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.     

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.     

Plasma steroid concentrations of adult male Atlantic sharpnose sharks, <Emphasis Type="Italic">Rhizoprionodon terraenovae,</Emphasis> in the northern Gulf of Mexico,with notes on potential long term shifts in reproductive timing

In previous literature it was proposed that Atlantic sharpnose sharks, Rhizoprionodon terraenovae, from the western Atlantic Ocean (WAO) population exhibited differences in their reproductive timing when compared to the northern Gulf of Mexico (GOM) population. The objective of the current study was to examine the reproductive cycle of mature male sharpnose sharks from the northern GOM population. Plasma testosterone (T) and estradiol (E₂) were measured from 76 mature male sharpnose sharks sampled from 1999 to 2001, and the gonadosomatic index (GSI) was determined for 53 additional mature males sampled from 2007-2008. Plasma T, E₂, and GSI exhibited similar cycles with peak values occurring in late spring (April/May) and lowest values occurring during the summer. These results suggest that male sharpnose sharks in the northern GOM are reproductively active one to two months earlier than previously reported, which now brings them into synchrony with the WAO population. Interestingly, this shift in reproductive timing corresponds with a 3.0°C (13.4%) increase in spring sea surface temperature (SST) from the Mississippi Sound over a 29 year period, which could translate into GOM male sharpnose sharks becoming reproductively active earlier in the year thus explaining the late spring peak in GSI.     

Aversive responses of captive sandbar sharks Carcharhinus plumbeus to strong magnetic fields

This experimental study focused on the possible deterrent effect of permanent magnets on adult sandbar sharks Carcharhinus plumbeus. Results showed that the presence of a magnetic field significantly reduced the number of approaches of conditioned C. plumbeus towards a target indicating that adult C. plumbeus can be deterred by strong magnetic fields. These data, therefore, confirm that the use of magnetic devices to reduce shark by‐catch is a promising avenue.     

Reproductive cycle of the blacknose shark Carcharhinus acronotus in the Gulf of Mexico

The reproductive periodicity of blacknose sharks Carcharhinus acronotus in the northern Gulf of Mexico was determined by examining reproductive tissues from specimens collected monthly from 2002 to 2005. Monthly changes in shell gland mass, right ovary mass and ovarian follicle diameter were assessed for 74 mature females. Temporal changes in testes mass, testes width and proportion of mature spermatocysts were examined for 64 mature males. Trends in female reproductive tissues suggested an annual peak in reproductive activity during June and July, while trends in male variables suggested an annual reproductive peak during May and June. Although male and female reproductive activity peaked in different months, a strong synchronicity existed between the proportion of mature spermatocysts and the diameter of the largest ovarian follicle. Based on these results, the mating season of blacknose sharks lasts from mid-May to July in the Gulf of Mexico. Maximum embryo sizes were observed in May, which suggested that partition occurs during late May or early June. Results indicate that blacknose sharks have a clearly defined annual cycle in the Gulf of Mexico. This conclusion is further supported by the complete absence of gravid females without vitellogenic ovarian follicles among all mature females examined.     

Reproductive cycle and gonadal development of the Atlantic sea urchin Arbacia punctulata in the Gulf of Mexico: changes in nutritive phagocytes in relation to gametogenesis

ABSTRACT

The annual reproductive cycle comprises steady gametogenic activities that synchronize gonadal maturation and spawning rhythms, which are important for aquatic organisms including marine echinoderms (Echinodermata, Echinoidea). In this study, we report the annual reproductive cycle, gonadal development, and changes in nutritive phagocytes (NPs, which accumulate nutrients in germ cells) in relation to gametogenesis of the Atlantic sea urchin (Arbacia punctulata, an edible echinoid) in the Gulf of Mexico. Monthly changes in gonadal development and maturation were observed morphologically and histologically. We calculated gonadosomatic index (GSI) and compared the stages of gonadal development in order to determine the NPs index, and characteristics of germ cells (eggs and sperm) during the annual reproductive cycle. According to GSI and histological analyses, gametogenic activities were classified into four stages of both sexes: mature (June–August), spent (September–November), recovery (December–March), and growing (April–May). The GSI values in both sexes were high during summer months. In males, testicular lobules were densely packed with sperm from June to August. In females, however, mature eggs first appeared in some ovaries in May, numerically increased from June to July, and decreased in August. During gametogenesis, on the other hand, NPs in both testes and ovaries were depleted from June to August. Collectively, our results suggest that the Atlantic sea urchin spawns during summer months in the Gulf of Mexico. This is the first report, to the best of our knowledge, on gonadal development and changes in NPs during the annual reproductive cycle of any Arbacia species in the Gulf of Mexico.     

Age and growth of the sandbar shark, Carcharhinus plumbeus, in Hawaiian waters through vertebral analysis

Age and growth estimates were determined for the sandbar shark, Carcharhinus plumbeus, from Oahu, Hawaii in the central Pacific Ocean. Age estimates were obtained through vertebral centra analysis of 187 sharks. We verified our age estimates through marginal increment analysis of centra and oxytetracycline marking methods of at liberty sandbar sharks. Sizes of sampled sharks ranged from 46 to 147 cm pre-caudal length. Four growth models were fitted to length-at-age data; two forms of the von Bertalanffy growth model, the Gompertz growth model, and a logistic growth model. Males and females exhibited statistically significant differences in growth, indicating that females grow slower and attain larger sizes than males. Growth parameter estimates revealed slower growth rates than previously estimated (based on captive specimens) for Hawaiian sandbar sharks. The von Bertalanffy growth model using empirical length-at-birth provided the best biological and statistical fit to the data. This model gave parameter estimates of L _∞ = 138.5 cm PCL and k = 0.12 year⁻¹ for males and L _∞ = 152.8 cm PCL, k = 0.10 year⁻¹ for females. Male and female sandbar sharks mature at approximately 8 and 10 years of age, respectively.     

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.     

Life history of the cownose ray, <Emphasis Type="Italic">Rhinoptera bonasus</Emphasis>, in the northern Gulf of Mexico,with comments on geographic variability in life history traits

Synopsis We determined age and growth, size at maturity, and fecundity for cownose rays, Rhinoptera bonasus, collected from the northern Gulf of Mexico. Vertebral age estimates ranged from 0+ to 18+ years for females and 0+ to 16+ years for males. Annual deposition of growth increments was verified with marginal increment analysis. Likelihood ratio tests indicated that the growth of the cownose ray was best described by a combined sexes Gompertz model. Median size at 50% maturity was determined to be 642 mm DW for males and 653 mm DW for females, or 4–5 years of age. Median pup size-at-birth was estimated to be 350 mm DW, with a gestation period of 11–12 months. In all cases, gravid females contained only one pup. Statistically significant differences were detected between growth curves for the Gulf of Mexico and the western Atlantic Ocean. Cownose rays in the Gulf of Mexico had lower estimates of DW_∞ and K, and a higher theoretical longevity than their conspecifics in the western Atlantic Ocean. Cownose rays in the Gulf of Mexico also attain maturity at a smaller size and earlier age than their counterparts in the western Atlantic Ocean.     

Human introduction or natural dispersion? Atlantic Ocean occurrence of the Indo‐Pacific whitetip reef shark Triaenodon obesus

Occurrence of multiple whitetip reef sharks Triaenodon obesus in the Atlantic Ocean is reported for the first time from near a sunken ferry off the Paraná coast in south‐eastern Brazil. This occurrence is hypothesized to have been caused by either a human introduction or a remarkably long oceanic displacement.     

Feeding habits of the tiger shark, <Emphasis Type="Italic">Galeocerdo cuvier,</Emphasis> in the northwest Atlantic Ocean and Gulf of Mexico

Tiger sharks, Galeocerdo cuvier, are apex predators that may structure marine communities through predation. Despite a large number of studies in other areas such as the Pacific Ocean, there are no quantitative data on the diet of tiger sharks in the northwest Atlantic Ocean and Gulf of Mexico. Diet was assessed from 169 tiger sharks by life stage, area, and environmental factors. Fifteen prey groups were identified, with teleosts, molluscs, birds, cephalopods, and reptiles being the predominant prey categories. There was an ontogenetic shift in diet, prey size and diversity. Molluscs were the most common prey in smaller sharks, while teleosts and reptiles became more important in the diet of larger sharks. Dietary overlap was significant by area (Gulf of Mexico vs Atlantic Ocean) and among all life stages except for young-of-the-year and adult tiger sharks. Juvenile tiger sharks also demonstrated selective feeding by targeting gastropod feet over ingesting the entire animal. While results were similar to feeding studies conducted on tiger sharks in other ocean basins, an understanding of area-specific trophic interactions is necessary to inform decision support tools for ecosystem-based approaches to management.     

Food habits and ontogenetic changes in the diet of the sandbar shark, Carcharhinus plumbeus, in Hawaii

The sandbar shark, Carcharhinus plumbeus, is a wide-ranging coastal species in tropical and temperate regions, and it is the most common species of shark in Hawaii, as in many locations where it occurs. Information on the diet and feeding habits of this species in the Pacific Ocean are extremely limited. For this study we quantified the diet of sandbar sharks in Hawaii based on records collected during the Hawaii Cooperative Shark Research and Control Program from 1967 to 1969. During this program a total of 565 stomachs were examined, of which 265 contained food. Sharks ranged in size from 59 to 190 cm total length. Teleosts were the most common prey group, but both cephalopods and crustaceans also occurred frequently. Ontogenetic changes in diet of sandbar sharks were apparent, with crustaceans forming a greater proportion of the diet of smaller sharks. Both cephalopods and elasmobranchs increased in importance with increasing shark size. Prey diversity also increased with size, with large, mobile, and reef prey species found more commonly in the diet of larger sharks. Mature male and female sharks appeared to segregate by depth, though major differences in the diet between the sexes were not apparent. However, there was some evidence of dietary differences between sharks caught in different depths and seasons. The results of this study suggest that sandbar sharks in Hawaii and throughout the world, are primarily piscivores, but also consume a variety of invertebrate prey, and that their diet varies with geographical location and stage of development.     

Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii

We tested for presence or absence of multiple paternity in single litters from each of three congeneric shark species in Hawaii: the sandbar shark, Carcharhinus plumbeus, bignose shark, Carcharhinus altimus, and Galapagos shark, Carcharhinus galapagensis. Based on eight polymorphic microsatellite loci, we excluded paternity by a single sire in sandbar and bignose sharks, but could not exclude a single sire for the litter from the Galapagos shark. This study doubles the number of shark species tested for multiple paternity, and is the first demonstration of multiple paternity in sandbar and bignose sharks.     

Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of western Atlantic populations coupled with recent Pacific dispersal

Although many coastal shark species have widespread distributions, the genetic relatedness of worldwide populations has been examined for few species. The blacktip shark, (Carcharhinus limbatus), inhabits tropical and subtropical coastal waters throughout the world. In this study, we examined the genetic relationships of blacktip shark populations (n = 364 sharks) throughout the majority of the species' range using the entire mitochondrial control region (1067-1070 nucleotides). Two geographically distinct maternal lineages (western Atlantic, Gulf of Mexico, and Caribbean Sea clades, and eastern Atlantic, Indian, and Pacific Ocean clades) were identified and shallow population structure was detected throughout their geographic ranges. These findings indicate that a major population subdivision exists across the Atlantic Ocean, but not the Pacific Ocean. The historical dispersal of this widespread, coastal species may have been interrupted by the rise of the Isthmus of Panama. This scenario implies historical dispersal across the Pacific Ocean (supported by the recovery of the same common haplotype from the Philippines, Hawaii, and the Gulf of California reflecting recent/contemporary dispersal abilities) and an oceanic barrier to recent migration across the Atlantic. Genetic structure within the eastern Atlantic/Indo-Pacific (Phi(ST) = 0.612, P < 0.001) supports maternal philopatry throughout this area, expanding previous western Atlantic findings. Eastern Atlantic/Indo-Pacific C. limbatus control region haplotypes were paraphyletic to Carcharhinus tilstoni haplotypes in our maximum-parsimony analysis. The greater divergence of western Atlantic C. limbatus than C. tilstoni from eastern Atlantic/Indo-Pacific C. limbatus reflects the taxonomic uncertainty of western Atlantic C. limbatus.     

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.     

Seasonal foraging movements and migratory patterns of female Lamna ditropis tagged in Prince William Sound, Alaska

Conventional and electronic tags were used to investigate social segregation, distribution, movements and migrations of salmon sharks Lamna ditropis in Prince William Sound, Alaska. Sixteen salmon sharks were tagged with satellite transmitters and 246 with conventional tags following capture, and were then released in Prince William Sound during summer 1999 to 2001. Most salmon sharks sexed during the study were female (95%), suggesting a high degree of sexual segregation in the region. Salmon sharks congregated at adult Pacific salmon Oncorhynchus spp. migration routes and in bays near Pacific salmon spawning grounds in Prince William Sound during July and August. Adult Pacific salmon were the principal prey in 51 salmon shark stomachs collected during summer months in Prince William Sound, but the fish appeared to be opportunistic predators and consumed sablefish Anoplopoma fimbria, gadids, Pacific herring Clupea pallasi, rockfish Sebastes spp. and squid (Teuthoidea) even when adult Pacific salmon were locally abundant. As Pacific salmon migrations declined in late summer, the salmon sharks dispersed; some continued to forage in Prince William Sound and the Gulf of Alaska into autumn and winter months, while others rapidly moved south‐east thousands of kilometres toward the west coasts of Canada and the U.S. Three movement modes are proposed to explain the movement patterns observed in the Gulf of Alaska and eastern North Pacific Ocean: ‘focal foraging’ movements, ‘foraging dispersals’ and ‘direct migrations’. Patterns of salmon shark movement are possibly explained by spatio‐temporal changes in prey quality and density, an energetic trade‐off between prey availability and water temperature, intra‐specific competition for food and reproductive success. Transmissions from the electronic tags also provided data on depth and water temperatures experienced by the salmon sharks. The fish ranged from the surface to a depth of 668 m, encountered water temperatures from 4·0 to 16·8° C and generally spent the most time above 40 m depth and between 6 and 14° C (60 and 73%, respectively).     

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.     

Reproductive and population parameters of spiny dogfish Squalus acanthias in the south‐western Atlantic Ocean

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 (L_T) and females from 235 to 925 mm L_T. The size at maturity of females (651 mm) was significantly greater than that of males (565 mm). The maximum proportion of mature individuals (P_max) 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 P_max 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.     

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.     

Re-evaluation of reproductive cycle and fecundity of finetooth sharks Carcharhinus isodon (Valenciennes 1839) from the Northwest Atlantic Ocean,with new observations on ovarian cycle and reproductive endocrinology of biennially reproducing sharks

To provide updated information on life history for improved fishery management, the reproductive cycle of the finetooth shark Carcharhinus isodon from Northwest Atlantic (NWA) populations was investigated by examining temporal changes in morphology and histology of reproductive organs. Changes in plasma concentrations of gonadal sex hormones in relation to reproductive stage were also examined. Increases in testis width, epididymis head width, plasma testosterone concentrations and occurrence of mature spermatozoa were observed in male sharks between December and April, suggesting a seasonal pattern in reproduction that culminates with copulatory activity in May. Increases in maximum follicular diameter, oviducal gland width, plasma 17β-estradiol concentrations and occurrence of vitellogenic follicles were observed in non-pregnant female sharks during the same time period along with the occurrence of newly pregnant females in May, demonstrating strong synchronicity between male and female reproductive cycles. Pregnant females bearing full-term embryos were also observed in May, indicating that parturition occurs between mid-May and early June and gestation requires 12 months. Only transient temporal changes in follicle size and oviducal gland width were observed in pregnant females, indicating that reproductive periodicity is biennial; nonetheless, a single female exhibiting signs of concurrent vitellogenesis and pregnancy was observed. Mean brood size ± S.D. was 3.9 ± 0.9 offspring/female. Fecundity was not significantly correlated with female size, in part due to an unexpectedly high rate of early embryo mortality, which occurred in 11% of pregnant females, and was more common in larger individuals. Changes in ovarian activity during mid-pregnancy were observed, suggesting possible roles for the ovary in regulating some aspects of early to mid-gestation. This study confirms that earlier characterizations of the reproductive cycle and fecundity in NWA finetooth sharks remain valid for use in fishery management. This study also highlights unusual features of finetooth shark pregnancy (e.g., early embryo death, mid-pregnancy changes in ovarian function) that may have broader relevance to understanding elasmobranch reproduction.