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.     

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.     

Movements of bonnetheads, <Emphasis Type="Italic">Sphyrna tiburo</Emphasis>, as a response to salinity change in a Florida estuary

The movement of bonnetheads, Sphyrna tiburo, within an estuarine system on the Gulf of Mexico coast of Florida was examined to define response to salinity change. Shark presence and movements were evaluated by acoustic monitoring and gillnet sampling. Acoustic monitoring data were used to investigate active selection of different zones within the estuary based on differences in salinity among zones. Sharks were monitored for 187 days in 2003 and 217 days in 2004 in salinities ranging from 11.0 to 31.0 ppt in 2003 and 15.8 to 34.6 ppt in 2004. Monitoring data supported the hypothesis that salinity played a role in the distribution and movement of S. tiburo. Catch per unit effort (CPUE) data obtained from gillnet sampling from 1995 to 2004 were examined to determine affinity or avoidance of specific salinities within the study site as calculated using an electivity index. Electivity analysis showed almost no affinity or avoidance for specific salinity values. The difference in results between the CPUE and acoustic monitoring in relation to the potential effects of salinity likely relate to the nature of the data, with acoustic monitoring providing continuous data and CPUE providing snapshot location data. The results of this study suggest that although S. tiburo are collected within a wide range of salinity levels, salinity may affect movement and distribution. Salinity effects may be more pronounced during periods of prolonged and/or large changes in salinity as detected by long-term monitoring.     

Functional morphology of the nasal region of a hammerhead shark

We describe several novel morphological features in the nasal region of the hammerhead shark Sphyrna tudes. Unlike the open, rounded incurrent nostril of non-hammerhead shark species, the incurrent nostril of S. tudes is a thin keyhole-like aperture. We discovered a groove running anterior and parallel to the incurrent nostril. This groove, dubbed the minor nasal groove to distinguish it from the larger, previously described, (major) nasal groove, is common to all eight hammerhead species. Using life-sized plastic models generated at 200 μm resolution from an X-ray scan, we also investigated flow in the nasal region. Even modest oncoming flow speeds stimulate extensive, but not complete, circulation within the model olfactory chamber, with flow passing through the two main olfactory channels. Flow crossed from one channel to another via a gap in the olfactory array, sometimes guided by the interlamellar channels. Major and minor nasal grooves, as well as directing flow into the olfactory chamber, can, in conjunction with the nasal bridge separating incurrent and excurrent nostrils, limit flow passing into the olfactory chamber, possibly to protect the delicate nasal structures. This is the first simulation of internal flow within the olfactory chamber of a shark.     

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.     

Population structure and cryptic speciation in bonnethead sharks Sphyrna tiburo in the south‐eastern U.S.A. and Caribbean

Population structure and lineage diversification within a small, non‐dispersive hammerhead shark species, the bonnethead shark Sphyrna tiburo, was assessed. Sphyrna tiburo is currently described as one continuously distributed species along the Atlantic continental margins of North, Central and South America, but recent genetic analysis of an insular population (Trinidad) suggests the possibility of cryptic speciation. To address this issue S. tiburo were sampled at six sites along c. 6200 km of continuous, continental coastline and from one island location (Grand Bahama) across a discontinuity in their distribution (the Straits of Florida), in order to test if they constitute a single lineage over this distribution. A total of 1030 bp of the mitochondrial control region (CR) was obtained for 239 S. tiburo, revealing 73 distinct haplotypes, high nucleotide diversity (0·01089) and a pair of highly divergent lineages estimated to have separated 3·61–5·62 million years ago. Mitochondrial cytochrome oxidase I and nuclear internal transcribed spacer loci show the same pattern. Divergence is similar within S. tiburo to that observed between established elasmobranch sister species, providing further evidence of cryptic speciation. A global AMOVA based on CR confirms that genetic diversity is primarily partitioned among populations (Φ_ST = 0·828, P < 0·001) because the divergent lineages are almost perfectly segregated between Belize and North America–The Bahamas. An AMOVA consisting solely of the North American and Bahamian samples is also significantly different from zero (Φ_ST = 0·088, P < 0·001) and pairwise F_ST is significantly different between all sites. These findings suggest that S. tiburo comprises a species complex and supports previous research indicating fine population structure, which has implications for fisheries management and biodiversity conservation.     

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.     

Placentation and associated aspects of gestation in the bonnethead shark, Sphyrna tiburo

The left ovary of the bonnethead shark, Sphyrna tiburo, is rudimentary, and the right ovary supplies both oviducts which share a common ostium situated in the falciform ligament. Preceding ovulation the nidamental gland of each oviduct hypertrophies and the caudal two-thirds of each oviduct is modified to form a uterus. In the Florida-Caribbean area Sphyrna tiburo probably mates in March and 3–7 eggs are fertilized in the vicinity of the nidamental gland of each oviduct. The developing embryo is nourished during the first 3–4 months of gestation by yolk stored in its extensive yolk sac. Approximately three and one-half months after fertilization, the distal portion of the yolk sac becomes convoluted and interdigitates with deep folds in the uterine wall to form a yolk-sac placenta. As the placenta develops, the maternal uterine epithelium is reduced from columnar cells to squamous cells, and the foetal yolk-sac epithelium is reduced from columnar and cuboidal cells to squamous cells. Exchange between the maternal and foetal blood systems takes place through maternal endothelium, reduced maternal epithelium, egg-case membrane, reduced foetal epithelium, and foetal endothelium.     

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.     

Head Morphology and Electrosensory Pore Distribution of Carcharhinid and Sphyrnid Sharks

Selection to maximize electroreceptive search area might have driven evolution of the cephalofoil head morphology of hammerhead sharks (family Sphyrnidae). The enhanced electrosensory hypothesis predicts that the wider head of sphyrnid sharks necessitates a greater number of electrosensory pores to maintain a comparable pore density. Although gross head morphology clearly differs between sphyrnid sharks and their closest relatives the carcharhinids, a quantitative examination is lacking. Head morphology and the distribution of electrosensory pores were compared between a carcharhinid, Carcharhinus plumbeus, and two sphyrnid sharks, Sphyrna lewini and S. tiburo. Both sphyrnids had greater head widths than the carcharhinid, although head surface area and volume did not differ between the three species. The raked head morphology of neonatal S. lewini pups, presumably an adaptation to facilitate parturition, becomes orthogonal to the body axis immediately post-parturition whereas this change is much less dramatic for the other two species. The general pattern of electrosensory pore distribution on the head is conserved across species despite the differences in gross head morphology. Sphyrna lewini has a mean of 3067 ± 158.9 SD pores, S. tiburo has a mean of 2028 ± 96.6 SD pores and C. plumbeus has a mean of 2317 ± 126.3 SD pores and the number of pores remains constant with age. Sphyrnids have a greater number of pores on the ventral surface of the head whereas C. plumbeus has an even distribution on dorsal and ventral surfaces. The greater number of pores distributed on a similar surface area provides S. lewini pups with a higher density of electrosensory pores per unit area compared to C. plumbeus pups. The greater number of ampullae, the higher pore density and the larger sampling area of the head combine to provide hammerhead sharks with a morphologically enhanced electroreceptive capability compared to comparably sized carcharhinids.     

Multiple substitutions and reduced genetic variability in sharks

The present study analyzed the genetic variability of the populations of four shark species (Carcharhinus limbatus, Carcharhinus porosus, Rhizoprionodon porosus, and Sphyrna tudes) from the Atlantic coast of the Amazon region. The analyses were based on the sequencing of the mitochondrial Control Region and Cytochrome b gene. S. tudes presented reduced diversity for both markers, which may be related to overexploitation by local fisheries. Most of the genetic variation in the four species was found in the 5′ portion of the Control Region, corresponding to a region of 210 bps, characterized by multiple substitutions (mutational hotspots) at the same sites. These mutations clearly biased the genetic diversity and affected the reliable of the analyses based exclusively on the Control Region. As Cytochrome b was not affected by these mutational events, this marker provided more reliable parameters for the evaluation of patterns of demographic expansion only for R. porosus. The present study indicated that the analysis of both markers is essential to guarantee the reliability of estimates of genetic variability, given that estimates based on the Control Region may be biased, and thus reduce the effectiveness of conservation and management measures designed to guarantee the long-term protection of stocks.     

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.     

Morphometrical analyses of northern Birch Mice (Sicista betulina Pallas, 1779; Mammalia; Rodentia) discovered in a rich locality from the Late Pleistocene of northwestern Switzerland

The discovery of 100 isolated teeth of Sicista betulina Pallas, 1779 in a doline filling of northwestern Switzerland (Vâ Tche Tchâ locality, Courtedoux, Ajoie) represents, in terms of richness, an exceptional occurrence for the Late Pleistocene of western Europe. This reference collection provides additional data for the identification of S. betulina, but also for the distinction of northern Birch Mice (S. betulina) and southern Birch Mice (S. subtilis) populations by morphometrical analyses (Mahlanobis distance, ratio diagrams) from isolated back teeth. Moreover, the determination of these two species is important for palaeoenvironmental studies, because they are associated to different biotopes.     

Interactions between root and shoot competition among four plant species in an alpine meadow on the Tibetan Plateau

At low altitudes, the interactions between root and shoot competition on plant growth have been extensively studied, and such interaction effects were found to be positive, negative, or neutral. However, little is known about such effects at high altitudes where the environmental conditions are harsher than those at low altitudes. We carried out a field experiment in an alpine meadow in the northeast Tibetan Plateau to test the hypothesis that a negative interaction between root and shoot competition exists for alpine plant species. Root and shoot competition were experimentally manipulated in the four grass species (Kobresia humilis, Saussurea superba, Stipa aliena and Elymus nutans). We found that K. humilis and S. aliena grew better without competition, whereas S. superba grew better with shoot competition and E. nutans grew better with root competition. The interactions between root and shoot competition were negative in K. humilis, positive in S. superba, but neutral in S. aliena and E. nutans, suggesting that the interaction effects are species-specific. This study also suggested that alpine plants may trade off both plant–plant interactions and competition shift between root and shoot to adapt to stressful environments.     

Eocene sand tiger sharks (Lamniformes,Odontaspididae) from the Bolca Konservat-Lagerstätte,Italy: palaeobiology,palaeobiogeography and evolutionary significance

Here we report the first record of one of the most common and widespread Palaeogene selachians, the sand tiger shark Brachycarcharias, from the Ypresian Bolca Konservat-Lagerstätte. The combination of dental character of the 15 isolated teeth collected from the Pesciara and Monte Postale sites (e.g. anterior teeth up to 25 mm with fairly low triangular cusp decreasing regularly in width; one to two pairs of well-developed lateral cusplets; root with broadly separated lobes; upper teeth with a cusp bent distally) supports their assignment to the odontaspidid Brachycarcharias lerichei (Casier, 1946), a species widely spread across the North Hemisphere during the early Palaeogene. The unambiguous first report of this lamniform shark in the Eocene Bolca Konservat-Lagerstätte improves our knowledge concerning the diversity and palaeobiology of the cartilaginous fishes of this palaeontological site, and provides new insights about the biotic turnovers that involved the high trophic levels of the marine settings after the end-Cretaceous extinction.     

Stomach content analysis of juvenile, scalloped hammerhead shark Sphyrna lewini captured off the coast of Mazatlán, Mexico

We quantified the diet of juvenile, scalloped hammerhead shark Sphyrna lewini in the area off Mazatlan, Sinaloa, Mexico, to understand their feeding ecology this shark. The prey species of Sphyrna lewini were identified and quantified from stomach content analysis. In addition, we determined the variations between genders. During two fishing seasons (2000–2001 and 2001–2002), we analyzed 232 stomachs, of which 85% contained food. The trophic spectrum was composed of three species of cephalopods, six of crustaceans and 19 species of fish from mainly pelagic and benthic habitats. According to the Index of Relative Importance (%IRI), the cephalopod Loliolopsis diomedeae with IRI = 18%, fish of the family Carangidae IRI = 25% and family Synodontidae IRI = 19% constituted the main prey in general. The trophic niche width was <0.4, which indicated that S. lewini juveniles in this area feed on a wide range of prey items, though they showed a preference for a few prey items.     

Respiratory and hematological responses of the bonnethead shark, Sphyrna tiburo, to acute changes in dissolved oxygen

Behavioral and physiological responses to acute changes in dissolved oxygen were examined in the bonnethead shark, Sphyrna tiburo. In two sets of respirometry experiments, sharks were randomly exposed to seawater in oxygen contents of 6.0, 5.0, 4.0 and 3.0 mg l⁻¹. During exposure, bonnetheads increased mouth gape from 0.8 cm at 6.0 mg l⁻¹ to 2.2 cm at 3.0 mg l⁻¹, while ventilation volume increased from 0.61 to 5.28 l min⁻¹ kg⁻¹. Standard oxygen consumption remained unchanged (163-181 mg O₂ kg⁻¹ h⁻¹) throughout all treatments and was not significantly different. Utilization (%) declined from 52.3% at 6.0 mg l⁻¹ to 21.3% when oxygen levels reached 3.0 mg l⁻¹. Changes in oxygen content of ambient water also caused no significant change in either blood oxygen content or hematocrit. Using cellulose acetate electrophoresis, a single hemoglobin profile was identified at seawater of 6.0 mg l⁻¹ and hypoxic conditions. Results suggest bonnetheads are physiologically able to tolerate moderate levels of hypoxia.     

Reproductive cycle and fecundity of the bonnethead Sphyrna tiburo L. from the northwest Atlantic Ocean

The present study examined temporal changes in plasma sex hormone concentrations and the morphology and histology of reproductive organs in mature northwest Atlantic (NWA) bonnetheads Sphyrna tiburo L. to characterize reproductive cycle, breeding periodicity and fertility in this still poorly studied population. Progressive increases in testis width, epididymis head width, plasma testosterone (T) concentrations, and occurrence of mature spermatozoa were observed in male S. tiburo from June to September, demonstrating that spermatogenesis occurs during the summer. Nonetheless, increases in maximum follicle diameter, oviducal gland width, plasma 17β-estradiol and T concentrations, and occurrence of vitellogenic follicles were not observed in mature females until between October and April, demonstrating non-synchronous patterns of gametogenesis in males and females. Fresh copulatory wounds were observed in females collected during late September along with histological evidence for sperm presence in the oviducal gland between September and April, confirming a 6- to 7 month period of female sperm storage. Ovulation occurred between mid-April and early May in concert with increases in female plasma progesterone concentrations. Gestation occurred during a 4.5- to 5 month period between May and early September, and 97% of mature females collected during this period were gravid, indicating a highly synchronized, annual reproductive periodicity. Brood size was significantly correlated with maternal size and ranged from 1 to 13 pups with a mean ± S.D. of 8.1 ± 2.2, which was significantly lower than reported in Gulf of Mexico (GOM) populations. The occurrence of non-fertile offspring was observed in 17% of broods with a range of 1–7 non-fertile eggs present in individual females. Thus, as previously reported in GOM S. tiburo, this unusual form of infertility also appears to be prevalent in the NWA population and requires further study. This study has demonstrated meaningful differences in reproductive biology of these populations, emphasizing the need for region-specific approaches for population management.     

Temporal priority effects on competition are not consistent among intermountain grassland species

Previous work indicates that priority effects exist, but mechanisms are not well understood. So we explored shifts in competitive outcomes and intensities as a potential general mechanism. In a standard greenhouse experiment the temporal priority effects of the target species Pseudoroegneria spicata and its competitive responses to five receptor species, i.e., Bromus ciliatus, Bromus marginatus, Coreopsis tinctoria, Senecio atratus, and Solidago canadensis were evaluated. P. spicata adults with a high root: shoot ratio had a significant inhibitory priority effect on B. ciliatus, B. marginatus, and C. tinctoria. Compared with the target species, under later and simultaneous sowing, B. ciliatus, B. marginatus, C. tinctoria, and S. atratus exhibited an increasing trend in terms of competition. However, S. canadensis did not display priority effects. In addition, the gram per gram competitive effect of P. spicata depended on the receptor species in the following order: B. marginatus > B. ciliatus > C. tinctoria > S. atratus. There were positive relationships between the relative interaction indices and the root: shoot ratios in B. ciliatus, B. marginatus, and C. tinctoria, thereby suggesting that the early germination or emergence of P. spicata may reduce the root: shoot ratios of these receptors. The results of this study indicate that priority effects occurred in early colonizers with high root: shoot ratios and greater competitive capacities.