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.     

Evaluation of passive integrated transponder tag retention from two tagging locations in juvenile pallid sturgeon

Population augmentation and propagation of pallid sturgeon (Scaphirhynchus albus) have been a focus of scientists since the mid‐1990s. Various tag types have been used to gain a better understanding of population characteristics, stocking success, and movement patterns. Passive integrated transponder (PIT) tags have been consistently used since the inception of recovery efforts to mark age‐1 and older pallid sturgeon. This tag has been successfully used with other sturgeon species, and tagging protocols for pallid sturgeon were developed in response to those successes. Tag retention rates in pallid sturgeon have been reported as variable or unknown and there has been no formal study to determine PIT tag retention in pallid sturgeon, particularly with age‐1 individuals that are propagated in hatcheries to be stocked into the wild. The objective was to evaluate retention rates of PIT tags inserted into the operculum and along the base of the dorsal fin of age‐1 pallid sturgeon (total fork length [FL] range = 214–358 mm). Tagged sturgeon (n = 80) were held in a large holding tank and inspected for tag loss twice a month for a total of 189 days. Final tag retention was 83% for tags inserted into the operculum and 85% for tags inserted near the dorsal fin. Tags shed from the operculum were from smaller fish (mean FL = 265 mm) and losses occurred during the first 60 days of the experiment. Tags shed from the dorsal site were predominantly from larger individuals (mean FL = 305 mm) and losses were continual throughout the experiment. Future research should determine size‐specific tag retention rates so that hatcheries can maximize retention in either tag placement location.     

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.     

Serum concentrations of reproductively-related circulating steroid hormones in the free-ranging lemon shark,Negaprion brevirostris

Synopsis We have examined the concentrations of reproductively-related steroid hormones in 5 species of carcharhinid sharks, marine fishes possessing the unique attribute of placental viviparity. Measurements of serum estradiol, testosterone, progesterone, dihydrotestosterone, and corticosterone have provided baseline data for these hormones in both immature and adult male and female placental sharks. Our studies include: (1) changes in hormonal levels during maturation, (2) concentrations of circulating steroid hormones during peak breeding season, and (3) hormonal levels during gestation, including the collection of serial samples through and beyond birth from free-ranging lemon sharks. Our data suggest that steroids, important in regulating reproduction in higher mammals, are also essential in these cartilaginous fishes.     

Testing assumptions of mark–recapture theory in the coral reef fish Lutjanus apodus

This study tested assumptions of the Cormack–Jolly–Seber capture–mark–recapture (CMR) model in a population of the tropical snapper Lutjanus apodus in the central Bahamas using a combination of laboratory and field studies. The suitability of three different tag types [passive integrated transponder (PIT) tag, T-anchor tag and fluorescent dye jet-injected into the fins] was assessed. PIT tags were retained well, whereas T-anchor tags and jet-injected dye were not. PIT tags had no detectable effect on the rates of growth or survival of individuals. The capture method (fish trapping) was found to provide a representative sample of the population; however, a positive trap response was identified and therefore the assumption of equal capture probability was violated. This study illustrates an approach that can be used to test some of the critical assumptions of the CMR theory and it demonstrates that CMR methods can provide unbiased estimates of growth and mortality of L. apodus provided that trap response is explicitly modelled when estimating survival probability.     

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.     

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.     

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.     

Novel Acoustic Technology for Studying Free-Ranging Shark Social Behaviour by Recording Individuals' Interactions

Group behaviours are widespread among fish but comparatively little is known about the interactions between free-ranging individuals and how these might change across different spatio-temporal scales. This is largely due to the difficulty of observing wild fish groups directly underwater over long enough time periods to quantify group structure and individual associations. Here we describe the use of a novel technology, an animal-borne acoustic proximity receiver that records close-spatial associations between free-ranging fish by detection of acoustic signals emitted from transmitters on other individuals. Validation trials, held within enclosures in the natural environment, on juvenile lemon sharks Negaprion brevirostris fitted with external receivers and transmitters, showed receivers logged interactions between individuals regularly when sharks were within 4 m (∼4 body lengths) of each other, but rarely when at 10 m distance. A field trial lasting 17 days with 5 juvenile lemon sharks implanted with proximity receivers showed one receiver successfully recorded association data, demonstrating this shark associated with 9 other juvenile lemon sharks on 128 occasions. This study describes the use of acoustic underwater proximity receivers to quantify interactions among wild sharks, setting the scene for new advances in understanding the social behaviours of marine animals.     

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.     

Retention of loop,monel, and passive integrated transponder tags by wild,free‐ranging Lake Sturgeon (Acipenser fulvescens Rafinesque, 1817)

Tagging or marking of fish is instrumental to fisheries biologists and managers seeking to distinguish groups of fish, track movement or migration patterns, and monitor population characteristics. However, tag loss can inhibit the ability of biologists and managers to reach these objectives. The ability of Lake Sturgeon to live for long periods of time and reach large sizes, in combination with their dynamic spawning activity, requires tags to be retained under a variety of environmental and physically demanding conditions. This study evaluated tag retention of loop, monel, and passive integrated transponder (PIT) tags on wild, free‐ranging Lake Sturgeon in Lake Huron and the St. Clair – Detroit River System. Lake Sturgeon in this study were double‐tagged with both a PIT tag under one of the three anterior‐most dorsal scutes and an external tag (loop or monel) at the base of the dorsal fin. Fish were at large for up to 16 years. Overall, tag loss for PIT tags was 1% followed by monel tags at 12% and loop tags at 36%. Tag loss for loop tags was higher when the initial length of Lake Sturgeon tagged was smaller. Tag loss for monel tags increased with time at large but was not related to length at initial tagging. Monel tags left behind abrasion marks when attached to smaller Lake Sturgeon. PIT tag retention was higher than reported in previous studies that tagged other sturgeon species in different body locations. Monel tag retention was higher than other external tag types evaluated in previous studies while loop tags had similar retention rates to external tag types. Most previous studies on tag retention of sturgeon species were of shorter duration and conducted in laboratory settings, therefore loop tags may have performed more favorably during studies under short term laboratory settings. Results of this study suggest that PIT tags inserted below dorsal scutes represent a viable option for long‐term tracking of Lake Sturgeon. Monel tags attached at the base of the dorsal fin also seem to be a viable option relative to other external tag types, but should be limited to larger sturgeon as they can leave behind abrasion marks.     

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.     

The potential use of PIT telemetry for identifying and tracking crayfish in their natural environment

A method for tracking crayfish and other benthic animals in rivers and streams, based on passive integrated transponder (PIT) technology, using a portable detector was investigated. The effect of implanting crayfish with PIT tags and the efficiency of the PIT tag detector system at locating tags is described. In a laboratory study 30 signal crayfish Pacifastacus leniusculus (>33.7 mm carapace length) were internally implanted with PIT tags (12-mm long×2.1-mm diameter) and 30 crayfish matched for size and sex were kept as controls and maintained for 6 months. Tagging had no significant effect on survival, moulting or growth of crayfish, and tag retention was 100%. The reader unit consists of an antenna coil mounted on a pole and designed to be moved over the streambed to search for tagged crayfish. Efficiency testing indicated that more than 80% of tags were identified and located when hidden within different stream microhabitats.     

A genetic assessment of polyandry and breeding-site fidelity in lemon sharks

We here employ 11 microsatellite markers and recently developed litter reconstruction methods to infer mating system parameters (i.e. polyandry and breeding-site fidelity) at a lemon shark nursery site in Marquesas Key, Florida. Four hundred and eight juvenile or subadult sharks were genotyped over eight complete breeding seasons. Using this information, we were able to infer family structure, as well as fully or partially reconstruct genotypes of 46 mothers and 163 fathers. Multiple litter reconstruction methods were used, and novel simulations helped define apparent bias and precision of at least some mating system parameters. For Marquesas Key, we find that adult female lemon sharks display high levels of polyandry (81% of all litters sampled) and stronger fidelity to the nursery site than do males. Indeed, few male sharks sired offspring from more than one litter during the course of the study. These findings were quite similar to previous results from another lemon shark nursery site (Bimini, Bahamas), suggesting conserved mating system parameters despite significant variation in early life-history traits (i.e. body size and growth) among sites. The finding of at least some site fidelity in females also supports the need for careful conservation of each nursery.     

Evaluation of VIE and PIT tagging methods for juvenile cyprinid fishes

Retention and mortality associated with visible implant elastomer (VIE) and passive integrated transponder (PIT) tagged juvenile chub [ Leuciscus cephalus (L.)], dace [ Leuciscus leuciscus (L.)] and roach [ Rutilus rutilus (L.)] were evaluated. PIT tag retention (96.6–100%) was higher than VIE over the 6-month duration of the experiment. VIE retention was significantly better in the head (96.3–98.8%) than in the fins (78.8–90.9%) the first month after tagging, but the opposite was found after 6 months (head = 21.5–57.5%; fins = 77.2–88.8%). Survival was not significantly different from controls for any treatment, except dace tagged with 23-mm PIT (significantly influenced by mass of fish at tagging) and sham PIT tagged dace, because of initial losses. PIT tags are recommended as the most suitable method for tagging individual juvenile chub, dace and roach based on high retention and survival. VIE implantation in the head (studies < 30 days) and fins (studies > 30 days) could provide a cheap, batch-marking alternative, provided retention rates are monitored.     

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.     

In situ swimming behaviors and oxygen consumption rates of juvenile lemon sharks (<Emphasis Type="Italic">Negaprion brevirostris</Emphasis>)

Knowing how often animals engage in different behaviors and their energetic costs may explain why animals behave the way they do in the wild. This study sought to investigate the relationship between the frequency of various swimming behaviors and their associated energetic costs (oxygen consumption rates) in situ for juvenile lemon sharks (Negaprion brevirostris). Behaviors were identified for captive animals and remotely observed for animals in the wild with accelerometers, and oxygen consumption rates of behaviors were estimated using acceleration-calibrated relationships. Lemon sharks rested infrequently (4.3% of deployment), and the occurrence of active swimming behaviors was inversely related to their respective oxygen consumption rates. Furthermore, time of day and tide state influenced when lemon sharks exhibited active swimming behaviors – but not resting – such that sharks were most active during the day on flooding tides. Oxygen consumption rates also differed across and within different behaviors with time of day and tide state, although mean oxygen consumption rates were highest on daytime flooding tides and uniformly reduced across all other diel and tide combinations. Despite variation in oxygen consumption rates, however, lemon shark activity occurred at 32.3–35.6% of their aerobic metabolic scope. These data do not provide a clear oxygen consumption basis for swimming behaviors observed in situ, which may have been masked by potentially stronger ecological drivers (e.g., predator-prey dynamics). However, these data are relevant to linking behavioral modifications to changes in energy use that shows much promise for addressing conservation issues in fishes.     

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.     

Suitability of surgically implanted 8-mm passive integrated transponder tags for small-bodied fishes

Innovative tools that benefit conservation are critical as freshwater fishes are lost at unprecedented rates. Mark-recapture methods can characterize population demographics and life-history traits of diverse fishes, but suitable techniques for tagging for individual recognition of small-bodied fishes are rare. Passive integrated transponder (PIT) tag technology may facilitate the tagging of small fishes and early life stages of larger species. However, relatively little research has evaluated the suitability of these small (8.4 × 1.4 mm) tags for many groups of small fishes. Tag loss (retention and survival) and growth of individuals implanted with PIT tags relative to control and sham treatments were compared for eight fishes of differing morphologies. Additionally, the utility of cyanoacrylate to improve tag retention was tested on a subset of taxa. Fish of each species were equally divided and randomly assigned to one of three treatment groups (handled [control], surgical incision [sham], or surgical incision and PIT tag implantation [PIT]). During the 42-d study period, mortalities and expelled tags were counted daily and growth was measured weekly. Researchers can generally expect little tag loss and uncompromised growth rates for a variety of small-bodied fishes; however, initial fish length was related to the magnitude of physiological effects for some taxa (i.e., blacknose dace Rhinichthys atratulus, johnny darter Etheostoma nigrum, juvenile white sucker Catostomus commersonii). Relatively poor survival (<80%) was observed for two benthic species: johnny darter and blacknose dace, often when incision wounds became inflamed before healing. Prevalent tag loss for johnny darter, tadpole madtom Noturus gyrinus, and a dorsal-laterally compressed cyprinid can be reduced by closing the wounds with cyanoacrylate, but with substantially increased mortality rates. This research demonstrates the broad applicability of PIT tagging technology for ecological studies of small-bodied fishes and alleviates many concerns when surgically implanting tags into several fishes.     

Low Rates of PIT-Tag Loss in an Insectivorous Bat Species

The rate of loss of tags used to mark individuals is an important consideration in wildlife research and monitoring. Passive integrated transponder (PIT) tags (or microchips) generally have high retention rates; however, tag loss rates for small mammals such as insectivorous bats are poorly understood. We double-marked a population of Gould's wattled bats (Chalinolobus gouldii) with forearm bands and PIT tags (with the injection site sealed with surgical adhesive) in January and February 2020 to determine rates of subsequent tag loss over the short- (1–2 months) and medium- (13–14 months) term. Loss of PIT tags occurred in 4 (2.7%) of 146 recaptured individuals, all within 2 months of microchipping. We also recorded 1 occurrence of band loss 11 months after banding. Our study supports assertions that PIT-tag retention rates in small mammals are high, and suggests that rates of tag loss in small bat species are low when surgical adhesive is applied. Quantifying the rate of tag loss enables this variable to be incorporated into mark-recapture models. © 2021 The Wildlife Society.