Functional morphology of the feeding apparatus,feeding constraints,and suction performance in the nurse shark Ginglymostoma cirratum

The nurse shark, Ginglymostoma cirratum, is an obligate suction feeder that preys on benthic invertebrates and fish. Its cranial morphology exhibits a suite of structural and functional modifications that facilitate this mode of prey capture. During suction‐feeding, subambient pressure is generated by the ventral expansion of the hyoid apparatus and the floor of its buccopharyngeal cavity. As in suction‐feeding bony fishes, the nurse shark exhibits expansive, compressive, and recovery kinematic phases that produce posterior‐directed water flow through the buccopharyngeal cavity. However, there is generally neither a preparatory phase nor cranial elevation. Suction is generated by the rapid depression of the buccopharyngeal floor by the coracoarcualis, coracohyoideus, and coracobranchiales muscles. Because the hyoid arch of G. cirratum is loosely connected to the mandible, contraction of the rectus cervicis muscle group can greatly depress the floor of the buccopharyngeal cavity below the depressed mandible, resulting in large volumetric expansion. Suction pressures in the nurse shark vary greatly, but include the greatest subambient pressures reported for an aquatic‐feeding vertebrate. Maximum suction pressure does not appear to be related to shark size, but is correlated with the rate of buccopharyngeal expansion. As in suction‐feeding bony fishes, suction in the nurse shark is only effective within approximately 3 cm in front of the mouth. The foraging behavior of this shark is most likely constrained to ambushing or stalking due to the exponential decay of effective suction in front of the mouth. Prey capture may be facilitated by foraging within reef confines and close to the substrate, which can enhance the effective suction distance, or by foraging at night when it can more closely approach prey. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Behavioural responses of fishes to chemical cues: results from a new bioassay

A new behavioural bioassay for determining the locomotor response by fish to chemical cues is described. The assay combines a behavioural trough, capable of delivering up to 10 discrete plumes of treated water, together with a digital method for quantifying the movements of single fish. Sample responses of two whitefish, Coregonus clupeaformis , one to an attractant (a food extract) and one to a repellant (quinine monohydrochloride), are provided. Their locomotor responses are analyzed in terms of such parameters as total distance travelled, average velocity, number of turns, average excursion distance, and the number of times specific boundaries are crossed. The assay's sensitivity is demonstrated through concentration-response curves by Arctic char, Salvelinus alpinus , to the bile acid, taurocholic acid, and the amino acids, L-serine and L-alanine. Behavioural response threshold concentrations for these three substances were estimated to be 10⁻¹⁵, 10⁻ⁿ, and 10⁻⁹ m, respectively.     

To go or not to go with the flow: Environmental influences on whale shark movement patterns

Seven whale sharks were tracked using satellite-linked tags from Ningaloo Reef, off northern Western Australia, following tagging in April and June 2002 and April-May 2005. We investigated how the movements of those whale shark tracks were influenced by geostrophic surface currents during sequential one-week periods by using a passive diffusion model parameterised with observed starting locations of the sharks and weekly maps of surface current velocity and direction (derived from altimetry). We compared the outputs from the passive diffusion model and maps of chlorophyll-a concentration (SeaWiFs/MODIS) and with the actual tracks of the sharks using GIS and generalized linear mixed-effects models (GLMM). The GLMM indicated very little support for passive diffusion with sea-surface ocean currents influencing whale shark distributions in the north eastern Indian Ocean. Moreover, the sharks' movements correlated only weakly with the spatial distribution of sea-surface chlorophyll-a concentrations. The seven whale sharks had average swimming speeds comparable with those recorded in other satellite tracking studies of this species. Swimming speeds of the seven sharks were similar to those reported in previous studies and up to three times greater than the maximum sea-surface current velocities that the sharks encountered while traversing into lower southerly latitudes (moving northward towards the equator). Our results indicate that whale sharks departing from Ningaloo travel actively and independently of near-surface currents where they spend most of their time despite additional metabolic costs of this behaviour.     

Modulation in Feeding Kinematics and Motor Pattern of the Nurse Shark <Emphasis Type="Italic">Ginglymostoma cirratum</Emphasis>

Synopsis Studies of feeding in bony fishes have almost universally demonstrated the ability of individuals to modulate their method of capture in response to differing stimuli. Preliminary evidence indicates that morphologically specialized inertial suction feeding sharks are the most likely fishes to lack inherent modulatory ability. We examined the ability of the nurse shark, Ginglymostoma cirratum, to modulate its feeding behavior based on different food types and sizes. G. cirratum is an inertial suction feeding fish that is apparently stereotyped in its food capture behavior. Electromyography showed no statistical difference between feeding motor patterns based on food type (squid or fish) or size (gape width or twice gape width), although there were slight inter-individual differences in the onset of muscle firing for some muscles. Kinematic analysis showed a statistical difference in variables associated with durations for different food types, with the durations for all variables being faster for squid bites than fish bites, but no difference based on the size of the food item. This apparent lack of modulation may be associated with specialization of the morphology and behavior of G. cirratum for obligate suction prey capture. This functional specialization constrains the method in which G. cirratum captures prey but does not appear to result in dietary specialization. An unusual post capture spit-suck manipulation allows this shark to handle and ingest large prey.     

Movement patterns and gallery use by the sexually dimorphic Wellington tree weta

The Wellington tree weta, Hemideina crassidens, is a harem-polygynous nocturnal insect whose males defend and mate groups of females residing in cavities in trees. In this study I examined sexual differences in gallery use (number of galleries occupied per unit time), distance travelled per night and activity patterns after sunset. In addition, I investigated how gallery size affected each of these variables. On average, males and females did not differ in the number of galleries visited per night, or in the distance they travelled per night; however, adult males were more likely to be seen earlier in the night than later. Although males and females did not differ in their gallery use or distance travelled, adult males occupied a significantly greater number of galleries and travelled greater distances per night at sites with small galleries than did males at sites with large galleries. These results suggest that habitat structure of a forest patch influences intrasexual tree weta behaviour.     

Ground reaction forces and lower-limb joint kinetics of turning gait in typically developing children

Turning is a common locomotor task essential to daily activity; however, very little is known about the forces and moments responsible for the kinematic adaptations occurring relative to straight-line gait in typically developing children. Thus, the aims of this study were to analyse ground reaction forces (GRFs), ground reaction free vertical torque (T_Z), and the lower-limb joint kinetics of 90° outside (step) and inside (spin) limb turns. Step, spin, and straight walking trials from fifty-four typically developing children were analysed. All children were fit with the Plug-in Gait and Oxford Foot Model marker sets while walking over force plates embedded in the walkway. Net internal joint moments and power were computed via a standard inverse dynamics approach. All dependent variables were statistically analysed over the entire curves using the mean difference 95% bootstrap confidence band approach. GRFs were directed medially for step turns and laterally for spin turns during the turning phase. Directions were reversed and magnitudes decreased during the approach phase. Step turns showed reduced ankle power generation, while spin turns showed large T_Z. Both strategies required large knee and hip coronal and transverse plane moments during swing. These kinetic differences highlight adaptations required to maintain stability and reorient the body towards the new walking direction during turning. From a clinical perspective, turning gait may better reveal weaknesses and motor control deficits than straight walking in pathological populations, such as children with cerebral palsy, and could potentially be implemented in standard gait analysis sessions.     

Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements

The sequential stepping of left and right limbs is a fundamental motor behavior that underlies walking movements. This relatively simple locomotor behavior is generated by the rhythmic activity of motor neurons under the control of spinal neural networks known as central pattern generators (CPGs) that comprise multiple interneuron cell types. Little, however, is known about the identity and contribution of defined interneuronal populations to mammalian locomotor behaviors. We show a discrete subset of commissural spinal interneurons, whose fate is controlled by the activity of the homeobox gene Dbx1, has a critical role in controlling the left-right alternation of motor neurons innervating hindlimb muscles. Dbx1 mutant mice lacking these ventral interneurons exhibit an increased incidence of cobursting between left and right flexor/extensor motor neurons during drug-induced locomotion. Together, these findings identify Dbx1-dependent interneurons as key components of the spinal locomotor circuits that control stepping movements in mammals.     

Multiple Paternity in the Nurse Shark, Ginglymostoma Cirratum

For over a decade, we have been studying the reproductive behavior of the nurse shark, Ginglymostoma cirratum, in the Dry Torugas off the Florida Keys, an important mating and nursery ground for this species. In the course of these studies, we have used a variety of tags and tagging protocols to monitor individual animals. Here we report the use of molecular methods for the genetic analysis of nurse sharks. Specifically we have analyzed genetic variation at the MHC II alpha locus using the polymerase chain reaction (PCR) followed by restriction fragment length polymorphism (RFLP) analysis of the amplified products. We found this technique to be a relatively rapid and reliable method for identifying genetic differences between individual sharks. Applying this method to a family of sharks consisting of a mother and 32 pups, we demonstrate that at least four fathers must have fathered this brood. Multiple paternity in the nurse shark suggests a mechanism by which populations of this species may maximize genetic variability. This seems especially valuable for philopatric species whose migratory movement, and thus potential for genetic diversity, is limited.     

Consequences of sexual size dimorphism on energetics and locomotor performance of Grammostola rosea (Araneae; Teraphosidae)

Most male spiders are smaller than females; during sexual maturity, males change their behaviour, abandoning their web or nest to seek out receptive females actively, whereas females stalk prey near their web or nest and tend not to move away from it. Considering this behavioural difference to be associated with increased locomotor activity at maturity, it may be hypothesized that males will have traits that increase locomotor performance. The present study examines the kinetics and energetics of the movements of the mygalomorph spider Grammostola rosea Walckenaer, a large spider with sexual size dimorphism. It is found that males have a higher maximum aerobic speed, average speed, distance travelled and critical angle of climbing than females, indicating better performance. Males also have lower costs of transport than females. These results support the hypothesis that sexual dimorphism in wandering spiders with active males, which are characterized by smaller body size and longer legs than the larger and more static females, is associated with low transport cost, high velocity and better locomotor performance.     

An Application of the Shark Skin Denticle Geometry for Windbreak Fence Design and Fabrication

Windbreak fences in open and urban areas can be used to effectively reduce the wind velocity.In this paper we examine how the geometrical shape of the windbreak fence can optimally mitigate wind velocity.We propose an approach for windbreak fence design based on a bionic parametric model of the shark skin denticle geometry,which improves the reduction of the wind velocity around and behind the windbreak fences.The generative model was used to estimate improvements by variations in the parameters of the fence panel's geometrical shape,inspired by shark skin denticles.The results of the Computational Fluid Dynamics (CFD) analysis indicates that the fence surface inspired by shark skin performs much better than both flat and corrugated surfaces.Taking into account the complex geometry of the surface inspired by shark skin denticles,we propose a fabrication process using an expanded polystyrene foam (EPS) material,created using an industrial robot ann with a hot-wire tool.Creating EPS moulds for the shark skin denticle panels allows for a richer variety material to be used in the final design,leading both to higher efficiency and a more attractive design.     

Mechanisms of Left-Right Coordination in Mammalian Locomotor Pattern Generation Circuits: A Mathematical Modeling View

The locomotor gait in limbed animals is defined by the left-right leg coordination and locomotor speed. Coordination between left and right neural activities in the spinal cord controlling left and right legs is provided by commissural interneurons (CINs). Several CIN types have been genetically identified, including the excitatory V3 and excitatory and inhibitory V0 types. Recent studies demonstrated that genetic elimination of all V0 CINs caused switching from a normal left-right alternating activity to a left-right synchronized “hopping” pattern. Furthermore, ablation of only the inhibitory V0 CINs (V0_D subtype) resulted in a lack of left-right alternation at low locomotor frequencies and retaining this alternation at high frequencies, whereas selective ablation of the excitatory V0 neurons (V0_V subtype) maintained the left–right alternation at low frequencies and switched to a hopping pattern at high frequencies. To analyze these findings, we developed a simplified mathematical model of neural circuits consisting of four pacemaker neurons representing left and right, flexor and extensor rhythm-generating centers interacting via commissural pathways representing V3, V0_D, and V0_V CINs. The locomotor frequency was controlled by a parameter defining the excitation of neurons and commissural pathways mimicking the effects of N-methyl-D-aspartate on locomotor frequency in isolated rodent spinal cord preparations. The model demonstrated a typical left-right alternating pattern under control conditions, switching to a hopping activity at any frequency after removing both V0 connections, a synchronized pattern at low frequencies with alternation at high frequencies after removing only V0_D connections, and an alternating pattern at low frequencies with hopping at high frequencies after removing only V0_V connections. We used bifurcation theory and fast-slow decomposition methods to analyze network behavior in the above regimes and transitions between them. The model reproduced, and suggested explanation for, a series of experimental phenomena and generated predictions available for experimental testing.     

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.     

Locomotion is not a privilege after birth: Ultrasound images of viviparous shark embryos swimming from one uterus to the other

Underwater ultrasound, a new tool for observing the internal body parts of aquatic animals by scuba divers, allowed us long‐term and frequent observations of the embryos of captive aquatic vertebrates. New ultrasound data of captive tawny nurse sharks (Nebrius ferrugineus) revealed that their embryos frequently migrate between the right and left uteri during gestation. This report is the first reliable evidence of active embryonic locomotion in live‐bearing vertebrates and is contradictory to the concept of “sedentary embryo” which has mainly arisen from studies of mammals. The tawny nurse shark is unique among orectolobiform sharks, in which the embryo develops by feeding on sibling eggs in utero. Thus, we hypothesized that swimming aids in an efficient search and capture of these eggs in the uterine environment.     

Locomotor adaptations within the Cercopithecus Genus: a multivariate approach.

Multivariate analysis as a technique for investigating locomotor differentiation among primates has proven its power and usefulness in many studies on various skeletal dimensions. In these analyses primate genera were distributed and sometimes clustered in a manner that was interpretable based on current knowledge of gross locomotor differences. In an effort to advance our understanding of arboreality and terrestriality in primates, the present research involves a careful look for the most subtle morphological differences in locomotor behavior. It is believed that by looking at such subtle shape differences an understanding of what it means morphologically for a primate to be either more or less arboreal may be achieved. The species within the primate genus Cercopithecus were analyzed. This genus includes species which may be placed along a habitat (ground-living to tree-dwelling) or activity spectrum. The different habitats or activity patterns clearly require slight variations in patterns of movement, which in turn may require subtle structural adaptations. Multivariate analyses of 67 postcranial variables on seven species within the genus allowed detection of slight degrees of morphological variation. However, when morphological differences are small, size variance among specimens may take on an inflated importance. A substantial amount of work was devoted to finding the least biased method of removing size variance from the variables while incorporating a discrete size variable into the study. Using these transformed skeletal variables, interspecific groupings were discovered. Much of this infrastructure is then related to differing locomotor behavior and provides an insight into the fine structure of primate locomotor adaptation in an arboreal habitat.     

Modeling of the evolution of bacterial densities in an eutrophic ecosystem (sewage lagoons)

The process of wastewater treatment was studied by modeling the relationships between physical, chemical, and biological (bacteria, phytoplankton, zooplankton) components of the sewage treatment lagoons of an urban wastewater center, based upon a two-year sampling program. The models of interactions between variables were tested by path analysis. The path coefficients were computed from the results of ridge regression, instead of linear multiple regression. The results show that fecal coliforms were effectively controlled by the environmental variables included in the model, which have a cyclic seasonal behavior. This control grew stronger with distance from the input (R ²=0.71) to the output (R ²=0.88) of the treatment plant, resulting in effective elimination of most enteric bacteria. Simultaneously, the ecosystem's community of aerobic heterotrophic bacteria became more independent from the model's predictive variables, with increased distance from the sewage input, thus demonstrating its maturation as an autonomous community in the lagoon ecosystem. Consequences of modeling are discussed, with respect to the understanding of biological wastewater treatment mechanisms and ecosystem dynamics and to plant management.     

Cellular and humoral aspects of innate immunity in the shark

Survival of many species depends, to a great extent, on their innate immunity. Innate immunity in the nurse shark (Ginglymostoma cirratum), a primitive elasmobranch, has been shown to consist of components, both humoral and cellular, which are in some respects similar to those found in mammals and other vertebrates. Innate immune factors present in the shark include complement (a complex system of serum proteins) and antibacterial proteins and enzymes, such as lysozyme. Shark complement, although opsonic and lytic in nature, differs from classical mammalian complement in the number of functionally distinct components involved in the activation sequence. Functional and structural analogues of several mammalian complement proteins have been isolated from the shark, and activation of shark serum by lipopolysaccharide or zymosan produces anaphylatoxin-like ligand(s) inducing mammalian smooth muscle contraction and chemotaxis of human leucocytes in vitro. Lysozyme activity has been recovered from shark leucocyte lysates, which also contain antibacterial peptides, distinct from lysozyme. The composition and antibacterial activity of shark leucocyte granules, the putative source of the activity, is under investigation. Cellular aspects of the inflammatory response which is an integral component of innate immunity, are leucocyte phagocytosis and chemotaxis. Both processes are functions of two distinct shark cell types, the granulocyte and the monocyte-macrophage. It should be noted that the innate resilience of the nurse shark is also augmented by a large pool of serum natural antibodies, which can account for as much as 45% of the total serum protein.     

High-resolution comparative mapping among man,cattle and mouse suggests a role for repeat sequences in mammalian genome evolution

Background

Sharks are members of the taxonomic class Chondrichthyes, the oldest living jawed vertebrates. Genomic studies of this group, in comparison to representative species in other vertebrate taxa, will allow us to theorize about the fundamental genetic, developmental, and functional characteristics in the common ancestor of all jawed vertebrates.

Aims

In order to obtain mapping and sequencing data for comparative genomics, we constructed a bacterial artificial chromosome (BAC) library for the nurse shark, Ginglymostoma cirratum.

Results

The BAC library consists of 313,344 clones with an average insert size of 144 kb, covering ~4.5 × 10¹⁰ bp and thus providing an 11-fold coverage of the haploid genome. BAC end sequence analyses revealed, in addition to LINEs and SINEs commonly found in other animal and plant genomes, two new groups of nurse shark-specific repetitive elements, NSRE1 and NSRE2 that seem to be major components of the nurse shark genome. Screening the library with single-copy or multi-copy gene probes showed 6–28 primary positive clones per probe of which 50–90% were true positives, demonstrating that the BAC library is representative of the different regions of the nurse shark genome. Furthermore, some BAC clones contained multiple genes, making physical mapping feasible.

Conclusion

We have constructed a deep-coverage, high-quality, large insert, and publicly available BAC library for a cartilaginous fish. It will be very useful to the scientific community interested in shark genomic structure, comparative genomics, and functional studies. We found two new groups of repetitive elements specific to the nurse shark genome, which may contribute to the architecture and evolution of the nurse shark genome.     

Spatial and temporal analysis of juvenile blacktip reef shark (Carcharhinus melanopterus) demographies identifies critical habitats

Reef shark species have undergone sharp declines in recent decades, as they inhabit coastal areas, making them an easy target in fisheries (i.e., sharks are exploited globally for their fins, meat, and liver oil) and exposing them to other threats (e.g., being part of by-catch, pollution, and climate change). Reef sharks play a critical role in coral reef ecosystems, where they control populations of smaller predators and herbivorous fishes either directly via predation or indirectly via behavior, thus protecting biodiversity and preventing potential overgrazing of corals. The urgent need to conserve reef shark populations necessitates a multifaceted approach to policy at local, federal, and global levels. However, monitoring programmes to evaluate the efficiency of such policies are lacking due to the difficulty in repeatedly sampling free-ranging, wild shark populations. Over nine consecutive years, we monitored juveniles of the blacktip reef shark (Carcharhinus melanopterus) population around Moorea, French Polynesia, and within the largest shark sanctuary globally, to date. We investigated the roles of spatial (i.e., sampling sites) and temporal variables (i.e., sampling year, season, and month), water temperature, and interspecific competition on shark density across 10 coastal nursery areas. Juvenile C. melanopterus density was found to be stable over 9 years, which may highlight the effectiveness of local and likely federal policies. Two of the 10 nursery areas exhibited higher juvenile shark densities over time, which may have been related to changes in female reproductive behavior or changes in habitat type and resources. Water temperatures did not affect juvenile shark density over time as extreme temperatures proven lethal (i.e., 33°C) in juvenile C. melanopterus might have been tempered by daily variation. The proven efficiency of time-series datasets for reef sharks to identify critical habitats (having the highest juvenile shark densities over time) should be extended to other populations to significantly contribute to the conservation of reef shark species.     

Bristled shark skin: a microgeometry for boundary layer control?

There exists evidence that some fast-swimming shark species may have the ability to bristle their scales during fast swimming. Experimental work using a water tunnel facility has been performed to investigate the flow field over and within a bristled shark skin model submerged within a boundary layer to deduce the possible boundary layer control mechanisms being used by these fast-swimming sharks. Fluorescent dye flow visualization provides evidence of the formation of embedded cavity vortices within the scales. Digital particle image velocimetry (DPIV) data, used to evaluate the cavity vortex formation and boundary layer characteristics close to the surface, indicate increased momentum in the slip layer forming above the scales. This increase in flow velocity close to the shark's skin is indicative of boundary layer control mechanisms leading to separation control and possibly transition delay for the bristled shark skin microgeometry.     

Defining distribution and habitat use of west‐central Florida’s coastal sharks through a research and education program

Identifying critical habitat for highly mobile species such as sharks is difficult, but essential for effective management and conservation. In regions where baseline data are lacking, non‐traditional data sources have the potential to increase observational capacity for species distribution and habitat studies. In this study, a research and education organization conducted a 5‐year (2013–2018) survey of shark populations in the coastal waters of west‐central Florida, an area where a diverse shark assemblage has been observed but no formal population analyses have been conducted. The objectives of this study were to use boosted regression tree (BRT) modeling to quantify environmental factors impacting the distribution of the shark assemblage, create species distribution maps from the model outputs, and identify spatially explicit hot spots of high shark abundance. A total of 1036 sharks were captured, encompassing eleven species. Abundance hot spots for four species and for immature sharks (collectively) were most often located in areas designated as “No Internal Combustion Engine” zones and seagrass bottom cover, suggesting these environments may be fostering more diverse and abundant populations. The BRT models were fitted for immature sharks and five species where n > 100: the nurse shark (Ginglymostoma cirratum), blacktip shark (Carcharhinus limbatus), blacknose shark (C. acronotus), Atlantic sharpnose shark (Rhizoprionodon terraenovae), and bonnethead (Sphyrna tiburo). Capture data were paired with environmental variables: depth (m), sea surface temperature (°C), surface, middle, and bottom salinity (psu), dissolved oxygen (mg/L), and bottom type (seagrass, artificial reef, or sand). Depth, temperature, and bottom type were most frequently identified as predictors with the greatest marginal effect on shark distribution, underscoring the importance of nearshore seagrass and barrier island habitats to the shark assemblage in this region. This approach demonstrates the potential contribution of unconventional science to effective management and conservation of coastal sharks.