unclear, particularly in nonmammalian vertebrates. The present study investigated the relationship between calcitonin and reproduction in the bonnethead shark (Sphyrna tiburo), a well-studied member of the oldest living vertebrate group (i.e. elasmobranchs) known to possess a calcitonin-producing organ. Serum calcitonin concentrations were measured in 28 reproductively mature female S. tiburo using a heterologous enzyme-linked immunosorbent assay (ELISA) system. Sites of calcitonin immunoreactivity were detected in tissues of mature female and embryonic S. tiburo using immunocytochemistry. Significant increases in serum calcitonin concentrations of mature female S. tiburo occurred during early stages of gestation, a period characterized by yolk-dependency of developing embryos. Immunoreactive calcitonin was detected in the duodenum and pancreas of embryonic S. tiburo sampled during the same period. The results from this study suggest that calcitonin obtained from endogenous and/or maternal sources may function in regulating yolk digestion in embryonic S. tiburo. Therefore, the association between calcitonin and reproduction in elasmobranchs may reflect an important role for this hormone in embryonic development.     

Geographic variation in reproduction between two populations of the bonnethead shark,Sphyrna tiburo

Synopsis A study of two populations of the bonnethead shark,Sphyrna tiburo was conducted in Florida Bay and Tampa Bay, Florida from September 1982 to December 1986. The maintenance of sharks in captivity at the Marine Science and Conservation Center in the Florida Keys, and the collection of sharks from widely separated geographical areas allowed the examination of latitudinal variation in reproduction. Several reproductive parameters were found to differ: (1) size at maturation, (2) age at maturation, (3) time of fertilization, (4) rate of embryonic development, (5) size at birth, (6) the energetic investment in producing offspring, (7) gestation period, and (8) the incidence of infertility. Average litter size and maximum age of females was not different between the two populations. These contrasting life history parameters are not easily explained. Food limitation and seasonal differences between the two areas are considered as factors controlling reproduction in these populations. It is noteworthy that the average size of adult females in Tampa Bay is significantly greater than that of Florida Keys sharks. This size difference may be important in explaining the observed differences in reproduction.     

The sexually dimorphic cephalofoil of bonnethead sharks, Sphyrna tiburo

Sexually dimorphic head shape is common in vertebrates from teleosts to mammals. Herein we document that cephalic sexual dimorphism is also found in the cartilaginous fishes (Chondrichthyes). Male bonnethead sharks develop a prominent bulge along the anterior margin of the cephalofoil at the onset of sexual maturity. This contrasts with the uniformly rounded anterior margin of adult females and juveniles and embryos of both sexes. The anterior cephalic bulge is produced by elongation of the rod-like rostral cartilages, and its appearance corresponds temporally with the elongation of the rod-like cartilages of the male intromittent organs (claspers). We propose that the rostral cartilage elongation is a byproduct of endocrinological changes at the onset of sexual maturity that stimulate growth of the clasper cartilages. The basal location of the chondrichthyan fishes within the vertebrate clade extends the earliest appearance of cephalic sexual dimorphism among the vertebrates.     

Age and growth of the bonnethead shark, Sphyrna tiburo, from northwest Florida, with comments on clinal variation

Age and growth rates of the bonnethead shark, Sphyrna tiburo, from northwest Florida were estimated from vertebrae collected between October 1992 and October 1995. The von Bertalanffy growth equation was fit to male and female vertebral age data. Initial growth was rapid (≈ 200 mm TL) for both sexes from age 0–1. At age 2 growth slowed for males but continued for females. Similar to many species of sharks, females grew slower than males (K = 0.28 and K = 0.69, respectively) but attained a larger maximum size (L_∞=1226 and L_∞=897). Maximum age was estimated in males and females to be 8+ and 12+ years, respectively. Growth of young-of-year sharks was 21 to 30 mm TL per month determined by three different methods. A comparison of age and growth estimates from populations at more southerly latitudes suggest that clinal variation in total length may be evident among bonnethead sharks in the Gulf of Mexico with females reaching larger sizes in northern areas as compared to south Florida. This revised version was published online in July 2006 with corrections to the Cover Date.     

Phylogeography and population genetics of the cryptic bonnethead shark Sphyrna aff. tiburo in Brazil and the Caribbean inferred from mtDNA markers

Resolving the identity, phylogeny and distribution of cryptic species within species complexes is an essential precursor to management. The bonnethead shark, Sphyrna tiburo, is a small coastal shark distributed in the Western Atlantic from North Carolina (U.S.A.) to southern Brazil. Genetic analyses based on mitochondrial markers revealed that bonnethead sharks comprise a species complex with at least two lineages in the Northwestern Atlantic and the Caribbean (S. tiburo and Sphyrna aff. tiburo, respectively). The phylogeographic and phylogenetic analysis of two mitochondrial markers [control region (mtCR) and cytochrome oxidase I (COI)] showed that bonnethead sharks from southeastern Brazil correspond to S. aff. tiburo, extending the distribution of this cryptic species >5000 km. Bonnethead shark populations are only managed in the U.S.A. and in the 2000s were considered to be regionally extinct or collapsed in southeast Brazil. The results indicate that there is significant genetic differentiation between S. aff. tiburo from Brazil and other populations from the Caribbean (Φ_ST = 0.9053, P < 0.000), which means that collapsed populations in the former are unlikely to be replenished from Caribbean immigration. The species identity of bonnethead sharks in the Southwest Atlantic and their relationship to North Atlantic and Caribbean populations still remains unresolved. Taxonomic revision and further sampling are required to reevaluate the status of the bonnethead shark complex through its distribution range.     

Residency and movement patterns of bonnethead sharks, Sphyrna tiburo, in a large Florida estuary

The use of a coastal estuary by bonnethead sharks, Sphyrna tiburo, was examined by acoustic monitoring, gillnet sampling and tag- recapture studies. Acoustic monitoring data were used to define the residency and movement patterns of sharks within Pine Island Sound, Charlotte Harbor, Florida. Sharks were monitored for periods of 1–173 days with individuals regularly moving in and out of the detection range of the acoustic system. Patterns of movement could not be correlated with tidal level or time of day. Home range sizes within the Pine Island Sound population were typically small with individuals using core areas on a daily basis. However, core areas shifted within the study site over time resulting in eventual usage of most of the available habitat. Gillnet sampling revealed that S. tiburo were abundant in shallow water near seagrass beds, but that presence of individuals at specific sites was variable. Tag-recapture data showed that most individuals remained within the Pine Island Sound region over time and did not appear to undergo long coastal migrations. The movement and residence patterns of S. tiburo suggest that individuals are resident within the estuary, but do not show site fidelity to specific areas within the estuary.     

Validated age,growth and maturity of the bonnethead Sphyrna tiburo in the western North Atlantic Ocean

The age, growth and maturity of bonnetheads Sphyrna tiburo inhabiting the estuarine and coastal waters of the western North Atlantic Ocean (WNA) from Onslow Bay, North Carolina, south to West Palm Beach, Florida, were examined. Vertebrae were collected and aged from 329 females and 217 males ranging in size from 262 to 1043 mm and 245 to 825 mm fork length, L_F, respectively. Sex‐specific von Bertalanffy growth curves were fitted to length‐at‐age data. Female von Bertalanffy parameters were L_∞ = 1036 mm L_F, k = 0·18, t₀ = ?1·64 and L₀ = 272 mm L_F. Males reached a smaller theoretical asymptotic length and had a higher growth coefficient (L_∞ = 782 mm L_F, k = 0·29, t₀ = ?1·43 and L₀ = 266 mm L_F). Maximum observed age was 17·9 years for females and 16·0 years for males. Annual deposition of growth increments was verified by marginal increment analysis and validated for age classes 2·5+ to 10·5+ years through recapture of 13 oxytetracycline‐injected specimens at liberty in the wild for 1–4 years. Length (L_F50) and age (A₅₀) at 50% maturity were 819 mm and 6·7 years for females, and 618 mm and 3·9 years for males. Both female and male S. tiburo in the WNA had a significantly higher maximum observed age, L_F50, A₅₀ and L_∞, and a significantly lower k and estimated L₀ than evident in the Gulf of Mexico (GOM). These significant differences in life‐history parameters, as well as evidence from tagging and genetic studies, suggest that S. tiburo in the WNA and GOM should be considered separate stocks.     

Reproductive cycle and fecundity of the bonnethead Sphyrna tiburo L. from the northwest Atlantic Ocean

The present study examined temporal changes in plasma sex hormone concentrations and the morphology and histology of reproductive organs in mature northwest Atlantic (NWA) bonnetheads Sphyrna tiburo L. to characterize reproductive cycle, breeding periodicity and fertility in this still poorly studied population. Progressive increases in testis width, epididymis head width, plasma testosterone (T) concentrations, and occurrence of mature spermatozoa were observed in male S. tiburo from June to September, demonstrating that spermatogenesis occurs during the summer. Nonetheless, increases in maximum follicle diameter, oviducal gland width, plasma 17β-estradiol and T concentrations, and occurrence of vitellogenic follicles were not observed in mature females until between October and April, demonstrating non-synchronous patterns of gametogenesis in males and females. Fresh copulatory wounds were observed in females collected during late September along with histological evidence for sperm presence in the oviducal gland between September and April, confirming a 6- to 7 month period of female sperm storage. Ovulation occurred between mid-April and early May in concert with increases in female plasma progesterone concentrations. Gestation occurred during a 4.5- to 5 month period between May and early September, and 97% of mature females collected during this period were gravid, indicating a highly synchronized, annual reproductive periodicity. Brood size was significantly correlated with maternal size and ranged from 1 to 13 pups with a mean ± S.D. of 8.1 ± 2.2, which was significantly lower than reported in Gulf of Mexico (GOM) populations. The occurrence of non-fertile offspring was observed in 17% of broods with a range of 1–7 non-fertile eggs present in individual females. Thus, as previously reported in GOM S. tiburo, this unusual form of infertility also appears to be prevalent in the NWA population and requires further study. This study has demonstrated meaningful differences in reproductive biology of these populations, emphasizing the need for region-specific approaches for population management.     

Temporal and latitudinal comparisons of reproductive parameters in a heavily exploited shark,the bonnethead,Sphyrna tiburo (L. 1758), in the southern Gulf of Mexico

In the southern Gulf of Mexico, the bonnethead shark, Sphyrna tiburo, is one of the most frequently captured species in landings of small-scale fisheries. Based on the analysis of two fishery-dependent sampling periods (1993–1994 and 2007–2014), this study aimed to determine reproductive parameters and identify temporal differences between the two time periods. In the first sampling period, 776 males and 352 females with a size range of 28.0–120.0 cm total stretched length (L_T) were analysed, and in the second sampling period, 387 males and 432 females with a size range of 28.0–122.0 cm L_T were analysed. The size at 50% maturity in the second sampling period was significantly different between sexes, 82.6 cm L_T for females and 73.8 cm L_T for males (no estimation was possible for the first sampling period). The size at 50% maternity was not different between sampling periods, 97.3 cm L_T for the first sampling period and 99.0 cm L_T for the second sampling period. Litter size varied from 3 to 19 embryos and the average was not statistically different in both periods, 10.1 (S.D. = 3.8) for the first sampling period and 11.3 (S.D. = 3.5) for the second sampling period. The female reproductive cycle is asynchronous, and it seems to be annual, with a gestation period of 5–6 months, and a consecutive ovarian cycle and gestation period. Temporal (between sampling periods) and latitudinal (southern Gulf versus northern regions) variations occur in the synchronicity of the reproductive cycle, temporal variation in the relationship between maternal length and litter size, and latitudinal variation in average size of mature sharks.     

Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation

There is growing interest in the mating systems of sharks and their relatives (Class Chondrichthyes) because these ancient fishes occupy a key position in vertebrate phylogeny and are increasingly in need of conservation due to widespread overexploitation. Based on precious few genetic and field observational studies, current speculation is that polyandrous mating strategies and multiple paternity may be common in sharks as they are in most other vertebrates. Here, we test this hypothesis by examining the genetic mating system of the bonnethead shark, Sphyrna tiburo, using microsatellite DNA profiling of 22 litters (22 mothers, 188 embryos genotyped at four polymorphic loci) obtained from multiple locations along the west coast of Florida. Contrary to expectations based on the ability of female S. tiburo to store sperm, the social nature of this species and the 100% multiple paternity observed in two other coastal shark species, over 81% of sampled bonnethead females produced litters sired by a single male (i.e. genetic monogamy). When multiple paternity occurred in S. tiburo, there was an indication of increased incidence in larger mothers with bigger litters. Our data suggest that sharks may exhibit complex genetic mating systems with a high degree of interspecific variability, and as a result some species may be more susceptible to loss of genetic variation in the face of escalating fishing pressure. Based on these findings, we suggest that knowledge of elasmobranch mating systems should be an important component of conservation and management programmes for these heavily exploited species.     

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.     

Gill lesions associated with Erpocotyle tiburonis (Monogenea: Hexabothriidae) on wild and aquarium-held bonnethead sharks (Sphyrna tiburo).

Gill lesions associated with infections of Erpocotyle tiburonis (Brooks, 1934) (Monogenea: Hexabothriidae) on wild bonnethead sharks (Sphyrna tiburo (L., 1758) (Carcharhiniformes: Sphyrinidae)) were compared with those on aquarium-held ones using light and scanning electron microscopy. Uninfected gill filaments had slender, triangular, smooth-surfaced lamellae and interlamellar water channels that were approximately equal in size. Four wild sharks were each infected by 3-11 widely separated adult E. tiburonis, and 1 of these sharks hosted a juvenile specimen. Lamellae flanking or touching adult E. tiburonis were pushed aside or bent, but were otherwise identical to those of uninfected filaments. Two aquarium-held sharks were each infected by hundreds of juvenile and adult E. tiburonis. In these sharks, lamellae near juveniles were pushed apart or bent, but were otherwise normal, whereas a thick, ragged-surfaced layer of hyperplastic epithelium both filled interlamellar water channels and partially or completely covered lamellae near adults. Results of this study suggest that the intense infections of E. tiburonis were facilitated by captivity and caused severe hyperplastic lesions that ultimately led to the death of the sharks by reducing or blocking the respiratory water flow over lamellae and thus reducing the exchange of gases and ions across the lamellar epithelium. In contrast, the wild sharks were infected by fewer worms and exhibited relatively minor lesions.     

Population structure and cryptic speciation in bonnethead sharks Sphyrna tiburo in the south‐eastern U.S.A. and Caribbean

Population structure and lineage diversification within a small, non‐dispersive hammerhead shark species, the bonnethead shark Sphyrna tiburo, was assessed. Sphyrna tiburo is currently described as one continuously distributed species along the Atlantic continental margins of North, Central and South America, but recent genetic analysis of an insular population (Trinidad) suggests the possibility of cryptic speciation. To address this issue S. tiburo were sampled at six sites along c. 6200 km of continuous, continental coastline and from one island location (Grand Bahama) across a discontinuity in their distribution (the Straits of Florida), in order to test if they constitute a single lineage over this distribution. A total of 1030 bp of the mitochondrial control region (CR) was obtained for 239 S. tiburo, revealing 73 distinct haplotypes, high nucleotide diversity (0·01089) and a pair of highly divergent lineages estimated to have separated 3·61–5·62 million years ago. Mitochondrial cytochrome oxidase I and nuclear internal transcribed spacer loci show the same pattern. Divergence is similar within S. tiburo to that observed between established elasmobranch sister species, providing further evidence of cryptic speciation. A global AMOVA based on CR confirms that genetic diversity is primarily partitioned among populations (Φ_ST = 0·828, P < 0·001) because the divergent lineages are almost perfectly segregated between Belize and North America–The Bahamas. An AMOVA consisting solely of the North American and Bahamian samples is also significantly different from zero (Φ_ST = 0·088, P < 0·001) and pairwise F_ST is significantly different between all sites. These findings suggest that S. tiburo comprises a species complex and supports previous research indicating fine population structure, which has implications for fisheries management and biodiversity conservation.     

Assessment of acid-base derangements among bonnethead (Sphyrna tiburo), bull (Carcharhinus leucas), and lemon (Negaprion brevirostris) sharks from gillnet and longline capture and handling methods

Blood gasses of wild bonnethead, bull, and lemon sharks were measured with the i-STAT clinical analyzer with the CG4+ cartridge immediately after capture; and again immediately prior to release after tagging, handling and morphometric measurements were taken. Relative reference ranges of post-capture status were established. Among species, stress response to capture was similar for all parameters; however, pH declined and lactate concentrations rose over time, indicating continued insult from capture and/or response to additional handling stress. pCO(2) rose faster for S. tiburo than for C. leucas, and lactate concentrations rose faster for S. tiburo than for N. brevirostris. All species caught in gillnets experienced lower pH and higher lactate concentrations than on longlines. Discriminant analysis justified the use of blood gas analysis to assess physiological stress induced by different capture methods. From these results, we recommend 1) that gear be monitored closely and sharks be removed immediately, or suboptimally, that gear is deployed for the shortest soak time possible; 2) longline over gillnet gear; and 3) extra caution with sensitive species (e.g., S. tiburo), which may include the administration of blood buffers and other therapeutics if a shark is beyond the limits of relative reference ranges reported here.     

New microsatellite loci for the endangered scalloped hammerhead shark, Sphyrna lewini

We isolated 15 microsatellite markers for the scalloped hammerhead shark, Sphyrna lewini. Loci were tested on 80 specimens of S. lewini from four Eastern Pacific samples. The number of alleles per locus ranged from 6 to 31 (mean = 14). Observed and expected levels of heterozygosity per locus ranged from 0.39 to 0.91 (mean = 0.70) and from 0.54 to 0.90 (mean = 0.76), respectively. No pairs of loci were in gametic disequilibrium after Bonferroni correction of α. One locus showed significantly lower heterozygosity than expected under Hardy–Weinberg proportions in two populations, possibly caused by null alleles.     

Baseline health parameters and species comparisons among free-ranging Atlantic sharpnose (Rhizoprionodon terraenovae), bonnethead (Sphyrna tiburo), and spiny dogfish (Squalus acanthias) sharks in Georgia, Florida, and Washington, USA

Sharks are of commercial, research, conservation, and exhibition importance but we know little regarding health parameters and population status for many species. Here we present health indicators and species comparisons for adults of three common wild-caught species: 30 Atlantic sharpnose sharks (Rhizoprionodon terraenovae) and 31 bonnethead sharks (Sphyrna tiburo) from the western Atlantic, and 30 spiny dogfish sharks (Squalus acanthias) from the eastern Pacific. All animals were captured during June-July 2009 and 2010. Median values and preliminary reference intervals were calculated for hematology, plasma biochemistry, trace nutrients, and vitamin A, E, and D concentrations. Significant differences, attributable to physiologic differences among the species, were found in the basic hematologic and plasma biochemistry variables. Significant species differences in arsenic and selenium plasma concentrations were found and appear to coincide with diet and habitat variability among these three species. Vitamin E was significantly higher in the bonnethead shark, again related to the foraging ecology and ingestion of plant material by this species. The Atlantic sharpnose had significantly higher vitamin A concentrations, supported by the higher proportion of teleosts in the diet. Vitamin D was below the limit of quantification in all three species. These preliminary reference intervals for health variables can be used to assess and monitor the population health and serve as indicators of nutritional status in these populations of wild elasmobranchs.     

The determinants of sexual segregation in the scalloped hammerhead shark,Sphyrna lewini

Synopsis Female scalloped hammerhead sharks move offshore at a smaller size than do males to form schools composed primarily of intermediate size female sharks. This movement results in smaller females feeding more on pelagic prey than do males and with greater predatory success. It is contended that this change in habitat causes females to grow more rapidly to reproductive size. Intermediate size females grow at a more rapid rate than males. Female scalloped hammerhead sharks mature at a size larger than males. For many elasmobranch species, females: (1) occupy a different habitat, (2) grow more rapidly prior to maturity and continue growth following maturation, (3) feed on different prey with increased feeding success, and (4) reproduce at a size larger than males. It is suggested that female segregation increases fitness, resulting in more rapid growth for the former sex. The females reach maturity at the larger size necessary to support embryonic young, yet similar age to males, matching the female reproductive lifetime to that of males.