Do sharks exhibit heterodonty by tooth position and over ontogeny? A comparison using elliptic Fourier analysis

Tooth morphology is often used to inform the feeding ecology of an organism as these structures are important to procure and process dietary resources. In sharks, differences in morphology may facilitate the capture and handling of prey with different physical properties. However, few studies have investigated differences in tooth morphology over ontogeny, throughout the jaws of a single species, or among species at multiple tooth positions. Bull (Carcharhinus leucas), blacktip (Carcharhinus limbatus), and bonnethead sharks (Sphyrna tiburo) are coastal predators that exhibit ontogenetic dietary shifts, but differ in their feeding ecologies. This study measured tooth morphology at six positions along the upper and lower jaws of each species using elliptic Fourier analysis to make comparisons within and among species over their ontogeny. Significant ontogenetic differences were detected at four of the six tooth positions in bull sharks, but only the posterior position on the lower jaw appeared to exhibit a functionally relevant shift in morphology. No ontogenetic changes in morphology were detected in blacktip or bonnethead sharks. Intraspecific comparisons found that most tooth positions significantly differed from one another across all species, but heterodonty was greatest in bull sharks. Additionally, interspecific comparisons found differences among all species at each tooth position except between bull and blacktip sharks at two positions. These morphological patterns within and among species may have implications for prey handling efficiency, as well as in providing insight for paleoichthyology studies and reevaluating heterodonty in sharks.     

Microsatellite Analyses of Blacktip Reef Sharks (Carcharhinus melanopterus) in a Fragmented Environment Show Structured Clusters

The population dynamics of shark species are generally poorly described because highly mobile marine life is challenging to investigate. Here we investigate the genetic population structure of the blacktip reef shark (Carcharhinus melanopterus) in French Polynesia. Five demes were sampled from five islands with different inter-island distances (50–1500 km). Whether dispersal occurs between islands frequently enough to prevent moderate genetic structure is unknown. We used 11 microsatellites loci from 165 individuals and a strong genetic structure was found among demes with both F-statistics and Bayesian approaches. This differentiation is correlated with the geographic distance between islands. It is likely that the genetic structure seen is the result of all or some combination of the following: low gene flow, time since divergence, small effective population sizes, and the standard issues with the extent to which mutation models actually fit reality. We suggest low levels of gene flow as at least a partial explanation of the level of genetic structure seen among the sampled blacktip demes. This explanation is consistent with the ecological traits of blacktip reef sharks, and that the suitable habitat for blacktips in French Polynesia is highly fragmented. Evidence for spatial genetic structure of the blacktip demes we studied highlights that similar species may have populations with as yet undetected or underestimated structure. Shark biology and the market for their fins make them highly vulnerable and many species are in rapid decline. Our results add weight to the case that total bans on shark fishing are a better conservation approach for sharks than marine protected area networks.     

Estimation of Shark Home Ranges using Passive Monitoring Techniques

We examined a population of blacktip sharks, Carcharhinus limbatus, within a coastal nursery area to define how individuals use the nursery habitat throughout the summer. We used a series of acoustic hydrophones to passively monitor the movement patterns of sharks for periods up to 167 days. We used passive monitoring data to calculate home range estimates using minimum convex polygon (MCP) and fixed kernel estimators. MCP calculated the extent of an individual's range. Kernel estimates provided information regarding the utilization of space within the home range including core area (50% kernel) and larger excursions outside the core area (95% kernel). Individuals within the nursery area typically used a consistently small core area. All sharks monitored in the study site underwent a home range expansion during the month of July, suggesting a synchronous population-level change in habitat use. This change in habitat use was reflected in all home range calculations. Passive monitoring revealed that young sharks remain within the nursery area for up to 6 months. The long-term use of this nursery area reflects its critical importance to young blacktip sharks.     

Antibiotic Susceptibilities of Bacteria Isolated within the Oral Flora of Florida Blacktip Sharks: Guidance for Empiric Antibiotic Therapy

Sharks possess a variety of pathogenic bacteria in their oral cavity that may potentially be transferred into humans during a bite. The aim of the presented study focused on the identification of the bacteria present in the mouths of live blacktip sharks, Carcharhinus limbatus, and the extent that these bacteria possess multi-drug resistance. Swabs were taken from the oral cavity of nineteen live blacktip sharks, which were subsequently released. The average fork length was 146 cm (±11), suggesting the blacktip sharks were mature adults at least 8 years old. All swabs underwent standard microbiological work-up with identification of organisms and reporting of antibiotic susceptibilities using an automated microbiology system. The oral samples revealed an average of 2.72 (±1.4) bacterial isolates per shark. Gram-negative bacteria, making up 61% of all bacterial isolates, were significantly (p<0.001) more common than gram-positive bacteria (39%). The most common organisms were Vibrio spp. (28%), various coagulase-negative Staphylococcus spp. (16%), and Pasteurella spp. (12%). The overall resistance rate was 12% for all antibiotics tested with nearly 43% of bacteria resistant to at least one antibiotic. Multi-drug resistance was seen in 4% of bacteria. No association between shark gender or fork length with bacterial density or antibiotic resistance was observed. Antibiotics with the highest overall susceptibility rates included fluoroquinolones, 3^rd generation cephalosporins and sulfamethoxazole/trimethoprim. Recommended empiric antimicrobial therapy for adult blacktip shark bites should encompass either a fluoroquinolone or combination of a 3^rd generation cephalosporin plus doxycycline.     

Dionchus postoncomiracidia (Monogenea: Dionchidae) from the skin of blacktip sharks, Carcharhinus limbatus (Carcharhinidae)

Postoncomiracidia of Dionchus sp. are described from specimens collected from the skin of 2 blacktip sharks Carcharhinus limbatus, captured in the northern Gulf of Mexico. The parasites resemble nonciliated oncomiracidia hatched from eggs laid by Dionchus sp. on gills of a cobia Rachycentron canadum and adults of Dionchus remorae that were collected from gills of a common sharksucker Echeneis naucrates, captured in association with a third blacktip shark. The hamuli of the postoncomiracidia were morphologically similar to those of adult D. remorae. This is the first report of dionchids from an elasmobranch and from a location other than the gills. These findings support the idea that some dionchid oncomiracidia colonize the skin of sharks or other aquatic vertebrates that sponsor remoras, prior to transferring to other remoras and maturing.     

Using unmanned aerial vehicle (UAV) surveys and image analysis in the study of large surface‐associated marine species: a case study on reef sharks Carcharhinus melanopterus shoaling behaviour

A novel image analysis‐based technique applied to unmanned aerial vehicle (UAV) survey data is described to detect and locate individual free‐ranging sharks within aggregations. The method allows rapid collection of data and quantification of fine‐scale swimming and collective patterns of sharks. We demonstrate the usefulness of this technique in a small‐scale case study exploring the shoaling tendencies of blacktip reef sharks Carcharhinus melanopterus in a large lagoon within Moorea, French Polynesia. Using our approach, we found that C. melanopterus displayed increased alignment with shoal companions when distributed over a sandflat where they are regularly fed for ecotourism purposes as compared with when they shoaled in a deeper adjacent channel. Our case study highlights the potential of a relatively low‐cost method that combines UAV survey data and image analysis to detect differences in shoaling patterns of free‐ranging sharks in shallow habitats. This approach offers an alternative to current techniques commonly used in controlled settings that require time‐consuming post‐processing effort.     

New insights into the trophic ecology of blacktip sharks (Carcharhinus limbatus) from a subtropical estuary in the western Gulf of Mexico

As environmental change persists, understanding resource use patterns is of value to predict the consequences of shifting trophic structures. While many sharks are opportunistic predators, some exhibit prey selectivity, putting them at higher risk compared to species with greater trophic plasticity. In the Gulf of Mexico (GOM), Clupeids and Sciaenids comprise 69% of blacktip shark (Carcharhinus limbatus) diets, which is consequential considering potential responses of these prey groups to disturbance and over harvesting. We assessed if blacktips exhibit selectivity for Clupeids and Sciaenids in the western GOM based on stomach contents from sharks in coastal Texas. Clupeids comprised <2% of diets, while striped mullet (Mugil cephalus) and red drum (Sciaenops ocellatus) comprised >70% of identifiable prey. Ontogenetic shifts from smaller (Clupeids, small Sciaenids) to larger, higher trophic level (Ariidae, Elasmobranchii) prey fits our understanding of foraging among coastal sharks, and suggests our regional understanding of blacktip trophic ecology may be limited by the sizes of sampled sharks. Observed increases in blacktip densities coupled with declines in prey (Mugilids, Sciaenids) is concerning if blacktips have limited diet plasticity. Yet GOM blacktips may be more generalized than previously thought, which is promising for conservation and management.     

The response of gastric pH and motility to fasting and feeding in free swimming blacktip reef sharks, Carcharhinus melanopterus

In many fish and reptiles, gastric digestion is responsible for the complete breakdown of prey items into semi-liquid chyme. The responses of the stomach to feeding and to periods of fasting are, however, unknown for many lower vertebrates. We inserted data loggers into the stomachs of free-swimming captive adult blacktip reef sharks (Carcharhinus melanopterus) to quantify gastric pH, motility and temperature during fasting and following ingestion of food. Gastric acid secretion was continuous, even during long periods of fasting, with a mean pH of 1.66 ± 0.40 (± 1 SD) when the stomach was empty. Stomach contractions were greater following meals of mackerel than for those of squid. Gastric motility following feeding on mackerel, was positively influenced by ambient temperature, and followed a quadratic relationship with meal size, with maximum motility occurring after meals of 0.8-1.0% body weight. Diel changes in gastric motility were apparent, and were most likely caused by diel changes in ambient temperature. Gastric digestion in blacktip reef sharks is affected by both biotic and abiotic variables. We hypothesize that behavioral strategies adopted by sharks in the field may be an attempt to optimize digestion by selecting for appropriate environmental conditions.     

Diel movements of the blacktip shark (<Emphasis Type="Italic">Carcharhinus limbatus</Emphasis>) in a Caribbean nursery

The blacktip shark (Carcharhinus limbatus) is a common coastal species in tropical and subtropical waters around the world. To examine the fine-scale movement ecology of this species in a Caribbean nursery, 17 neonate blacktip sharks were acoustically tagged in May, 2012 and tracked for one year in Coral Bay, St John, USVI. By quantifying linear movement and shifts in position from a fixed Inner harbor location, we identified a diel movement pattern where blacktip sharks spend daylight hours within core habitat of Inner Coral Harbor and move each night to the central and outer portions of the Bay, a linear shift of 174–934 m. When compared to standard home range calculations applied to the overall movement data, these nightly positions were outside of the 95% activity space and, therefore, undetected using traditional space utilization methods, despite their predictable daily occurrence. Cluster analysis and nonmetric multidimensional scaling indicated distinct movement periods and locations: daytime (sun up) within Inner Coral Harbor; nighttime (sun down) in the center of the Bay; and brief periods approximately six hours after sunset at the mouth of the Bay. This diel shift in habitat use is likely associated with nocturnal foraging because it coincides with similar shifts in potential prey species. Habitat and resource management that incorporates the blacktip shark movements described herein is critical to the protection of these vulnerable life stages. The findings of this paper advance the understanding of blacktip shark behavior and acoustic telemetry experimental design.     

Spatial separation without territoriality in shark communities

Spatial separation within predator communities can arise via territoriality but also from competitive interactions among and within species. However, linking competitive interactions to predator distribution patterns is difficult and theoretical models predict different habitat selection patterns dependent on habitat quality and how competition manifests itself. While models generally consider competitors to be either equal in ability, or for one phenotype to have a fixed advantage over the other, few studies consider that an animal may only have a competitive advantage in specific habitats. We used  10 years of telemetry data, habitat surveys and behavioral experiments, to show spatial partitioning between and within two species of reef shark (grey reef Carcharhinus amblyrhinchos and blacktip reef sharks C. melanopterus) at an unfished Pacific atoll. Within a species, sharks remained within small ‘sub‐habitats’ with very few movements of individuals between sub‐habitats, which previous models have suggested could be caused by intra‐specific competition. Blacktip reef sharks were more broadly distributed across habitat types but a greater proportion used lagoon and backreef habitats, while grey reef sharks preferred forereef habitats. Grey reef sharks at a nearby atoll where blacktip reef sharks are absent, were distributed more broadly between habitat types than when both species were present. A series of individual‐based models predict that habitat separation would only arise if there are competitive interactions between species that are habitat‐specific, with grey reefs having a competitive advantage on the forereefs and blacktips in the lagoons and backreef. We provide compelling evidence that competition helps drive distribution patterns and spatial separation of a marine predator community, and highlight that competitive advantages may not be constant but rather dependent on habitats.     

Shark bite wounds of the valvular intestine: The cause of an acute mortality syndrome of captive blacktip reef sharks,Carcharhinus melanopterus

During 1987–1990 nine cases of mortality in captive blacktip reef sharks (Carcharhinus melanopterus) were attributed to bite wounds to the valvular intestine. Necropsies revealed lacerations, amputation of the scroll valve folds, or complete severance of the valvular intestine. Wounding resulting from attack by tankmates occurred during episodes of intestinal eversion, an apparently regular event of unclear physiological function in sharks with a scroll valve intestine. This paper adds intestinal biting as a putative cause of mortality in captive shark species having a scroll valve intestine.     

Responses of a coral reef shark acutely exposed to ocean acidification conditions

Anthropogenic ocean acidification (OA) is a threat to coral reef fishes, but few studies have investigated responses of high-trophic-level predators, including sharks. We tested the effects of 72-hr exposure to OA-relevant elevated partial pressures of carbon dioxide (pCO₂) on oxygen uptake rates, acid–base status, and haematology of newborn tropical blacktip reef sharks (Carcharhinus melanopterus). Acute exposure to end-of-century pCO₂ levels resulted in elevated haematocrit (i.e. stress or compensation of oxygen uptake rates) and blood lactate concentrations (i.e. prolonged recovery) in the newborns. Conversely, whole blood and mean corpuscular haemoglobin concentrations, blood pH, estimates of standard and maximum metabolic rates, and aerobic scope remained unaffected. Taken together, newborn blacktip reef sharks appear physiologically robust to end-of-century pCO₂ levels, but less so than other, previously investigated, tropical carpet sharks. Our results suggest peak fluctuating pCO₂ levels in coral reef lagoons could still physiologically affect newborn reef sharks, but studies assessing the effects of long-term exposure and in combination with other anthropogenic stressors are needed.

     

A novel field method to distinguish between cryptic carcharhinid sharks,Australian blacktip shark Carcharhinus tilstoni and common blacktip shark C. limbatus,despite the presence of hybrids

Multivariate and machine‐learning methods were used to develop field identification techniques for two species of cryptic blacktip shark. From 112 specimens, precaudal vertebrae (PCV) counts and molecular analysis identified 95 Australian blacktip sharks Carcharhinus tilstoni and 17 common blacktip sharks Carcharhinus limbatus. Molecular analysis also revealed 27 of the 112 were C. tilstoni × C. limbatus hybrids, of which 23 had C. tilstoni PCV counts and four had C. limbatus PCV counts. In the absence of further information about hybrid phenotypes, hybrids were assigned as either C. limbatus or C. tilstoni based on PCV counts. Discriminant analysis achieved 80% successful identification, but machine‐learning models were better, achieving 100% successful identification, using six key measurements (fork length, caudal‐fin peduncle height, interdorsal space, second dorsal‐fin height, pelvic‐fin length and pelvic‐fin midpoint to first dorsal‐fin insertion). Furthermore, pelvic‐fin markings could be used for identification: C. limbatus has a distinct black mark >3% of the total pelvic‐fin area, while C. tilstoni has markings with diffuse edges, or has smaller or no markings. Machine learning and pelvic‐fin marking identification methods were field tested achieving 87 and 90% successful identification, respectively. With further refinement, the techniques developed here will form an important part of a multi‐faceted approach to identification of C. tilstoni and C. limbatus and have a clear management and conservation application to these commercially important sharks. The methods developed here are broadly applicable and can be used to resolve species identities in many fisheries where cryptic species exist.     

Analysis of Sharksucker, Echeneis naucrates, Induced Behavior Patterns in the Blacktip Shark, Carcharhinus limbatus

I analyzed and quantified the behavior of blacktip sharks, Carcharhinus limbatus, irritated by sharksuckers, Echeneis naucrates, attached to their bodies. The sharksucker induced behavior patterns were divided into simple rotational patterns, expressed by body turns along their main axes (roll, yaw, pitch); and complex patterns (wiggle, shake, wind, chafe), consisting of a combination or a repetition of simple behavior patterns. Three nonrotational behavior patterns were also observed (freeze, yawn, flicker). Of the 78 blacktip sharks examined, 70 performed either a simple or a complex pattern, or a combination of the two types. Of the total 195 rotational behavior patterns observed, only three wind patterns, performed as chaffing, led to the dislocation of a sharksucker, implying that the shark's primary intention may not be to shake off the teleost, but to initiate a position change to a less sensitive part of its body. Three sharks showed behavior patterns resembling typical agonistic display patterns, but they were induced by sharksuckers, not triggered by the presence of humans.     

Metabolic rates and the energetic cost of external tag attachment in juvenile blacktip sharks Carcharhinus limbatus

This study reports on the metabolic rate of the blacktip shark Carcharhinus limbatus and the energetic costs of external tag attachment. Metabolic rates, swimming speed and tail‐beat (B_T) frequency were measured in a static respirometer with untagged animals and animals equipped with a small data logger. Tagged sharks showed significantly higher routine oxygen consumption and lower swimming speeds than untagged animals, indicating that tagging significantly affected the swimming efficiency and energetic requirements in these small sharks, and that these effects must be accounted for when interpreting telemetry data from free‐ranging individuals.     

Skin lesions caused by Dermophthirius penneri (Monogenea: Microbothriidae) on wild-caught blacktip sharks (Carcharhinus limbatus)

Skin lesions caused by the ectoparasite Dermophthirius penneri Benz, 1987 (Monogenea: Microbothriidae) on 2 wild-caught blacktip sharks (Carcharhinus limbatus) from the northern Gulf of Mexico were studied using light and scanning electron microscopy. Grossly, lesions appeared as multifocal, well-demarcated, ovoid or irregularly shaped, light gray patches of skin. Scanning electron microscopy of lesions revealed gaps between placoid scales apparently created by detachment and loss of placoid scales, rotated and tilted placoid scales with blunt distal tips and shallow ridges, and a frayed epithelium that covered some placoid scales and filled some spaces between placoid scales. Light microscopy of lesions revealed epithelial hyperplasia accompanied by dermal infiltrates of moderate numbers of loosely arranged lymphocytes interposed between collagen bundles in the superficial layers of the stratum compactum. This report provides the first details of microbothriid skin lesions on wild sharks. Our results indicate that D. penneri caused chronic skin lesions not associated with bacterial infection or severe, debilitating, skin disease in the studied sharks.     

Morphological scaling of body form in four shark species differing in ecology and life history

Body form can change across ontogeny, and can influence how animals of different sizes move and feed. Scaling data on live apex predatory sharks are rare and, therefore, we examined patterns of scaling in ontogenetic series of four sympatric shark species exhibiting a range of sizes, ecologies and life histories (tiger, bull, blacktip, and nurse shark). We evaluated 13 linear morphological variables and two areas (caudal and dorsal) that could influence both animal condition and locomotor performance. These measurements included dimensions of the dorsal, pectoral, and caudal fins, as well as several dimensions of body circumference, and of the head. For all four species, the body axis (eye‐to‐eye, lateral span, frontal span, proximal span) scaled close to isometry (expected slope of 1.0). The two largest sharks (tiger and bull sharks) also showed significant negative allometry for elements of the caudal fin. We found significant negative allometry in the lengths of the upper lobe of the caudal fin (caudal fin 1) and the overall height of the caudal fin (caudal fin 2) in tiger and bull sharks, with slopes ranging from about 0.60 to 0.73. Further, tiger sharks showed negative allometry in caudal fin area. These results suggest that in terms of overall body dimensions, small sharks are roughly geometrically similar to large sharks, at least within the species we examined. However, juvenile tiger (and to a lesser extent bull sharks) are notable in having proportionately larger caudal fins compared to adult sharks. As the caudal fin contributes to generating thrust during forward locomotion, this scaling implies differences among adult and juvenile sharks in locomotor ability. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 126–135.     

Exclusive predation of sea turtle hatchlings by juvenile blacktip reef sharks Carcharhinus melanopterus at a turtle nesting site in Malaysia

This study reports the discovery of the exclusive predation of sea turtle hatchlings by several juvenile blacktip reef sharks (Carcharhinus melanopterus) in Chagar Hutang bay on Redang Island, Malaysia, in the South China Sea. Three dead specimens of C. melanopterus were retrieved from ghost nets, and the entire digestive tracts of these sharks solely contained the partially digested bodies of sea turtle hatchlings, with no evidence of the remains of any other prey. Thus, juvenile C. melanopterus may opportunistically feed primarily on turtle hatchlings during times when hatchling abundance is high.     

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.     

Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea

Abstract We investigated the genetic structure of blacktip shark (Carcharhinus limbatus) continental nurseries in the northwestern Atlantic Ocean, Gulf of Mexico, and Caribbean Sea using mitochondrial DNA control region sequences and eight nuclear microsatellite loci scored in neonate and young-of-the-year sharks. Significant structure was detected with both markers among nine nurseries (mitochondrial PhiST = 0.350, P < 0.001; nuclear PhiST = 0.007, P < 0.001) and sharks from the northwestern Atlantic, eastern Gulf of Mexico, western Gulf of Mexico, northern Yucatan, and Belize possessed significantly different mitochondrial DNA haplotype frequencies. Microsatellite differentiation was limited to comparisons involving northern Yucatan and Belize sharks with nuclear genetic homogeneity throughout the eastern Gulf of Mexico, western Gulf of Mexico, and northwestern Atlantic. Differences in the magnitude of maternal vs. biparental genetic differentiation support female philopatry to northwestern Atlantic, Gulf of Mexico, and Caribbean Sea natal nursery regions with higher levels of male-mediated gene flow. Philopatry has produced multiple reproductive stocks of this commercially important shark species throughout the range of this study.