Reproductive biology of Carcharhinus acronotus in the coastal waters of South Carolina

The reproductive biology of blacknose sharks Carcharhinus acronotus in the western North Atlantic Ocean was studied by examining specimens collected in the coastal waters of South Carolina. Males begin the maturation process between 875 and 910 mm fork length ( L _F), as indicated by the presence of functional claspers and siphon sacs. The presence of vitellogenic oocytes and developing oviducal glands and uteri indicated that females begin to mature at c . 870 mm L _F. Length at which 50% of the population reached maturity was 896 and 964 mm L _F, equivalent to 4·3 and 4·5 years, for males and females, respectively. Gonado‐somatic indices suggested that spermatogenesis and vitellogenesis began after December. Mating took place during the end of May and the beginning of June. Fertilization occurred during late June and early July, suggesting that female blacknose sharks were capable of sperm storage. Based on the timing of fertilization and occurrence of females carrying near‐term pups in late May and early June, the gestation period for blacknose sharks was c . 11 months. Female blacknose sharks reproduced biennially based on the absence of vitellogenic oocytes in near‐term females and there being no indication of vitellogenesis in postpartum females. Male blacknose sharks were capable of reproducing annually as indicated by turgid genital ducts, which were observed in all mature males collected during late May and early June.     

Age and growth of the blacknose shark, <Emphasis Type="Italic">Carcharhinus acronotus</Emphasis>, in the western North Atlantic Ocean with comments on regional variation in growth rates

We examined the age and growth of the blacknose shark, Carcharhinus acronotus, in the western North Atlantic Ocean by obtaining direct age estimates using vertebral centra. We verified annual deposition of growth increments with marginal increment analysis and validated it by analyzing vertebrae marked with oxytetracycline from a female blacknose shark held in captivity. Von Bertalanffy growth parameters indicated that female blacknose sharks have a lower growth constant (k), a larger theortical maximum size (L), and are longer lived than males. We compared these growth parameters for blacknose sharks in the western North Atlantic Ocean to growth parameters for blacknose sharks collected in the eastern Gulf of Mexico to test for differences between regions. Females in the western North Atlantic Ocean have a significantly lower L, lower k, and a higher theoretical longevity than females in the Gulf of Mexico. Males in the western North Atlantic Ocean have a higher L<>, lower k, and higher theoretical longevity than males in the Gulf of Mexico. The significant differences between these life history parameters for blacknose sharks suggest that, when possible, future management initiatives concerning blacknose sharks should consider managing the populations in the western North Atlantic and the Gulf of Mexico as separate stocks.     

Age and growth estimates of the bull shark,Carcharhinus leucas,from the northern Gulf of Mexico

Synopsis Length at age and growth rates for 59 bull sharks, Carcharhinus leucas, collected from the northern Gulf of Mexico were estimated from the band patterns formed seasonally in the vertebral centra. The combined age at length data for both sexes were applied to a von Bertalanffy growth model producing parameter estimates of L = 285 cm TL, K = .076, t₀ = –3.0 yr. Lengths at age for males and females were similar except that males did not attain as great a length as females. Growth was apparently slow and varied among individuals, but in general, was estimated to be 15–20 cm yr^–1 for the first five years, 10 cm yr^–1 for years 6–10, 5–7 cm yr^–1 for years 11–16, and less than 4–5 cm yr^–1 thereafter. Males mature at 210–220 cm TL or 14–15 yr of age; females mature at>225 cm TL or 18+ yr of age. The largest male (245 cm TL) was 21.3 yr old; the largest female (268 cm TL) was 24.2 yr old.     

Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico

To investigate patterns of polyandry in the sandbar shark (Carcharhinus plumbeus), 20 pregnant females were sampled from the western North Atlantic and Gulf of Mexico. Five species-specific microsatellite markers were used to genotype each shark and its litter. Of 20 litters, 17 (85%) were shown to have multiple sires. In multiply sired litters, the estimated minimum number of sires ranged from two to five with an average of 2.3 males per litter. Regression analysis did not demonstrate a significant relationship between female reproductive success and female body size or sire number and female body size. There was a high incidence of reproductive skew noted in litters, and two groups of males with significantly different mean reproductive success were observed. Analyses using Bateman's principles suggest that there is less direct benefit for females that acquire multiple mates than for males who bias paternity within litters. In light of past morphological and behavioural studies, these data suggest that patterns of polyandry in elasmobranchs may be determined by coercive mating, and that breeding behaviour has likely evolved in the context of sexual conflict.     

Reproductive biology,multiple paternity and polyandry of the bull shark Carcharhinus leucas

To improve understanding of bull shark Carcharhinus leucas reproductive biology, we analysed reproductive traits from 118 bull sharks caught along Reunion Island coasts (Western Indian Ocean), including 16 gravid females. Specific microsatellite loci were used to investigate the frequency of multiple paternity. Males and females reached maturity at c. 234 cm and 257 cm total length (L_T), respectively, and litter sizes ranged from 5 to 14 embryos. Analysis of the 16 litters collected in various months of the year indicated that parturition occurs between October and December, with a size at birth c. 60–80 cm L_T and that the gestation period is probably c. 12 months. Assuming a 1 year resting period and a period of sperm storage (4–5 months) between mating (in June–September) and fertilisation, the reproductive cycle of bull sharks at Reunion Island would be biennial. At least 56.25% of the litters investigated were polyandrous, sired by 2–5 males. Several males that each sired several litters conceived during the same or distinct mating seasons were detected, suggesting both a seasonal aggregation of sharks to mate and some male fidelity to mating site. Altogether, these findings provide valuable information for both shark risk management and conservation of the species in the Western Indian Ocean.     

Histological and morphological aspects of reproduction in the sandbar shark Carcharhinus plumbeus in the U.S. south‐eastern Atlantic Ocean and Gulf of Mexico

The reproduction of the sandbar shark Carcharhinus plumbeus in the U.S. south‐eastern Atlantic Ocean including the Gulf of Mexico was examined using a combination of histological and morphological characteristics of C. plumbeus collected through fishery‐dependent and ‐independent sampling programmes (n = 1,567). Indices of maturity were constructed using measurements of gonads, reproductive tracts and claspers, and sandbar sharks exhibited 50% maturity sizes of 140 and 148 cm fork length for males and females respectively. Gonado‐somatic indices and variation in reproductive tract condition were used to determine seasonal trends in reproduction of mature C. plumbeus. Sandbar sharks have discrete seasonal reproductive cycles in which males produce sperm from January to May with a peak in May and females develop eggs from January to May with ovulation occurring in June. Females were shown to exhibit a >2 year reproductive cycle. Embryonic development was assessed through measurements of masses and lengths of uterine contents. Gestation was 12 months, from July to the following June, with parturition in late June. This research highlights a difference from previously reported data on the periodicity of female reproduction in C. plumbeus in the U.S. south‐eastern Atlantic Ocean and Gulf of Mexico, which may have major effects on future C. plumbeus stock management.     

Contemporary population structure and post‐glacial genetic demography in a migratory marine species,the blacknose shark,Carcharhinus acronotus

Patterns of population structure and historical genetic demography of blacknose sharks in the western North Atlantic Ocean were assessed using variation in nuclear‐encoded microsatellites and sequences of mitochondrial (mt)DNA. Significant heterogeneity and/or inferred barriers to gene flow, based on microsatellites and/or mtDNA, revealed the occurrence of five genetic populations localized to five geographic regions: the southeastern U.S Atlantic coast, the eastern Gulf of Mexico, the western Gulf of Mexico, Bay of Campeche in the southern Gulf of Mexico and the Bahamas. Pairwise estimates of genetic divergence between sharks in the Bahamas and those in all other localities were more than an order of magnitude higher than between pairwise comparisons involving the other localities. Demographic modelling indicated that sharks in all five regions diverged after the last glacial maximum and, except for the Bahamas, experienced post‐glacial, population expansion. The patterns of genetic variation also suggest that the southern Gulf of Mexico may have served as a glacial refuge and source for the expansion. Results of the study demonstrate that barriers to gene flow and historical genetic demography contributed to contemporary patterns of population structure in a coastal migratory species living in an otherwise continuous marine habitat. The results also indicate that for many marine species, failure to properly characterize barriers in terms of levels of contemporary gene flow could in part be due to inferences based solely on equilibrium assumptions. This could lead to erroneous conclusions regarding levels of connectivity in species of conservation concern.     

Reproductive aspects of the Atlantic angel shark Squatina dumeril in the southern Caribbean Sea

The maturity and reproduction of the Atlantic angel shark Squatina dumeril were assessed using 77 females (29·2–110·4 cm total length; L_T) and 269 males (58·7–108·2 cm L_T) harvested by artisanal gillnetters off Venezuela. The biased sex ratio implied segregation or sex‐specific gear selectivity. Based on the development of the reproductive tract, 50% L_T at sexual maturity (L_T50, mean ± s.e .) for females and males were estimated at 86·14 ± 0·64 and 81·55 ± 0·12 cm, respectively. Uterine fecundity ranged between one and six and with a maximum embryo size of 25·7 cm L_T. Gravid females were observed from August to December, including those close to parturition and while the gestation period was not confirmed, the size of ovarian follicles among some specimens implied protraction. The low fecundity of the species supports close monitoring of catches.     

Parthenogenesis in a large‐bodied requiem shark,the blacktip Carcharhinus limbatus

Genetic evidence is provided for parthenogenesis in a large‐bodied shark, the blacktip Carcharhinus limbatus, from the speciose and commercially important family Carcharhinidae, the first verified case of asexual development in this lineage and only the second for any chondrichthyan. The parthenogenetic embryo exhibited elevated homozygosity relative to its mother, indicating that automictic parthenogenesis is the most likely mechanism. Although this finding shows that parthenogenesis is more common and widespread in sharks than previously realized and supports the early existence of parthenogenetic abilities in vertebrates, the adaptive significance of automixis in these ancient fishes remains unclear.     

Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea

Abstract We investigated the genetic structure of blacktip shark (Carcharhinus limbatus) continental nurseries in the northwestern Atlantic Ocean, Gulf of Mexico, and Caribbean Sea using mitochondrial DNA control region sequences and eight nuclear microsatellite loci scored in neonate and young-of-the-year sharks. Significant structure was detected with both markers among nine nurseries (mitochondrial PhiST = 0.350, P < 0.001; nuclear PhiST = 0.007, P < 0.001) and sharks from the northwestern Atlantic, eastern Gulf of Mexico, western Gulf of Mexico, northern Yucatan, and Belize possessed significantly different mitochondrial DNA haplotype frequencies. Microsatellite differentiation was limited to comparisons involving northern Yucatan and Belize sharks with nuclear genetic homogeneity throughout the eastern Gulf of Mexico, western Gulf of Mexico, and northwestern Atlantic. Differences in the magnitude of maternal vs. biparental genetic differentiation support female philopatry to northwestern Atlantic, Gulf of Mexico, and Caribbean Sea natal nursery regions with higher levels of male-mediated gene flow. Philopatry has produced multiple reproductive stocks of this commercially important shark species throughout the range of this study.     

Reproductive Biology of the Smooth Dogfish, Mustelus canis, in the Northwest Atlantic Ocean

Shark populations tend to be highly vulnerable to overexploitation due to low fecundity and slow growth rates. Recent fishing pressure on the smooth dogfish in the northwest Atlantic has created a necessity for more information about their basic biology. Length and age at maturity, fecundity, and reproductive season were estimated. Total length at 50% maturity was 102cm for females, and 86cm for males. The majority of females were mature at age 4 or 5, and all males were mature at 2 or 3 years of age. Females had an 11–12 month gestation with parturition occurring in May, ovulation occurring between May and July likely in late May and early June, and mating occurring between May and September. Fecundity ranged between 3 and 18 pups per litter, and was positively related to length and age, with a mean of 9.53 pups per litter. Sperm was found in the terminal zone of the oviducal gland of females throughout the year.     

The behavioural role of pit organs in the epaulette shark

Epaulette sharks Hemiscyllium ocellatum in three treatments, pit organs (free neuromasts) ablated, sham-operated and normal ( n  = 8 for each treatment), showed a significant preference for facing upstream in a flume ( P  < 0·05). There were no significant differences in the mean angles or angular variances among treatments. Individuals with ablated pit organs, however, spent significantly less time moving around than controls ( P  < 0·05), suggesting that pit organs contributed to motivation for activity. Pit organs do not appear to make an important contribution to rheotaxis in H. ocellatum . It is suggested that this may be due to structural differences in the pit organs of H. ocellatum compared with other species.     

Histology of dart tag insertion sites in the epaulette shark

Samples of dermal and epidermal tissues of epaulette sharks Hemiscyllium ocellatum were examined histologically to assess damage caused by tagging. Tissues from around tag sites were removed at time intervals ranging from 100 min to 284 days post-tagging. These samples showed acute and chronic responses to tagging. Acute responses consisted of localized tissue breakdown and haemorrhaging, and occurred within the first few hours after tag insertion. At 10 h post-tagging, an intermediate response was apparent. This phase was characterized by further haemorrhaging and red and white blood cell movement into the wound area. The chronic response observed in the 10–284-day post-tagging samples was characterized by fibrous tissue formation to sequester the tag. This tissue presumably protects the adjacent musculature from further trauma produced by movement of the tag and provides a continuous barrier between the internal and external milieu. Tissue repair appeared to progress consistently in all specimens and no secondary infections at the tag site were seen. Tagging produced only localized tissue disruption and did not appear to be detrimental to the long term health of individual sharks. Our findings show that spaghetti style dart tagging is an acceptable method for marking individuals (40–75+ cm total length) of this species.     

Distribution, Movements and Growth of Young Sandbar Sharks, Carcharhinus Plumbeus, in the Nursery Grounds of Delaware Bay

During the spring and summer months of 1995, 1996 and 1997, gillnet and longline surveys were conducted in conjunction with tag and recapture experiments to outline spatial and seasonal distribution of young sandbar sharks, Carcharhinus plumbeus, in Delaware Bay for essential fish habitat mapping, to assess abundance of young sandbar sharks, and to quantify growth during the summer nursery season. Sandbar sharks (n = 943) ranging from 40 to 120cm fork length (48 to 130cm total length) were captured; yearly totals were 199, 314 and 430 in 1995, 1996 and 1997, respectively. Individuals were captured between June and October in water temperatures ranging from 15.4° to 28.5°C and salinities ranging from 22.8 to 30.3 ppt. Presence of neonates and catch per unit effort data indicate that pupping begins in late June near the southwestern coast of the Bay. Juveniles were present from early June through September and their spatial distribution in the Bay appeared uniform. Of 782 sandbar sharks tagged and released during the three years, 50 were recaptured. Mean distance from tag to recapture location and mean days-at-liberty of sandbar sharks recaptured in Delaware Bay during the year of tagging were 10km and 18 days, respectively. Some sharks were recaptured as far as 957km from the release location. Length distributions show young-of-the-year sandbar sharks grow about 2–3cm in length during the nursery season.     

Reproductive biology of the milk shark Rhizoprionodon acutus and the bigeye houndshark Iago omanensis in the coastal waters of Oman

Female Rhizoprionodon acutus were found to mature between 62 and 74 cm total length ( L _T) whereas males matured between 63 and 71 cm L _T. The L _T at 50% maturity was 64·3 cm for females and 64·7 cm for males. Litter size varied from one to six embryos, and was positively correlated with maternal L _T. Female embryos outnumbered males by a ratio of 2·3:1. The size at birth was c . 37 cm L _T. Full‐term embryos and post‐partum females were observed during all seasons although their occurrence was highest in spring. Spermatozoa were rarely recorded in the oviducal gland, indicating that this species does not store sperm. It was not possible to generate maturity curves for Iago omanensis but it was evident that females matured by the time they reached 35 cm and males were mature by 31 cm L _T. This species displayed a clearly defined reproductive cycle with parturition occurring primarily in spring, after a gestation period of c . 1 year. Maximal embryo size was 19 cm L _T while maximal litter size was 24 embryos. The oviducal gland appeared to act as a seminal receptacle and it appeared that females may utilize these stores by not mating every year.     

Characterization of large basking shark Cetorhinus maximus aggregations in the western North Atlantic Ocean

Cetorhinus maximus aggregations recorded during extensive aerial survey efforts off the north‐eastern United States between 1980 and 2013 included aggregations centring on sightings with group sizes of at least 30 individuals. These aggregations occurred in summer and autumn months and included aggregation sizes of up to 1398 individuals, the largest aggregation ever reported for this species. The aggregations were associated with sea surface temperatures of 13–24° C and chlorophyll‐a concentrations of 0·4–2·6 mg m^?3 and during one aggregation, a high abundance of zooplankton prey was present. Photogrammetric tools allowed for the estimation of total body lengths ranging between 4 and 8 m. Characterization of these events provides new insight into the potential biological function of large aggregations in this species.     

Age and growth of Carcharhinus leucas in the northern Gulf of Mexico: incorporating variability in size at birth

Age and growth rates of bull shark Carcharhinus leucas[n = 255; 555–2230 mm fork length (L_F)] from the northern Gulf of Mexico were estimated from ring counts on vertebral sections collected from fishery‐dependent and ‐independent surveys. Two growth models were fitted to observed data: the von Bertalanffy growth model (VBGM) with t₀ as the third parameter and a modified version of the VBGM using a fixed size‐at‐birth intercept as the third parameter. To address the variability in size‐at‐birth, a Monte Carlo simulation was incorporated into the size‐at‐birth intercept. The sex‐specific growth models were not significantly different, allowing a sexes combined model to be generated. The traditional VBGM predicted a theoretical maximum size (L_∞) of 3007·1 mm L_F, a growth coefficient (K) of 0·042 year^?1 and a theoretical age at zero length (t₀) of –6·844 years. The modified VBGM with a fixed size‐at‐birth intercept of 565 mm L_F predicted an L_∞ of 2289·2 mm L_F and a K value of 0·089 year^?1. When comparing model estimates to previously published information, the traditional VBGM predicted a significantly lower theoretical maximum size and a higher growth coefficient than those produced using data collected during the 1980s. Overall, results obtained using the VBGM with a fixed size‐at‐birth produced more biologically realistic parameters than that of the VBGM with t₀. The Monte‐Carlo simulation incorporating variability in size‐at‐birth produced similar results to the VBGM using a fixed size‐at‐birth. This study provides the first attempt to incorporate variability at size‐at‐birth and provide measurements of variability around the individual parameter estimates for an elasmobranch.     

Reproductive aspects of the Atlantic angel shark Squatina dumeril

Atlantic angel sharks Squatina dumeril were collected by fishery‐dependent and independent trawls from 2002 to 2008 for reproductive analysis. Female S. dumeril have only one functional ovary (left), with an average litter size of seven pups. The reproductive cycle is at least biennial, though the seasonality of vitellogenesis could not be determined. Gestation is c. 12 months, and embryo data support a seasonal trend in reproduction, with parturition occurring in the spring months (February to June). Mature male S. dumeril have spines on the outer margins of their pectoral fins, and there is an apparent peak in gonad size in the spring. The total length at which 50% of the population is mature is 85·8 and 92·9 cm for females and males, respectively.     

Isolation and characterization of five dinucleotide microsatellite loci in the sandbar shark,Carcharhinus plumbeus

Five dinucleotide markers were isolated and optimized from a microsatellite‐enriched genomic library obtained from the sandbar shark, Carcharhinus plumbeus. Genotypic distributions of all markers were found to be in conformance with the expectations of Hardy–Weinberg equilibrium with four to 39 alleles present per locus. We amplified these loci in two female sharks and their litters. A maternal allele was recovered at each locus in all progeny indicating reliable amplification. More than two paternal alleles were recovered across both litters indicating genetic polyandry. Additionally, these markers were amplified across 10 carcharhiniform species to examine their utility in other studies.