Polymorphic microsatellite markers for studies of the conservation and reproductive genetics of imperilled sand tiger sharks (Carcharias taurus)

We report on the isolation of eight microsatellites from the sand tiger shark, Carcharias taurus, using an enrichment protocol. All loci, with the exception of Cta45–183, were in Hardy–Weinberg equilibrium. Loci exhibited three to 15 alleles, and observed and expected heterozygosities of 0.095–1.000 and 0.284–0.924, respectively. An additional marker (Iox‐12) developed from a shortfin mako library was variable in sand tigers. These markers will be used to examine population genetics and mating patterns of this imperilled species.     

Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic

Tiger sharks (Galeocerdo cuvier) are a wide ranging, potentially keystone predator species that display a variety of horizontal movement patterns, making use of coastal and pelagic waters. Far less, however, is known about their vertical movements and use of the water column. We used pop‐up satellite archival tags with two data sampling rates (high rate and standard rate tags) to investigate the vertical habitat use and diving behavior of tiger sharks tagged on the Puerto Rico–Virgin Islands platform and off Bermuda between 2008 and 2009. Useable data were received from nine of 14 sharks tagged, tracked over a total of 529 days. Sharks spent the majority of their time making yo‐yo dives within the upper 50 m of the water column and considerable time within the upper 5 m of the water column. As a result, sharks typically occupied a narrow daily temperature range (~2°C). Dives to greater than 200 m were common, and all sharks made dives to at least 250 m, with one shark reaching a depth of 828 m. Despite some similarities among individuals, a great deal of intraspecific variability in vertical habit use was observed. Four distinct depth distributions that were not related to tagging location, horizontal movements, sex, or size were detected. In addition, similar depth distributions did not necessitate similar dive patterns among sharks. Recognition of intraspecific variability in habitat use of top predators can be crucial for effective management of these species and for understanding their influence on ecosystem dynamics.     

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.     

Age and length at maturity of the female spiny dogfish,Squalus acanthias,in the Strait of Georgia,British Columbia,Canada

Synopsis A total of 3068 female spiny dogfish were examined to determine the age and length at maturity. The median age at maturity for females was 35.5 years with 95% confidence limits between 35.0 and 35.9 years. It was found that slower growing dogfish tended to mature at a smaller size. A deterministic model incorporating fecundity, growth and reproduction was used to examine the reproductive style of spiny dogfish. The age at maturity reported corresponds to the level that theoretically maximizes lifetime reproductive output for a cohort.     

Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes

Summary How do organisms adapt to the differences in temperature and length of the growing season that occur with latitude? Among Atlantic silversides (Menidia menidia) along the east coast of North America, the length of the first growing season declines by a factor of about 2.5 with increasing latitude. Yet body size at the end of the first growing season does not decline. High-latitude fish must, therefore, grow faster within the growing season than do low-latitude fish. This geographical pattern has a genetic basis. Laboratory experiments on fish from six different locations revealed a latitudinal gradient in the capacity for growth (i.e., maximum growth potential). In two subsequent experiments using fish from Nova Scotia (NS), New York (NY) and South Carolina (SC) that had been separately reared in a common environment for several generations, differences in growth rate among populations were highly significant. The rank order was NS>NY>SC, but the difference among populations depended on temperature. High-latitude fish outperformed those from low latitudes primarily at the high temperatures that low-latitude fish would be expected to experience most often in nature. These results suggest that instead of being adapted for growth at low temperatures, fish from high latitudes are adapted for rapid elevation of growth rate during the brief interval of the year when high temperatures occur. Selection on growth rate results from sizedependent winter mortality: the importance to winter survival of being large increases with latitude but the length of the growing season simultaneously decreases. The end result is countergradient variation in growth rate, a phenomenon that may be much more widespread than currently recognized.     

Food habits of the smooth dogfish, Mustelus canis, dusky shark, Carcharhinus obscurus, Atlantic sharpnose shark, Rhizoprionodon terraenovae, and the sand tiger, Carcharias taurus, from the northwest Atlantic Ocean

Diet and feeding habits of the smooth dogfish, Mustelus canis, Atlantic sharpnose, Rhizoprionodon terraenovae, dusky, Carcharhinus obscurus, and the sand tiger, Carcharias taurus sharks, were investigated through analysis of stomach contents. Diet in M. canis was relatively homogeneous and was dominated by crustaceans, consisting mostly of rock crabs, Cancer irroratus. Diet in R. terraenovae was more heterogeneous and consisted largely of crustaceans and teleosts, in similar levels of prey importance. Use of cumulative prey curves as a measure of precision indicated that data were insufficient to fully describe the diets of C. obscurus and C. taurus. Nonetheless, these data suggested that both species are generalized feeders and consume a variety of teleost and elasmobranch prey. Further studies are necessary to fully characterize diet in these two species.     

A phenotypic trade-off between previous growth and present fecundity in round sardinella <Emphasis Type="Italic">Sardinella aurita</Emphasis>

The decision of how to allocate surplus energy to reproduction and growth can have important effects on fish population dynamics as well as on other life history traits. The natural examples on the interrelationship between maternal growth and number of offspring produced in fishes are scarce. We tested the hypothesis that these traits are competing for resources by estimating maternal previous growth decisions, using back-calculation, and present reproduction, expressed as absolute fecundity, of female round sardinella (Sardinella aurita) in the northeastern Mediterranean Sea. Despite the overall increasing trend of fecundity with age, individual fecundity was negatively related to individual specific growth rate between the most recent annulus formation and spawning within ages. A decreasing trend between previous growth rate and present fecundity emerged, showing that round sardinella allocate increasingly less energy to growth with age and more into reproduction and that the previous growth decisions determine present fecundity.     

Metal concentrations and metallothionein metal detoxification in blue sharks,Prionace glauca L. from the Western North Atlantic Ocean

BackgroundElasmobranchs are particularly vulnerable to environmental metal contamination, accumulating these contaminants at high rates and excreting them slowly. The blue shark Prionace glauca L. is one of the most heavily fished elasmobranchs, although information regarding metal contamination and detoxification in this species is notably lacking.MethodsBlue sharks were sampled in the western North Atlantic Ocean, in offshore waters adjacent to Cape Cod, Massachusetts. Total and metallothionein-bound liver and muscle metal concentrations were determined by inductively coupled plasma mass spectrometry (ICP-MS), metallothionein detoxification and oxidative stress endpoints were determined by UV–vis spectrophotometry.ResultsMetallothionein detoxification occurred for As, Cd, Cs, Cu, Hg, Pb, Se, Ti and Zn in liver, and for As, Cd, Cs, Pb, Se, and Zn in muscle, while reduced glutathione defenses seem to be related to Co and Zn exposure.ConclusionThis is the first report for several metals (Ag, Co, non-radioactive Cs, Sb, Ti and V) for this species, which will aid in establishing baseline elemental data for biomonitoring efforts, health metrics, and conservation measures.     

Early life-history dynamics of Caribbean coral species on artificial substratum: the importance of competition, growth and variation in life-history strategy

The development of a coral community was monitored for 6 years (1998–2004) on 46 m² of artificial settlement substrate in Curaçao, Netherlands Antilles. Growth and survival of recruits (n=1385) belonging to 16 different species were quantified in relation to characteristics of the benthic community developing around them. The early life history dynamics (i.e. growth rate, growth strategy and survival) of corals differed among species although these differences were small for species occupying similar habitats (i.e. underside versus topside of substratum). In contrast to recruit survival, juvenile growth rates were highly variable and unrelated to benthic community structure, at least at the scale of this study. Competing benthic organisms affected coral recruitment success through space preemption (mainly by macroalgae) or recruit overgrowth (mainly by sponges). The results highlight the small spatial scale (mm–cm) at which the processes responsible for recruitment success or failure occur and emphasize the need to include such small-scale observations in studies of coral early life-phase dynamics.     

Investigations into depth and temperature habitat utilization and overwintering grounds of juvenile sandbar sharks, Carcharhinus plumbeus: the importance of near shore North Carolina waters

Defining the location and habitat characteristics of areas of aggregation of Atlantic shark species has been identified as an important information need for current and future management efforts. The primary objective of this project was to investigate the depths and temperatures of the waters occupied by large juvenile sandbar sharks of the northwest Atlantic population during the winter months and the overwintering localities of these animals using a fishery independent method. During the summer of 2003, 21 sandbar sharks captured in the Eastern Shore of Virginia bays and lagoons were outfitted with satellite transmitters that were programmed to detach during the following winter. The sharks occurred in significantly colder and deeper waters during the winter period than during the summer nursery period with a mean depth and temperature recorded by the transmitters during the winter period of 19.9°C and 20.8 m and a mean depth and temperature recorded during the summer period of 24.0°C and 4.3 m. Despite this decrease in temperature and increase in depth of occurrence, the sharks remained in relatively warm waters and shallow depths throughout the overwintering period. Satellite pop-off locations during the overwintering period were concentrated in central North Carolina coastal waters, where a unique combination of shallow depths and warm temperatures may contribute to the survivorship of these animals while they overwinter in these waters.     

The fishery,biology, and management of Atlantic sturgeon,Acipenser oxyrhynchus,in North America

Synopsis The Atlantic sturgeon supported major fisheries along the entire Atlantic coast of North America. These fisheries peaked about 1890 and then suffered almost total collapse by 1905. The Atlantic sturgeon is anadromous and highly susceptible to capture during spawning migrations. Further, this species biological characteristics makes it very vulnerable to man-induced changes in natural habitat and slow to recover. Atlantic sturgeon mature at an advanced age (7–27 year for females, depending on latitude), exhibit a long interspawning period (2–5 year), and require suitable riverine, estuarine, and coastal environments for successful completion of their life cycle. Today, only remnant stocks exist in areas of former abundance. Management regulations vary considerably from state to state and range from full protection to no protection. Biological data are needed to: identify and characterize specific spawning and nursery areas; delineate migratory patterns and recruitment to various stocks; establish stock abundance; and, assess effects of various management strategies. In order to protect remaining stocks, the imposition of a total harvesting moratorium is recommended.     

Evolution of thermal physiology and growth rate between populations of the western fence lizard (Sceloporus occidentalis)

Summary Hatchling Sceloporus occidentalis from northern populations (central Oregon) grow more slowly than hatchlings from southern populations (southern California) in nature. In this study, I determine whether this difference in growth rate results from differences in thermal environment and/or in thermoregulatory behavior. To determine the degree to which the thermal environment affects growth rate among populations, I reared hatchings from the northern and southern populations in a cycling thermal regime in one of three experimental treatments differing in access to radiant heat (6, 9, or 12 h radiant heat; remainder of 24 h at 15°C). I also measured the body temperature that each individual voluntarily selected over the course of the daily activity cycle. Growth rate varied positively with duration of access to radiant heat. Within the three treatments, individual growth rate was positively correlated with body temperature. Moreover, the difference in growth rate between the northern and southern populations was due in part to differences in behavior — individuals from northern populations selected lower body temperatures. I found that significant variation in body temperature was associated with family membership, suggesting that thermal physiology has a genetic basis. Moreover, growth rate was correlated with body temperature among families in each population suggesting a genetic correlation underlies the phenotypic correlations. Thus, genetically based variation in thermal physiology contributes to differences in growth rate among individuals within a population as well as to differences among populations.     

Age at first reproduction and growth rate are independent of basal metabolic rate in mammals

This study tested an emergent prediction from the Metabolic Theory of Ecology (MTE) that the age at first reproduction (α) of a mammal is proportional to the inverse of its mass-corrected basal metabolic rate: The hypothesis was tested with multiple regression models of conventional species data and phylogenetically independent contrasts of 121 mammal species. Since age at first reproduction is directly influenced by an individual’s growth rate, the hypothesis that growth rate is proportional to BMR was also tested. Although the overall multiple regression model was significant, age at first reproduction was not partially correlated with either body mass, growth rate or BMR. Similarly, growth rate was not correlated with BMR. Thus at least for mammals in general, there is no evidence to support the fundamental premise of the MTE that individual metabolism governs the rate at which energy is converted to growth and reproduction at the species level. The exponents of the BMR allometry calculated using phylogenetic generalized least squares regression models were significantly lower than the three-quarter value predicted by the MTE. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Thermal sensitivity of growth rate in hatchling Sceloporus lizards: environmental,behavioral and genetic aspects

Summary To investigate the physiological, behavioral, and genetic contributions to growth rate, we studied the thermal sensitivity of growth rate in hatchlings of the iguanid lizards Sceloporus occidentalis and S. graciosus in the laboratory. We used a cycling thermal regime patterned after thermal environments found in nature. Growth rates increased with duration of access to radiant heat. Thus, variation in the thermal environment can cause phenotypic variation in growth rate and hence body size. The two species differed in both the magnitude and thermal sensitivity of growth rate, and these differences were associated with differences in behavioral thermoregulation. Thus, growth is determined interactively by both behavior and physiology. We found evidence of among-family variation in the growth rates of S. occidentalis, suggesting that growth rate has the genetic potential to evolve. In S. occidentalis, both growth rate and egg size affected body size of hatchlings at several weeks of age. In turn, hatchling size may affect fitness: for example, larger S. occidentalis hatchlings had higher sprint speeds and may therefore be more adept at capturing prey or evading predators. Our results demonstrate that growth rate has genetic, behavioral, and physiological components, and that the resulting effects on body size may have important consequences for ecological performance e.g., sprint speed.     

Reproductive output,costs of reproduction,and ecology of the smooth snake,Coronella austriaca,in the eastern Italian Alps

A 5-year mark-recapture study of smooth snakes (Coronella austriaca) in the Carnic Alps (1100 m above sea level) of north-eastern Italy provided extensive information on the biology and life-history of these small viviparous snakes. Offspring were relatively large (mean=15 cm total length, 2.9 g) when they were born in late summer, and females grew to maturity (44 cm, 50 g) in approximately 4 years. Larger neonates retained their size advantage for at least 12 months, but did not have a higher probability of survival. Although sexual size dimorphism (at birth and at mean adult body sizes) was minor, the sexes differed significantly in several respects. Females grew faster than males during juvenile life, and adult females diverged in dietary habits from the rest of the population. Whereas juveniles (of both sexes) and adult males fed primarily on lizards, larger females shifted to feeding less frequently, but taking larger prey (mammals and snakes). Reproductive output increased strongly with maternal body size: larger females reproduced more frequently, produced larger litters of larger neonates, had higher relative clutch masses (RCMs), and had a lower proportion of stillborn off-spring. Most females produced a litter every 2nd or 3rd year. We did not detect significant year-to-year variation in reproductive traits over the 5 years of our study. Females were consistent from one litter to the next in several traits (e.g., litter sizes, offspring sizes and shapes, proportions of stillborn neonates, RCMs), but this consistency was due to differences in body size among females rather than to size-independent maternal effects. Overall litter sex ratios averaged 50/50, but sex ratios tended to be more male-biased in litters that were unusually large relative to maternal body size, and in litters containing a high proportion of stillborn offspring. Costs of reproduction appear to be high in this population, in terms of both energy allocation and risk. Reproduction reduced growth rates, and females that recovered condition more quickly in the year after reproduction were able to reproduce again after a briefer delay. Mortality was highest in reproducing females with high RCMs, and in females that were very emaciated after parturition. The marked increase in reproductive output with increasing maternal body size in C. austriaca may reflect a reduction in costs as females grow larger, and the dietary shift to larger prey may enhance the rate that females can accumulate energy for reproduction.     

Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside

Understanding the evolution of growth rate requires knowledge of the physiology of growth. This study explored the physiological basis of countergradient variation (CnGV) in somatic growth across latitudinal populations of the Atlantic silverside, Menidia menidia. Energetics of northern (Nova Scotia, Canada) and southern (South Carolina, USA) genotypes were compared across resource levels, temperatures, and fish sizes to identify trade-offs to rapid growth. Offered unlimited resources, genotypes differed in both energy acquisition and allocation. Food consumption, growth, and efficiency of northern genotypes were consistently higher than in southern genotypes, across temperatures and body sizes. Feeding metabolism (specific dynamic action; SDA) was proportional to meal size, differing between genotypes to the extent that food consumption differed. Given limited resources, northern and southern genotypes displayed similar growth, efficiency, routine activity, and SDA across temperatures and fish sizes. Routine metabolism was equal at 17°C and 22°C, yet was significantly higher in northern fish at 28°C. Growth rates in M. menidia do not appear to trade off across environments or body sizes, i.e., at no temperature, ration, or size do southern fish outgrow northern conspecifics. Nor does submaximal growth result from increased costs of maintenance, tissue synthesis, or routine activity. Based on our findings, we propose that CnGV consumption and growth in M. menidia likely result from trade-offs with other energetic components, namely sustained and burst swimming. Received: 26 January 1999 / Accepted: 14 September 1999     

Validated age and growth of the leopard shark,Triakis semifasciata,with comments on reproduction

Synopsis The age, growth, and sexual maturation of the leopard shark, Triakis semifasciata, from central California were studied. Growth band counts in vertebral centra of 162 leopard sharks produced von Bertalanffy growth curves with L, K. and t_o parameters of 1536 mm. 0.082, and -2.31, respectively, for both sexes combined. The L₈ value for females (1602 mm TL) was slightly but insignificantly higher than for males (1499 mm TL), but the K and t_o values were almost identical. Seasonal changes in size modes of young-of-the-year leopard sharks, centrum edge characteristics, and growth and tetracycline mark-recapture from the field were used to validate annual deposition of vertebral centrum band pairs. Sexual maturity was evaluated by the gonads and presence of sperm and eggs; males mature at 7 yr and at about 63% of asymptotic length, and females mature at 10 yr, and at about 72% of asymptotic length. This slow growth, late maturity, and relatively low fecundity may increase their susceptibility to over-exploitation.     

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.     

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.