Homing ability of young lemon sharks, <Emphasis Type="Italic">Negaprion brevirostris</Emphasis>

Synopsis We carried out the first experimental study testing an elasmobranchs ability to return home. We displaced juvenile lemon sharks,Negaprion brevirostris, 4–16 km from their observed home ranges at Bimini Islands, Bahamas during daylight and at night. We tracked all sharks except one back to the Bimini Islands and most returned to their home ranges observed before displacement. Even sharks displaced to a site closer to another island with suitable habitat for young lemon sharks returned to their home ranges at Bimini Islands. Sharks displayed a preferred compass direction (PCD) toward the east as their first swimming direction after release, suggesting an innate sense of direction. This bearing was followed shortly afterwards by a home-oriented direction. Swimming speeds prior to reaching shore were approximately twice as fast than the usual cruising speed reported for juvenile lemon sharks. The return of young (0–2 years), inexperienced sharks to their original home range indicate high site fidelity and an ability to home.     

Effects of large-scale anthropogenic development on juvenile lemon shark (Negaprion brevirostris) populations of Bimini, Bahamas

The waters around Bimini (25° 43.70′ N, 79° 18.00′ W) provide an ideal nursery location for juvenile lemon sharks, Negaprion brevirostris, but this habitat is threatened by the development of a large resort. Since 1999 the North Sound (NS) has been subjected to intermittent periods of dredging, the most intensive of which was in March 2001. Possible effects from the development up to June 2006 were investigated by: comparing growth rates of juvenile lemon sharks in the NS, Sharkland (SL) and South Bimini (SB) nurseries between 1995-2005 using before-after, control-impact (BACI) analysis; analyzing survival of juvenile lemon sharks in the NS and SL between 1995–2006; and by comparing habitat structures in the NS and SB nurseries in 2003 and 2005. BACI analysis detected no statistically significant difference between the growth rates of juvenile lemon sharks in the three nurseries before and after the impact date of March 2001. However, a reduction in the survival rate of juvenile lemon sharks in the NS after March 2001 was statistically significant, including a 23.5% decline in first-year survival. Habitat structure of the NS in 2003 and 2005 also varied with the mean percentage cover of the seagrass Thalassia testudinum declining by 17.7% since 2003. Our results indicate a correlation between the development thus far and a decline in the survival rates of juvenile lemon sharks and changes in the habitat structure of the NS. To elucidate further information regarding potential effects of the resort development on juvenile lemon sharks in the NS nursery, we suggest several future research directions.     

Habitat selection by juvenile lemon sharks,Negaprion brevirostris

Synopsis We surgically implanted ultrasonic transmitters in 38 lemon sharks,Negaprion brevirostris, and manually tracked the sharks for 1–153 days. This yielded 2281 positional fixes recorded at 15-min intervals. We used these positional data with availability data of four environmental variables (water depth, temperature, salinity, and bottom type), sampled at 213 stations along 15 transects, to examine usage of habitat. All sharks used contours of water depth, water temperature, and bottom type disproportionately to the availability of these variables in the study site. Specifically, juvenile lemon sharks selected shallower, warmer water with an underlying rocky or sandy substrate, perhaps for predator avoidance. This is the first report on habitat selection by any elasmobranch.     

Spatial ecology of juvenile lemon sharks (<Emphasis Type="Italic">Negaprion brevirostris</Emphasis>) in tidal creeks and coastal waters of Eleuthera,The Bahamas

Fisheries exploitation and habitat alteration are threatening lemon shark (Negaprion bevirostris) populations because they use nearshore regions as nursery sites. As such, there is a need for information on the spatial ecology of juvenile lemon sharks to identify critical habitats that require protection, as well as to understand their basic ecology. The purpose of this study was to determine the habitat preferences and movement patterns of juvenile lemon sharks along a sub-section of coastline characterized by coastal flats and tidal creeks of Eleuthera, The Bahamas. Eleven juvenile lemon sharks (766 ± 127 mm total length; mean±SD) were captured from various tidal creeks within the 23 km study area and were surgically implanted with acoustic transmitters. A series of 27 hydrophone receivers acted as a passive monitoring array to detect tagged individuals as they moved among habitats. Findings suggest that juvenile lemon sharks tagged in this study prefer shallow water habitats within tidal creeks, and typically display high site fidelity with occasional forays to alternate habitats or creeks. In fact, more than 90% of tagged lemon sharks had the greatest percentage of detections located at a receiver at or close to the location where they were tagged. There was no evidence of differences in diel or seasonal movement and habitat use. Knowledge gained from this study will be useful for directing future conservation and management strategies including coastal development plans and marine protected areas.     

Food limitation in a nursery area: estimates of daily ration in juvenile scalloped hammerheads, Sphyrna lewini (Griffith and Smith, 1834) in Kāne'ohe Bay, ō'ahu, Hawai'i

Gastric evacuation and daily ration were studied in juvenile scalloped hammerhead sharks in Kāne'ohe Bay in order to better understand their ecology and role as apex predators in the marine environment. Three major variables known to affect the rate of gastric evacuation were manipulated: meal size, prey species, and temperature. Rates of gastric evacuation were faster than have previously been measured for sharks. The time for 80% of the meal weight (dry) to be evacuated ranged from 5.4 to 22.1 h. Daily ration was estimated using two different methods based on gastric evacuation rates and stomach content data. Estimates ranged from 2.12% to 3.54% of the body weight, which is relatively high compared to other elasmobranchs, but lower than estimates of maintenance ration for juvenile scalloped hammerheads. Data available for diet and growth of juvenile scalloped hammerhead sharks in Kāne'ohe Bay as well as data for their prey species suggest that these sharks may be surviving much of the time at consumption levels below maintenance ration.     

Ontogenetic diet shifts and prey selection in nursery bound lemon sharks, Negaprion brevirostris, indicate a flexible foraging tactic

Ontogenetic variations in shark diet are often qualitatively inferred from dietary analysis and hindered by high levels of unidentified prey or small sample sizes. This study focused on nursery bound lemon sharks (Negaprion brevirostris, n?=?396), enabling some control over the confounding variables of prey choice associated with ontogeny. Nursery bound lemon sharks exhibited weak ontogenetic variation in dietary composition with high levels of dietary overlap. Variation in prey preference of lemon sharks with ontogeny was complex, but revealed a continuous shift from predominantly opportunistic benthic foraging as neonates to more selective piscivory with increasing shark size while in the nursery. Lemon sharks demonstrated a discrete ontogenetic shift in the number of prey consumed and stomach content weight (Kruskal-Wallis tests p?<?0.01), as well as prey size (ANOVA, p?<?0.001). All sizes of sharks exhibited positive size selection of prey (Mann?CWhitney U tests, p?<?0.01). However, the lack of size preference by all but the largest lemon sharks for their major prey (yellowfin mojarra, Gerres cinereus), suggests neonate sharks, while capable of occasionally foraging on large prey, are relatively inept opportunistic foragers. This was evident in high diet breadth, low diversity of consumed prey and lower trophic level than larger sharks. This study represents the first quantitative analysis of ontogenetic variation in prey preference and size selection in sharks, indicating a flexible foraging tactic in lemon sharks and the importance of hunting ability and predator size in prey choice.     

Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris

Because sharks possess an unusual suite of reproductive characteristics, including internal fertilization, sperm storage, relatively low fecundity, and reproductive modes that range from oviparity to viviparity, they can provide important insight into the evolution of mating systems and sexual selection. Yet, to date, few studies have characterized behavioral and genetic mating systems in natural populations of sharks or other elasmobranchs. In this study, highly polymorphic microsatellite loci were used to examine breeding biology of a large coastal shark, the lemon shark, Negaprion brevirostris, at a tropical lagoon nursery. Over six years, 910 lemon sharks were sampled and genotyped. Young were assigned into sibling groups that were then used to reconstruct genotypes of unsampled adults. We assigned 707 of 735 young sharks to one of 45 female genotypes (96.2%), and 485 (66.0%) were assigned to a male genotype. Adult female sharks consistently returned to Bimini on a biennial cycle to give birth. Over 86% of litters had multiple sires. Such high levels of polyandry raise the possibility that polyandry evolved in viviparous sharks to reduce genetic incompatibilities between mother and embryos. We did not find a relationship between relatedness of mates and the number of offspring produced, indicating that inbreeding avoidance was probably not driving pre- or postcopulatory mate choice. Adult male sharks rarely sired more than one litter at Bimini and may mate over a broader geographic area.     

The use of an unoccupied aerial vehicle to survey shark species over sand and rocky-reef habitats in a marine protected area

Cabo Pulmo National Park was established in 1995 and has since seen a large increase in fish biomass. An unoccupied aerial vehicle (UAV) was used to survey shallow coastal habitat in which lemon sharks (Negaprion brevirostris), bull sharks (Carcharhinus leucas) and Pacific nurse sharks (Ginglymostoma unami) were recorded. Sharks were more common in the afternoon, potentially using warmer shallow areas to behaviourally thermoregulate. This study highlights UAV surveying to be a viable tool for species identification, a limitation of previous terrestrial surveys conducted in the area.     

Review of Elasmobranch Behavioral Studies Using Ultrasonic Telemetry with Special Reference to the Lemon Shark, Negaprion Brevirostris, Around Bimini Islands, Bahamas

A review of past behavioral ultrasonic telemetry studies of sharks and rays is presented together with previously unpublished material on the behavior of the lemon shark, Negaprion brevirostris, around the Bimini Islands, Bahamas. The review, focusing on movement behaviors of 20 shark and three ray species, reveals that elasmobranchs exhibit a variety of temporal and spatial patterns in terms of rates-of-movement and vertical as well as horizontal migrations. The lack of an apparent pattern in a few species is probably attributable to the scarcity of tracking data. Movements are probably governed by several factors, some still not studied, but data show that food, water temperature, bottom type, and magnetic gradient play major roles in a shark's decision of where and when to swim. A few species exhibit differences in behavior between groups of sharks within the same geographical area. This interesting finding warrants further research to evaluate the causes of these apparent differences and whether these groups constitute different subpopulations of the same species. The lack of telemetry data on batoids and some orders of sharks must be addressed before we can gain a more comprehensive understanding of the behavior of elasmobranch fishes. Previously unpublished data from 47 smaller and 38 larger juvenile lemon sharks, collected over the decade 1988–1998, provide new results on movement patterns, habitat selection, activity rhythms, swimming speed, rate-of-movement, and homing behavior. From these results we conclude that the lemon shark is an active predator with a strong, apparently innate homing mechanism. This species shows ontogenetic differences in habitat selection and behavior, as well as differences in movements between groups of individuals within the same area. We suggest three hypotheses for future research on related topics that will help to understand the enigmatic behavior of sharks.     

Spatial and ontogenetic variation in growth of nursery-bound juvenile lemon sharks, <Emphasis Type="Italic">Negaprion brevirostris</Emphasis>: a comparison of two age-assigning techniques

Synopsis We compared growth rates of the lemon shark, Negaprion brevirostris, from Bimini, Bahamas and the Marquesas Keys (MK), Florida using data obtained in a multi-year annual census. We marked new neonate and juvenile sharks with unique electronic identity tags in Bimini and in the MK we tagged neonate and juvenile sharks. Sharks were tagged with tiny, subcutaneous transponders, a type of tagging thought to cause little, if any disruption to normal growth patterns when compared to conventional external tagging. Within the first 2 years of this project, no age data were recorded for sharks caught for the first time in Bimini. Therefore, we applied and tested two methods of age analysis: (1) a modified minimum convex polygon method and (2) a new age-assigning method, the cut-off technique. The cut-off technique proved to be the more suitable one, enabling us to identify the age of 134 of the 642 previously unknown aged sharks. This maximised the usable growth data included in our analysis. Annual absolute growth rates of juvenile, nursery-bound lemon sharks were almost constant for the two Bimini nurseries and can be best described by a simple linear model (growth data was only available for age-0 sharks in the MK). Annual absolute growth for age-0 sharks was much greater in the MK than in either the North Sound (NS) and Shark Land (SL) at Bimini. Growth of SL sharks was significantly faster during the first 2 years of life than of the sharks in the NS population. However, in MK, only growth in the first year was considered to be reliably estimated due to low recapture rates. Analyses indicated no significant differences in growth rates between males and females for any area.This revised version was published online in April 2005 with corrections to the fourth authors email address and affiliation.     

Long-term natal site-fidelity by immature lemon sharks (Negaprion brevirostris) at a subtropical island

Although many sharks begin their life confined in nursery habitats, it is unknown how rapidly they disperse away from their natal area once they leave the nursery. We examine this issue in immature lemon sharks ( Negaprion brevirostris ) from the time they leave the nursery (∼ age 3) at a subtropical island (Bimini, Bahamas), through to the onset of sexual maturity (∼ age 12). From 1995 to 2007 we tagged and genotyped a large fraction of the nursery-bound sharks at this location (0–3 years of age, N  = 1776 individuals). From 2003 to 2007 we sampled immature sharks aged from 3 to 11 years ( N  = 150) living around the island and used physical/genetic tag recaptures coupled with kinship analysis to determine whether or not each of these 'large immature sharks' was locally born. We show that many island-born lemon sharks remain close to their natal area for long periods (years) after leaving the nursery; more than half of the sampled sharks up to 135 cm total length (∼6 years old) were locally born. The fraction of locally born sharks gradually declined with increasing shark size, indicating that dispersal is relatively slow and does not primarily occur after sharks reach a threshold size. Local conservation measures (e.g. localized fishery closures, marine protected areas) can therefore help protect island-born lemon sharks even after they leave the nursery habitat.     

The effects of ration level on food retention time in juvenile lemon sharks,Negaprion brevirostris

Synopsis Fecal production was monitored to observe the effects of meal size on retention time of food in the digestive tracts of lemon sharks, Negaprion brevirostris. Initial appearance of feces occurred more rapidly when ration level was increased. The onset of fecal production was negatively correlated with rate of intake. Production of feces continued for a longer period of time when meal size was increased. Retention time of food was directly related to feeding rate, suggesting that the rate of digestion was constant. The correlation between retention time and intake on a percentage body weight basis was greater than the correlation between retention time and intake on an energy density basis. The use of agar to bind food may have delayed digestion and prolonged food passage for sharks fed an experimental diet.     

Effect of weight and frontal area of external telemetry packages on the kinematics,activity levels and swimming performance of small‐bodied sharks

This study sought to observe the effects of submerged weight and frontal cross‐sectional area of external telemetry packages on the kinematics, activity levels and swimming performance of small‐bodied juvenile sharks, using lemon sharks Negaprion brevirostris (60–80 cm total length, L_T) as a model species. Juveniles were observed free‐swimming in a mesocosm untagged and with small and large external accelerometer packages that increased frontal cross‐sectional area of the animals and their submerged weight. Despite adhering to widely used standards for tag mass, the presence of an external telemetry package altered swimming kinematics, activity levels and swimming performance of juvenile N. brevirostris relative to untagged individuals, suggesting that tag mass is not a suitable standalone metric of device suitability. Changes in swimming performance could not be detected from tail‐beat frequency, which suggests that tail‐beat frequency is an unsuitable standalone metric of swimming performance for small N. brevirostris. Lastly, sharks experienced treatment‐specific changes in activity level and swimming kinematics from morning to afternoon observation. Therefore, the presence of external telemetry packages altered the kinematics, activity levels and swimming performance of small young‐of‐the‐year N. brevirostris and these data may therefore be relevant to other similar‐sized juveniles of other shark species.     

The breeding biology of lemon sharks at a tropical nursery lagoon

Surprisingly little is known about the reproductive behaviour and breeding biology of most shark species, especially in natural populations. Here, we characterize reproductive patterns and use of a natal nursery at Bimini, Bahamas by lemon sharks, Negaprion brevirostris. We systematically and exhaustively sampled young lemon sharks at Bimini annually from 1995 to 2000 and opportunistically sampled adults over the same period. Out of the 897 young sharks sampled, 119 could be assigned to five sampled mothers using microsatellite genotyping. Reproductive females showed strong philopatry to the nursery, returning to Bimini every two years to give birth. Each of these females may rely entirely on the Bimini nursery for recruitment. The protection of known nursery grounds should therefore figure prominently in conservation efforts for large coastal shark species. The reconstruction of paternal genotypes indicates that litters are sired by multiple males, and females mate with different males nearly every breeding cycle. The ubiquitous polyandry reported here raises the possibility that genetic incompatibility and post-copulatory paternity-biasing mechanisms may operate in viviparous sharks.     

The shark nursery of Bulls Bay,South Carolina,with a review of the shark nurseries of the southeastern coast of the United States

Synopsis Shark nurseries, or nursery areas, are geographically discrete parts of a species range where the gravid females of most species of coastal sharks deliver their young or deposit their eggs, and where their young spend their first weeks, months, or years. These areas are usually located in shallow, energy rich coastal areas where the young find abundant food and have little predation by larger sharks. Nurseries are characterized by the presence of both gravid females and free swimming neonates. Neonates are young bearing fresh, unhealed umbilical scars in the case of placental species, or those at or near the birth size in aplacental species. Bulls Bay, South Carolina, is a nursery for the blacknose, spinner, finetooth, blacktip, sandbar, dusky, Atlantic sharpnose, scalloped hammerhead, and smooth dogfish sharks. The lemon shark has its nursery in shallow waters of south Florida and the Bahamas. The bull shark has its nursery in the lagoons of the east coast of central Florida.     

Effect of ration size on growth and gross conversion efficiency of young lemon sharks, Negaprion brevirostris

Young lemon sharks, Negaprion brevirostris , were kept under controlled conditions in an aquarium and fed blue runner, Caranx crysos , at different ration levels. The relationship between feeding rate and growth rate was best described by a von Bertalanffy growth curve, which predicted a maximum growth rate of 140 kJ kg⁻¹ day⁻¹ (0·66% b.w. day⁻¹), a maintenance ration of 199 kJ kg⁻¹ day⁻¹ (1·06% b.w. day⁻¹), and losses due to starvation of -236kJ kg⁻¹ day⁻¹ (1·11% b.w. day⁻¹). The relationship between gross conversion efficiency ( K ₁) and feeding rate was also examined. K₁ ranged from - 64 to 25% and did not drop at high ration levels. Activity levels of both starved sharks and sharks fed at maintenance were not significantly different (0·2 body lengths s⁻¹). K ₁ values generated from both laboratory and field data suggest that young lemon sharks can convert food to new tissue as efficiently as teleosts.     

Gastric evacuation in the sandbar shark, Carcharhinus plumbeus

Sandbar sharks maintained in an enclosure in the natural environment were fed meals of soft blue crab, Callinectes sapidus , or menhaden, Brevoortia lyrannus , and were sacrificed at intervals after feeding to measure rates of gastric emptying. Regression analysis was used to evaluate the adequacy of various models in describing the decrease in stomach contents with time after feeding. A Gompertz growth curve provided the best fit to the data for both food types. This model suggests that gastric emptying is characterized by an initial lag phase during which evacuation rate increases, a period of maximal evacuation, and a decreasing evacuation rate during the later stages of digestion. Passage of food from the stomach was slow relative to other species of fish studied. The time required to evacuate 98% of a meal was 92–3 and 70–7 h for sharks fed menhaden and blue crab respectively. Evacuation rates did not differ between day and night periods.     

Microsatellite loci within sixgill sharks, Hexanchus griseus

Novel sixgill shark (Hexanchus griseus) microsatellite loci were developed and tested on five shark species. A suite of microsatellite loci previously developed for lemon sharks (Negaprion brevirostris) was also tested. Data on 15 microsatellites are presented including primer sequences, number of alleles (a), observed (H_O) and expected heterozygosities (H_E), and F_IS values for sixgill sharks (a = 10–69, H_O = 0.24–1.00, H_E = 0.76–0.96 and F_IS = –0.21–0.60), sevengill sharks (Notorynchus cepedianus) (a = 6–40, H_O = 0.20–0.73, H_E = 0.59–0.94 and F_IS = –0.47–0.58), Pacific spiny dogfish (Squalus acanthias) (a = 3–13, H_O = 0.00–0.96, H_E = 0.24–0.93 and F_IS =–0.52–1.00), angle sharks (Squatina californica) (a = 1–4, H_O = 0.00–1.00, H_E = 0.60–1.00 and F_IS =–1.00–0.25), and leopard sharks (Triakis semifasciata) (a = 3–16, H_O = 0.20–1.00, H_E = 0.53–0.92 and F_IS = –0.57–1.00). A final suite of 14 microsatellites (13 developed from sixgill sharks and one from lemon sharks) were found to be polymorphic and conform to Hardy–Weinberg equilibrium within sixgill sharks.     

Evoked Potential Audiograms of the Nurse Shark (Ginglymostoma cirratum) and the Yellow Stingray (Urobatis jamaicensis)

The hearing thresholds of the nurse shark, Ginglymostoma cirratum, and the yellow stingray, Urobatis jamaicensis, were measured using auditory evoked potentials (AEP). Stimuli were calibrated using a pressure-velocity probe so that the acoustic field could be completely characterized. The results show similar hearing thresholds for both species and similar hearing thresholds to previously measured audiograms for the lemon shark, Negaprion brevirostris, and the horn shark, Heterodontis francisi. All of these audiograms suggest poor hearing abilities, raising questions about field studies showing attraction of sharks to acoustic signals. By extrapolating the particle acceleration thresholds into estimates of their equivalent far-field sound pressure levels, it appears that these sharks cannot likely detect most of the sounds that have attracted sharks in the field.     

Genetic tagging to determine passive integrated transponder tag loss in lemon sharks

Multilocus genotypes using nine DNA microsatellite loci provided an effective and permanent individual identification mark for lemon sharks Negaprion brevirostris , the first example of genetic tagging for any elasmobranch species. The double-tagging provided by micro-satellites afforded a means to determine passive integrated transponder (PIT) tag shed rate in lemon sharks. Of 388 sharks that were recaptured, 47 (12.1%) had shed their PIT tag.