Microstructural morphology in early dermal denticles of hammerhead sharks (Elasmobranchii: Sphyrnidae) and related taxa

Mello, W.C., de Carvalho, J.J., Brito, P.M.M. 2011. Microstructural morphology in early dermal denticles of hammerhead sharks (Elasmobranchii: Sphyrnidae) and related taxa. —Acta Zoologica (Stockholm) 00 : 1–7. This study uses scanning electron microscopies to investigate and describe the microstructural diversity of dermal denticles in the family Sphyrnidae, which comprises all living hammerhead shark species, comparing them to other related taxa (i.e. Carcharhinus dussumieri, Carcharhinus plumbeus, Carcharhinus acronotus, Rhizoprionodon acutus, Negaprion brevirostris and Hemigaleus microstoma). The results reveal that sphyrnids present noticeable microstructures in the dermal denticles, distinguishing them from the other related species investigated. Additionally, scale patterns are the same in three distinct body regions (i.e. cephalic, branchial and dorsal fin). Species of Sphyrnidae that reach bigger total lengths and that are widely distributed (i.e. Sphyrna lewini and Sphyrna mokarran) presented more, smaller and nearly hexagonal microstructures that do not cover the entire scale surface, unlike species reaching smaller sizes and restricted to coastal habits (i.e. Sphyrna tiburo, Sphyrna tudes, Sphyrna media and Eusphyra blochii). The sphyrnid scales are similar to R. acutus and C. dussumieri rather than to the other species, but it is not possible to identify the sphyrnid species only by scale features. It is clear that a similar morphology of scales is not necessarily related to similar life habits, and that they are candidates to provide new characters in phylogenetical studies among sphyrnids.     

Olfactory morphology of carcharhinid and sphyrnid sharks: Does the cephalofoil confer a sensory advantage?

Many hypotheses have been advanced to explain the adaptive significance of the sphyrnid cephalofoil, including potential advantages of spacing the olfactory organs at the distal tips of the broad surface. We employed comparative morphology to test whether the sphyrnid cephalofoil provides better stereo-olfaction, increases olfactory acuity, and samples a greater volume of the medium compared to the situation in carcharhiniform sharks. The broadly spaced nares provide sphyrnid species with a significantly greater separation between the olfactory rosettes, which could lead to an enhanced ability to resolve odor gradients. In addition, most sphyrnid species possess prenarial grooves that greatly increase the volume of water sampled by the nares and thus increase the probability of odorant encounter. However, despite a much greater head width, and a significantly greater number of olfactory lamellae, scalloped hammerhead sharks do not possess a greater amount of olfactory epithelial surface area than the carcharhiniform sandbar sharks. Therefore, sphyrnid sharks might not possess any greater olfactory acuity than carcharhinids. Despite this, there are clear olfactory advantages to the cephalofoil head morphology that could have led to its evolution, persistence, and diversification. persistence, and diversification.     

Maneuvering in juvenile carcharhinid and sphyrnid sharks: the role of the hammerhead shark cephalofoil

The peculiar head morphology of hammerhead sharks has spawned a variety of untested functional hypotheses. One of the most intuitively appealing ideas is that the anterior foil acts, as in canard-winged aircraft, to increase maneuverability. We tested this hypothesis by determining whether juveniles of two hammerhead species (Sphyrna tiburo and S. lewini) turn more sharply, more often, and with greater velocity than a juvenile carcharhinid shark (Carcharhinus plumbeus). Although the hammerheads were more maneuverable, further investigation revealed that they do not roll their body during turns, suggesting that the cephalofoil does not act as a steering wing. We also show that hammerhead sharks demonstrate greater lateral flexure in a turn than carcharhinids, and that this flexibility may be due to cross sectional shape rather than number of vertebrae.     

The storage of spermatozoa in the oviducal glands of western North Atlantic sharks

Synopsis Spermatozoa stored in oviducal glands of sharks sampled off the North American east coast were revealed by viewing stained tissue sections using light microscopy. Of eleven species surveyed, sperm were found in nine:Alopias vulpinus, Lamna nasus, Carcharhinus obscurus, Carcharhinus plumbeus, Galeocerdo cuvieri, Prionace glauca, Rhizoprionodon terraenovae, Sphyrna lewini andSphyrna tiburo. Three insemination patterns are proposed to account for differences noted in these findings: (1) non-storage/immediate insemination for sharks such asLamna nasus; (2) short-term storage/delayed insemination as found in sharks in which ovulation is prolonged over weeks or months such asRhizoprionodon terraenovae, and (3) long-term storage/repeated insemination, a characteristic of nomadic sharks such asPrionace glauca andCarcharhinus obscurus which can store sperm in specialized tubules for months to years.     

Contributions to the tooth morphology in early embryos of three species of hammerhead sharks (Elasmobranchii: Sphyrnidae) and their evolutionary implications

The tooth types in the embryos of the hammerhead sharks Sphyrna tiburo, Sphyrna tudes and Eusphyra blochii are here described in labial and lingual views, and, in some cases, in additional views. The presence of cusplets was observed in the anterior teeth of S. tiburo and S. tudes, which is secondarily lost after early embryonic stages. Many aligned root foramina were detected in the sphyrnids, which, as the cusplets, are shared by many phylogenetic-related carcharhinids. Other anatomic features, related to the root and central cusp, are presented for the first time. Such characters represent the first step to compare the teeth of extant and fossil species.     

A revision of Platybothrium Linton, 1890 (Tetraphyllidea: Onchobothriidae), with a phylogenetic analysis and comments on host-parasite associations

A revision of Platybothrium Linton, 1890 is presented, based on available type and voucher material, as well as extensive new collections from elasmobranchs belonging to the Carcharhinidae (requiem sharks) and Sphyrnidae (hammerhead sharks). All 10 nominal Platybothrium species are treated or redescribed herein. Four of these 10 nominal species, in addition to one former member of Dicranobothrium Euzet, 1953, are considered valid members of Platybothrium. Five new Platybothrium species are described: P. angelbahiense n. sp. ex Carcharhinus leucas, P. coshtaprum n. sp. ex C. plumbeus, P. jondoeorum n. sp. ex Negaprion acutidens and C. melanopterus, P. kirstenae n. sp. ex C. obscurus, and P. tantulum n. sp. ex Sphyrna lewini and S. zygaena. Sixty-three morphological characters were employed in cladistic analyses of nine Platybothrium species and five outgroup species. Coding and analysis strategies were varied to assess the effects of coding inapplicable characters as missing or as a separate character state, and of excluding characters for which data are missing in more than 10% of the taxa. The analysis in which inapplicable characters were coded as a separate character state and no characters were excluded produced the best-supported and most conservative estimate of the interrelationships of Platybothrium spp. Platybothrium appears to be a monophyletic assemblage, with the most basal species being P. spinulifera Southwell, 1912. The group of species possessing an accessory piece between the hooks forms a clade within the genus. Species lacking an accessory piece, which had previously been placed in Dicranobothrium Euzet, 1953, do not appear to be each other's closest relatives; thus, Dicranobothrium is considered a synonym of Platybothrium. An examination of host associations indicated that Platybothrium species are broadly distributed among, and entirely restricted to, carcharhinid and sphyrnid shark species. Most Platybothrium species exhibit oioxenous host-specificity, with all but two species each parasitising only a single host species. In several host species, multiple Platybothrium congeners parasitise the same host individual, a phenomenon not previously reported for Platybothrium.     

Catch composition and aspects of the biology of sharks caught by Thai commercial fisheries in the Andaman Sea

Catch composition, landing patterns and biological aspects of sharks caught by commercial fishing fleet operating in the Andaman Sea were recorded from landing sites in Ranong province of Thailand over a period of 1 year. Of the 64 species previously reported in the existing Thailand checklist, only 17 species were recorded in this study. Shark landings from the Andaman Sea appear now to be dominated largely by bamboo sharks Chiloscyllium spp. (Hemiscylliidae), which contribute c. 65% of the total number of sharks recorded. The carcharhinid sharks comprised c. 30·5% to the total catch, while the remaining c. 4·5% of landings comprised sharks from the families Squalidae, Stegostomatidae, Sphyrnidae and Triakidae. The catch composition is remarkably different from the previous landing survey in 2004, in that the current study found noticeable declines in landings of slow‐growing, late‐ maturing and low‐fecundity species (especially sphyrnid and carcharhinid species). The absences of many species and changes in life‐stage composition suggest that the populations of these groups may be close to collapse. The results from this study emphasize the urgency for additional research and monitoring efforts and also the need for management incentives in order to manage shark fisheries effectively in the Andaman Sea.     

Notes on the long‐term transport of the scalloped hammerhead shark (Sphyrna lewini)

The capture and transport of scalloped hammerhead sharks (Sphyrna lewini Griffith and Smith, 1834) historically has represented a difficult, expensive, and uncertain undertaking for the public aquarium community. In this study, techniques were developed to improve the successful long‐term transport of S. lewini by mitigating some of the deleterious effects associated with hyperactivity and impaired swimming patterns. The relationship between the transport vessel size and shark sizes, numbers, and swimming behavior was considered when formulating the transport regime. By balancing these factors and adopting a comprehensive water treatment method, it was possible to extend the duration of a successful transport by up to 60 hr. Implications for the future transport of S. lewini and other free‐swimming sharks are discussed. Zoo Biol 21:243–251, 2002. © 2002 Wiley‐Liss, Inc.     

Identification of young‐of‐the‐year great hammerhead shark Sphyrna mokarran in northern Florida and South Carolina

Two sharks, visually identified in the field as young‐of‐the‐year (YOY) scalloped hammerhead Sphyrna lewini, were identified as great hammerhead Sphyrna mokarran based on nuclear‐encoded single nucleotide polymorphisms (SNP) and sequences of mtDNA. Individuals were captured and released in Bulls Bay, SC, and Saint Joseph Bay, FL, in 2013 and 2014, respectively. These findings indicate S. mokarran may be pupping in or around these areas and highlight new regions that may be a productive focus for future research on early life history of S. mokarran.     

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.     

Phylogeography and population genetics of the cryptic bonnethead shark Sphyrna aff. tiburo in Brazil and the Caribbean inferred from mtDNA markers

Resolving the identity, phylogeny and distribution of cryptic species within species complexes is an essential precursor to management. The bonnethead shark, Sphyrna tiburo, is a small coastal shark distributed in the Western Atlantic from North Carolina (U.S.A.) to southern Brazil. Genetic analyses based on mitochondrial markers revealed that bonnethead sharks comprise a species complex with at least two lineages in the Northwestern Atlantic and the Caribbean (S. tiburo and Sphyrna aff. tiburo, respectively). The phylogeographic and phylogenetic analysis of two mitochondrial markers [control region (mtCR) and cytochrome oxidase I (COI)] showed that bonnethead sharks from southeastern Brazil correspond to S. aff. tiburo, extending the distribution of this cryptic species >5000 km. Bonnethead shark populations are only managed in the U.S.A. and in the 2000s were considered to be regionally extinct or collapsed in southeast Brazil. The results indicate that there is significant genetic differentiation between S. aff. tiburo from Brazil and other populations from the Caribbean (Φ_ST = 0.9053, P < 0.000), which means that collapsed populations in the former are unlikely to be replenished from Caribbean immigration. The species identity of bonnethead sharks in the Southwest Atlantic and their relationship to North Atlantic and Caribbean populations still remains unresolved. Taxonomic revision and further sampling are required to reevaluate the status of the bonnethead shark complex through its distribution range.     

Sex, seasonal, and stress-related variations in elasmobranch corticosterone concentrations

Serum corticosterone was previously studied in numerous elasmobranch fishes (sharks, skates and rays), but the role of this steroid, widespread throughout many taxa, has yet to be defined. The goal of this study was to test whether corticosterone varied in response to acute and chronic capture stress, and across the reproductive cycle in the bonnethead shark, Sphyrna tiburo, and Atlantic stingray, Dasyatis sabina. Serum corticosterone in S. tiburo increased following capture and again 24 h post-capture, possibly caused by interference with 1α-hydroxycorticosterone, the primary stress hormone in elasmobranchs. Higher serum concentrations in males compared to females were observed in both species. Variations in corticosterone also occurred during the reproductive cycle in both species. Consistent with other taxa, elevations in male bonnethead sharks and stingrays coincided with peak testicular development and mating. Elevations in female bonnethead sharks occurred from the time of mating through sperm storage into early gestation. In contrast, corticosterone levels in female stingrays were low during their protracted mating season, but elevated through late gestation and parturition. These results indicate that corticosterone has a limited role, if any, in acute and chronic stress associated with capture in S. tiburo, but likely has physiological functions associated with its glucocorticoid properties across the reproductive cycle of both species.     

Residency and movement patterns of bonnethead sharks, Sphyrna tiburo, in a large Florida estuary

The use of a coastal estuary by bonnethead sharks, Sphyrna tiburo, was examined by acoustic monitoring, gillnet sampling and tag- recapture studies. Acoustic monitoring data were used to define the residency and movement patterns of sharks within Pine Island Sound, Charlotte Harbor, Florida. Sharks were monitored for periods of 1–173 days with individuals regularly moving in and out of the detection range of the acoustic system. Patterns of movement could not be correlated with tidal level or time of day. Home range sizes within the Pine Island Sound population were typically small with individuals using core areas on a daily basis. However, core areas shifted within the study site over time resulting in eventual usage of most of the available habitat. Gillnet sampling revealed that S. tiburo were abundant in shallow water near seagrass beds, but that presence of individuals at specific sites was variable. Tag-recapture data showed that most individuals remained within the Pine Island Sound region over time and did not appear to undergo long coastal migrations. The movement and residence patterns of S. tiburo suggest that individuals are resident within the estuary, but do not show site fidelity to specific areas within the estuary.     

Bioenergetics of free-ranging juvenile scalloped hammerhead sharks (Sphyrna lewini) in Kāne'ohe Bay, ō'ahu, HI

Metabolic and activity rates determined from free-ranging juvenile scalloped hammerhead shark pups (Sphyrna lewini) in Kāne'ohe Bay, ō'ahu, HI, were used to develop a simplified energy budget for this population. Five shark pups were tracked using a specially designed acoustic tail beat transmitter. Previous laboratory experiments determined that tail beat frequency (TBF) and water temperature could be used as predictors of instantaneous swimming speed (U) and oxygen consumption rates (V?o₂). Sharks carrying transmitters had higher cost of transport than uninstrumented sharks, but because the difference was quantifiable, appropriate corrections could be made for transmitter effects on energy consumption of instrumented sharks. Sharks tracked in Kāne'ohe Bay had an overall average TBF of 70±10 beats min⁻¹ and a U of 0.81±0.1 body lengths s⁻¹, but swam significantly faster at night than during the day. These sharks also exhibited high average metabolic rates (MR) (96±15 kJ kg⁻¹ day⁻¹) compared with other species of sharks previously studied. Sharks tracked during warmer summer months swam slightly faster and exhibited higher MR than one tracked in December. The high MR measured for sharks in the bay indicate that these sharks require a high daily ration. The relatively low caloric value of the most common prey (snapping shrimp, Alpheus malabaricus) suggests that high numbers must be consumed to meet the sharks' daily requirements. Low and/or negative growth rates of shark pups in the field and declining population size over the summer season suggests that a significant percentage of pups in Kāne'ohe Bay may starve as the result of their high MR requirements. Although availability of A. malabaricus may not be limiting in Kāne'ohe Bay, foraging skills of some neonates may be inadequate to enable them to meet their daily energetic needs. However, sharks that are successful in surviving through the winter may actually grow faster in the colder months due to the temperature dependent decrease of their MR and a reduction in conspecific competition as the result of high summer seasonal attrition due to starvation and emigration.     

French naiad (Bivalvia: Margaritiferidae,Unionidae) species distribution models: prediction maps as tools for conservation

The aim of this study was to determine whether juvenile scalloped hammerhead sharks (Sphyrna lewini) use the south-eastern Gulf of California as a nursery and feeding area. This information could help lay the groundwork required for the conservation of this endangered species. To address this, we carried out stable isotope (δ¹⁵N and δ¹³C) and stomach content analyses of sharks caught between 2000 and 2004 in Mazatlan, Mexico. Stomach contents and δ¹³C values indicated that S. lewini is a predator that feeds on benthic prey near the coast. Differences in δ¹⁵N average values between sizes classes (<100 vs. >100 cm) suggest that there was an ontogenetic change in this shark’s feeding habits and also in their living environment (from benthic areas to pelagic areas). The trophic position indicated that S. lewini is a tertiary consumer, but with a high degree of trophic plasticity, and thus, different trophic roles, highlighting the importance of this predator as a regulator of prey populations. Finally, the linear isotopic relationship between S. lewini and its prey indicates a long residency within the Mazatlan area. Our results demonstrate that the south-eastern Gulf of California is a nursery area that offers abundant food for juvenile scalloped hammerhead sharks.     

Historical records reveal potential extirpation of four hammerhead sharks (Sphyrna spp.) in Mexican Pacific waters

Populations of hammerhead sharks (Sphyrna and Eusphyra) have declined in many regions of the world. Six of the eight hammerheads known to date are distributed in the Mexican Pacific: S. corona, S. lewini, S. media, S. mokarran, S. tiburo and S. zygaena. These species, with exception of S. corona, were abundant in the Gulf of California in 1960s. I analyze records from fishery-dependent and fishery-independent surveys, and records from ichthyological collections to determine the presence and frequency of hammerheads in the Mexican Pacific. The most frequent hammerheads in fishery-dependent and fishery-independent surveys were S. lewini and S. zygaena. It appears that S. media, S. mokarran and S. tiburo might have been extirpated from the Gulf of California. In the last two decades, records of S. mokarran (n = 61) were restricted to Central and Southern Mexican Pacific, and records of S. tiburo (n = 3) and S. media (n = 3) were restricted to the Southern region. Given the continued fishing pressure, inferred declines and the probable extirpation of populations, S. tiburo and S. media should be reassessed for the IUCN red list as Endangered or Critically Endangered. Sphyrna corona should be reassessed as Endangered or Critically Endangered, because it is endemic to the Eastern Pacific and recent records have been obtained only from Colombian waters. The Endangered status of S. mokarran is confirmed for this region.     

Vulnerability to longline fisheries of three hammerhead shark Sphyrna species in the south‐western and equatorial Atlantic Ocean

Catch and effort data from 29 418 longline sets from Brazilian tuna longline vessels operating in the south‐western and equatorial Atlantic Ocean between 2004 and 2011 were analysed to investigate the distribution, catch rate and size of three species of hammerhead sharks (Sphyrna lewini, Sphyrna mokarran and Sphyrna zygaena). During that period, 6172 hammerhead sharks were caught. Among the elasmobranchs, the highest percentage of hammerhead sharks were caught in 2007, when they accounted for 3·90% of the group, while the lowest value of 0·40% was recorded in 2010. In general, the spatial distribution of the mean catch per unit effort (CPUE) by years and quarters showed a trend of higher catches near the equatorial region and in southern Brazil. The nominal mean CPUE was 0·12 Sphyrna spp. 1000⁻¹ hooks, with the highest value being recorded in 2007 (0·30 Sphyrna spp. 1000⁻¹ hooks). The standardized yearly CPUE estimated by a generalized linear model assuming a zero inflated negative binomial (ZINB) distribution were not much different from nominal values. Of the 205 sexed specimens, 117 were females and 88 were males, resulting in a sex ratio with a predominance of females (1·30:1·00), although not statistically significant. The total length of females ranged from 1200 to 2800 mm and of males from 1100 to 3100 mm. Juvenile hammerhead sharks represented 82 and 54% of the sexed female and male specimens, respectively.     

Potential expansion in the spatial distribution of subtropical and temperate west Australian sharks

Fishery-dependent and -independent data collected since 1975 were examined to explore the spatial distribution of 30 shark and ray species in the west coast of Australia. Bigeye sixgill (Hexanchus nakamurai), tiger (Galeocerdo cuvier) and spinner (Carcarhinus brevipinna) sharks, and scalloped hammerhead (Sphyrna lewini) were observed >1000 and 300 km to the east of the edge of their reported distributions. Broadnose sevengill sharks (Notorhyncus cepedianus) and southern sawsharks (Pristiophorus nudipinnis) were observed >1000 km to the west of the edge of their reported distributions. Our study highlights the value of collecting and examining long time-series of data for understanding the spatial distribution of large marine predators.     

Feeding ecology and trophic comparisons of six shark species in a coastal ecosystem off southern Brazil

The diets of six shark species, Sphyrna lewini, Sphyrna zygaena, Carcharhinus obscurus, Carcharhinus limbatus, Rhizoprionodon lalandii and Galeocerdo cuvier, were investigated in a subtropical coastal ecosystem of southern Brazil. Stomach content data were obtained to assess foraging niche segregation and ontogenetic shifts in the diets of these sharks. Five of the shark species off the Paraná coast were ichthyophagous, with the exception of S. zygaena, which was teutophagous. With the exception of G. cuvier, which had a generalist diet, the other five species displayed specialization in their feeding. Ontogenetic shifts were observed in C. obscurus and S. lewini with large individuals consuming elasmobranchs. Owing to the diet overlap between C. obscurus and S. lewini, C. obscurus and C. limbatus and R. lalandii and C. limbatus, future studies on the spatial and temporal distributions of these species are needed to understand the extent of competitive interactions.