Samuel H. Gruber

Home Range of Juvenile Lemon Sharks, Negaprion brevirostris

Manual acoustic telemetry techniques were used to study spatial and temporal patterns of movement of juvenile lemon sharks. Ultrasonic transmitters were implanted into the coelom of 38 sharks, yielding trackings totaling 2281 telemetry fixes. Activity space varied from 0.23 km2 to 1.26 km2 and was positively correlated with shark size. Three indices of site attachment demonstrated that juvenile lemon sharks establish a home range. An index of site defense and field observations indicated that no territoriality was observed against conspecifics.

Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion)

Seascapes are complex environments, and populations are often isolated by factors other than distance. Here we investigate the role of coastal habitat preference and philopatry in shaping the distribution and population structure of lemon sharks. The genus Negaprion comprises the amphiatlantic lemon shark (N. brevirostris), with a relict population in the eastern Pacific, and its Indo‐West Pacific sister species, the sicklefin lemon shark (N. acutidens). Analyzing 138 individuals throughout the range of N. brevirostris (N = 80) and N. acutidens (N = 58) at microsatellite loci (nine and six loci, respectively) and the mitochondrial control region, we find evidence of allopatric speciation corresponding to the Tethys Sea closure (10–14 million years ago) and isolation of the eastern Pacific N. brevirostris population via the emergence of the Isthmus of Panama (~3.5 million years ago). There is significant isolation by oceanic distance (R2 = 0.89, P = 0.005), defined as the maximum distance travelled at depths greater than 200 m. We find no evidence for contemporary transatlantic gene flow (m, M = 0.00) across an oceanic distance of ~2400 km. Negaprion acutidens populations in Australia and French Polynesia, separated by oceanic distances of at least 750 km, are moderately differentiated (FST = 0.070–0.087, P≤ 0.001; ΦST = 0.00, P = 0.99), with South Pacific archipelagos probably serving as stepping stones for rare dispersal events. Migration between coastally linked N. brevirostris populations is indicated by nuclear (m = 0.31) but not mitochondrial (m < 0.001) analyses, possibly indicating female natal site fidelity. However, philopatry is equivocal in N. acutidens, which has the lowest control region diversity (h = 0.28) of any shark yet studied. Restricted oceanic dispersal and high coastal connectivity stress the importance of both local and international conservation efforts for these threatened sharks.

Habitat selection by juvenile lemon sharks,Negaprion brevirostris

SynopsisWe 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.

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 sharks 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.

Age Assessment of the Lemon Shark, Negaprion brevirostris, Using Tetracycline Validated Vertebral Centra

Vertebral centra were removed from 55 tag-recaptured lemon sharks, Negaprion brevirostris, that had been injected intramuscularly with tetracycline hydrochloride at a dosage level of 12.5 mg/kg at the time of release. Tetracycline deposited at sites of active calcification on the vertebral centra served as a fluorescent marker along the periphery of each centrum at the time of injection. Thin growth zones, or circuli, were observed in ground and stained sections. A lunar periodicity of approx. 29 d was validated for circulus deposition. Precision of circulus counts was evaluated, with an index of average percent error of 3.4% for a single reader. Age estimates were then obtained using circulus counts for a total of 110 sharks, with a plot of precaudal length against estimated age for both sexes fitting a von Bertalanffy growth curve with the parameters Loo = 317.65, k = 0.057, and to = -2.302. The predicted age at maturity for males is 11.6 yr and for females is 12.7 yr. These results show that this species is slow growing and long-lived.

Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation.

DNA microsatellite markers were used to characterize the population genetic structure of the lemon shark, Negaprion brevirostris, in the western Atlantic. This study demonstrates for the first time the usefulness of microsatellites to study population genetic structure and mating systems in the Chondricthyes. Lemon sharks (mostly juveniles) were sampled non‐destructively from four locations, Gullivan Bay and Marquesas Key in Florida, Bimini, Bahamas, and Atol das Rocas, Brazil. At least 545 individuals were genotyped at each of four dinucleotide loci. The number of alleles per locus ranged from 19 to 43, and expected heterozygosities ranged from 0.69 to 0.90. Relatively little genetic structure was found in the western Atlantic, with small but significant values for estimators of FST and RST among populations, θ (0.016) and ρ (0.026), respectively. No sharp discontinuities were found between the Caribbean sites and Brazil, and most alleles were found at all four sites, indicating that gene flow occurs throughout the western Atlantic with no evidence for distinct stocks.

RECONSTRUCTION OF PARENTAL MICROSATELLITE GENOTYPES REVEALS FEMALE POLYANDRY AND PHILOPATRY IN THE LEMON SHARK, NEGAPRION BREVIROSTRIS

Abstract 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.

Sharks: Attraction by Low-Frequency Sounds

Large sharks (Carcharhinidae, Sphyrnidae), in their natural environment, were attracted to low-frequency (predominantly 20 to 60 cy/sec) pulsed sounds, but apparently not to higher frequency (400 to 600 cy/sec) pulsed sounds, or to low-frequency continuous sounds. The sharks apparently detected and oriented to the sounds in the acoustic far field.

The Behavior of the Bonnethead Shark, Sphyrna tiburo

Behavioral activities of a colony of 10 bonnethead sharks, Sphyrna t. tiburo, held under semi-natural conditions, were examined over a period of six months. All sharks had attained, or were approaching, sexual maturity. Objectives of the study were to describe species-typical motor patterns and postures, to analyze the diurnality of patrolling activity and to characterize pattern(s) of organization underlying social interactions noted within the colony. Eighteen postures and patterns of movement were described, almost half of them having apparent social relevance. In specific instances, functional significance of a pattern was cautiously given. Patrolling activity appeared to have a diurnal rhythm, with a peak occurring in the late afternoon; smaller individuals were more erratic in their patrolling. Finally, a clear but subtle social organization, based on a straight-line, size-dependent, dominance hierarchy was found. Though position within the hierarchy was not determined by sex, data indicated that all individuals tended to shy away from larger males. Sexual differences in the performance of certain patterns of movement were also established.

Survival of Juvenile Lemon Sharks at Bimini, Bahamas, Estimated by Mark–Depletion Experiments

Abstract The survival rate of juvenile lemon sharks Negaprion brevirostris in North Sound, Bimini, Bahamas, was estimated by marking a cohort of small sharks (≤53 cm precaudal length) each spring from 1995 to 1999 and by estimating the number of survivors 1 year later by using a depletion method on the marked population. Annual survival rate estimates varied between 38% and 65%, which was somewhat higher than the 39% steady-state survival predicted from a life cycle (Leslie matrix) model. These are the first direct estimates of the survival rate of a juvenile elasmobranch, and the results support modeling efforts that have been used in determining limits to sustainable exploitation of elasmobranchs. Estimates of survival rates in the present study were negatively correlated with estimated initial abundance and are consistent with strong, density-dependent survival.