Maria Laura Habegger

Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico

The feeding anatomy, behavior and diet of the whale shark Rhincodon typus were studied off Cabo Catoche, Yucatan Peninsula, Mexico. The filtering apparatus is composed of 20 unique filtering pads that completely occlude the pharyngeal cavity. A reticulated mesh lies on the proximal surface of the pads, with openings averaging 1.2mm in diameter. Superficial to this, a series of primary and secondary cartilaginous vanes support the pads and direct the water across the primary gill filaments. During surface ram filter feeding, sharks swam at an average velocity of 1.1m/s with 85% of the open mouth below the waters surface. Sharks on average spent approximately 7.5h/day feeding at the surface on dense plankton dominated by sergestids, calanoid copepods, chaetognaths and fish larvae. Based on calculated flow speed and underwater mouth area, it was estimated that a whale shark of 443 cm total length (TL) filters 326 m(3)/h, and a 622 cm TL shark 614 m(3)/h. With an average plankton biomass of 4.5 g/m(3) at the feeding site, the two sizes of sharks on average would ingest 1467 and 2763 g of plankton per hour, and their daily ration would be approximately 14,931 and 28,121 kJ, respectively. These values are consistent with independently derived feeding rations of captive, growing whale sharks in an aquarium. A feeding mechanism utilizing cross-flow filtration of plankton is described, allowing the sharks to ingest plankton that is smaller than the mesh while reducing clogging of the filtering apparatus.

Scale morphology and flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus

We quantified placoid scale morphology and flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus. The shortfin mako shark has shorter scales than the blacktip shark. The majority of the shortfin mako shark scales have three longitudinal riblets with narrow spacing and shallow grooves. In comparison, the blacktip shark scales have five to seven longitudinal riblets with wider spacing and deeper grooves. Manual manipulation of the scales at 16 regions on the body and fins revealed a range of scale flexibility, from regions of nonerectable scales such as on the leading edge of the fins to highly erectable scales along the flank of the shortfin mako shark body. The flank scales of the shortfin mako shark can be erected to a greater angle than the flank scales of the blacktip shark. The shortfin mako shark has a region of highly flexible scales on the lateral flank that can be erected to at least 50°. The scales of the two species are anchored in the stratum laxum of the dermis. The attachment fibers of the scales in both species appear to be almost exclusively collagen, with elastin fibers visible in the stratum laxum of both species. The most erectable scales of the shortfin mako shark have long crowns and relatively short bases that are wider than long. The combination of a long crown length to short base length facilitates pivoting of the scales. Erection of flank scales and resulting drag reduction is hypothesized to be passively driven by localized flow patterns over the skin. J. Morphol. 2012.

Remodeling in bone without osteocytes: Billfish challenge bone structure–function paradigms

Significance A fundamental paradigm of bone biology is that the remodeling process—by which bones detect and repair damage—is orchestrated by osteocytes. The bones of most extant fish, however, lack these cells and should be unable to repair damage in their bones. We provide evidence for intense remodeling in the anosteocytic bone of billfishes, such as swordfish and marlin. Our observations challenge the central axiom that osteocytes alone are responsible for remodeling, suggesting alternate mechanisms in bone physiology and/or variation in the roles of bone cells. In addition, billfish bone exhibits an array of striking material properties that distinguish it from mammalian bone despite having similar composition, underlining that skeletal biology concepts are limiting when based on mammalian tissues alone. A remarkable property of tetrapod bone is its ability to detect and remodel areas where damage has accumulated through prolonged use. This process, believed vital to the long-term health of bone, is considered to be initiated and orchestrated by osteocytes, cells within the bone matrix. It is therefore surprising that most extant fishes (neoteleosts) lack osteocytes, suggesting their bones are not constantly repaired, although many species exhibit long lives and high activity levels, factors that should induce considerable fatigue damage with time. Here, we show evidence for active and intense remodeling occurring in the anosteocytic, elongated rostral bones of billfishes (e.g., swordfish, marlins). Despite lacking osteocytes, this tissue exhibits a striking resemblance to the mature bone of large mammals, bearing structural features (overlapping secondary osteons) indicating intensive tissue repair, particularly in areas where high loads are expected. Billfish osteons are an order of magnitude smaller in diameter than mammalian osteons, however, implying that the nature of damage in this bone may be different. Whereas billfish bone material is as stiff as mammalian bone (unlike the bone of other fishes), it is able to withstand much greater strains (relative deformations) before failing. Our data show that fish bone can exhibit far more complex structure and physiology than previously known, and is apparently capable of localized repair even without the osteocytes believed essential for this process. These findings challenge the unique and primary role of osteocytes in bone remodeling, a basic tenet of bone biology, raising the possibility of an alternative mechanism driving this process.

Movable shark scales act as a passive dynamic micro-roughness to control flow separation

Shark scales on fast-swimming sharks have been shown to be movable to angles in excess of 50°, and we hypothesize that this characteristic gives this shark skin a preferred flow direction. During the onset of separation, flow reversal is initiated close to the surface. However, the movable scales would be actuated by the reversed flow thereby causing a greater resistance to any further flow reversal and this mechanism would disrupt the process leading to eventual flow separation. Here we report for the first time experimental evidence of the separation control capability of real shark skin through water tunnel testing. Using skin samples from a shortfin mako Isurus oxyrinchus, we tested a pectoral fin and flank skin attached to a NACA 4412 hydrofoil and separation control was observed in the presence of movable shark scales under certain conditions in both cases. We hypothesize that the scales provide a passive, flow-actuated mechanism acting as a dynamic micro-roughness to control flow separation.

Feeding in billfishes: inferring the role of the rostrum from a biomechanical standpoint

ABSTRACT Perhaps the most striking feature of billfishes is the extreme elongation of the premaxillary bones forming their rostra. Surprisingly, the exact role of this structure in feeding is still controversial. The goal of this study is to investigate the use of the rostrum from a functional, biomechanical and morphological standpoint to ultimately infer its possible role during feeding. Using beam theory, experimental and theoretical loading tests were performed on the rostra from two morphologically different billfish, the blue marlin (Makaira nigricans) and the swordfish (Xiphias gladius). Two loading regimes were applied (dorsoventral and lateral) to simulate possible striking behaviors. Histological samples and material properties of the rostra were obtained along their lengths to further characterize structure and mechanical performance. Intraspecific results show similar stress distributions for most regions of the rostra, suggesting that this structure may be designed to withstand continuous loadings with no particular region of stress concentration. Although material stiffness increased distally, flexural stiffness increased proximally owing to higher second moment of area. The blue marlin rostrum was stiffer and resisted considerably higher loads for both loading planes compared with that of the swordfish. However, when a continuous load along the rostrum was considered, simulating the rostrum swinging through the water, swordfish exhibited lower stress and drag during lateral loading. Our combined results suggest that the swordfish rostrum is suited for lateral swiping to incapacitate their prey, whereas the blue marlin rostrum is better suited to strike prey from a wider variety of directions. Summary: Biomechanical differences derived from rostrum morphology and composition lead to species-specific feeding behavior in billfishes.

Shark Skin Boundary Layer Control

An investigation into the separation control mechanisms found on the skin of fast-swimming sharks, with a particular focus on the shortfin mako (Isurus oxyrinchus) which is considered to be one of the fastest pelagic shark species, was carried out. Previous researchers have reported a bristling capability of the scales, or denticles, in certain species of sharks. This study identified that bristling angle is highly dependent on body location, with some scales easily erectable to angles in excess of 50∘. The flexibility of the scale appears to be due to a reduction in the size of the base of the scale where anchored into the skin. It is hypothesized that the scales act as a passive, flow-actuated mechanism as a means of controlling flow separation.

Experimental study of laminar and turbulent boundary layer separation control of shark skin

The Shortfin Mako shark (Isurus oxyrinchus) is a fast swimmer and has incredible turning agility, and has flexible scales known to bristle up to 50° in the flank regions. It is purported that this bristling capability of the scales may result in a unique pass flow control method to control flow separation and reduce drag. It appears that the scales have evolved to be only actuated when the flow over the body is reversed; thereby inducing a method of inhibiting flow reversal close to the surface. In addition, bristled scales form cavities which could induce boundary layer mixing and further assist in delaying flow separation. To substantiate the hypothesis, samples of skin from the flank region of the mako have been tested in a water tunnel facility under various strengths of adverse pressure gradient (APG). Laminar and turbulent separation over the skin was studied experimentally using time-resolved digital particle image velocimetry, where the APG was generated and varied using a rotating cylinder. Shark skin results were compared with that of a smooth plate data for a given amount of APG. Both the instantaneous and time-averaged results reveal that shark skin is capable of controlling laminar as well as turbulent separation. Under laminar conditions, the shark skin also induces an early transition to turbulence and reduces the degree of laminar separation. For turbulent separation, the presence of the shark skin reduces the amount of backflow and size of the separation region. Under both flow conditions, the shark skin also delayed the point of separation as compared to a smooth wall.

Passive bristling of mako shark scales in reversing flows

Shark skin has been shown to reduce drag in turbulent boundary layer flows, but the flow control mechanisms by which it does so are not well understood. Drag reduction has generally been attributed to static effects of scale surface morphology, but possible drag reduction effects of passive or active scale actuation, or ‘bristling’, have been recognized more recently. Here, we provide the first direct documentation of passive scale bristling due to reversing, turbulent boundary layer flows. We recorded and analysed high-speed videos of flow over the skin of a shortfin mako shark, Isurus oxyrinchus. These videos revealed rapid scale bristling events with mean durations of approximately 2 ms. Passive bristling occurred under flow conditions representative of cruise swimming speeds and was associated with two flow features. The first was a downward backflow that pushed a scale-up from below. The second was a vortex just upstream of the scale that created a negative pressure region, which pulled up a scale without requiring backflow. Both flow conditions initiated bristling at lower velocities than those required for a straight backflow. These results provide further support for the role of shark scale bristling in drag reduction.

Beneficial aerodynamic effect of wing scales on the climbing flight of butterflies

It is hypothesized that butterfly wing scale geometry and surface patterning may function to improve aerodynamic efficiency. In order to investigate this hypothesis, a method to measure butterfly flapping kinematics optically over long uninhibited flapping sequences was developed. Statistical results for the climbing flight flapping kinematics of 11 butterflies, based on a total of 236 individual flights, both with and without their wing scales, are presented. Results show, that for each of the 11 butterflies, the mean climbing efficiency decreased after scales were removed. Data was reduced to a single set of differences of climbing efficiency using are paired t-test. Results show a mean decrease in climbing efficiency of 32.2% occurred with a 95% confidence interval of 45.6%-18.8%. Similar analysis showed that the flapping amplitude decreased by 7% while the flapping frequency did not show a significant difference. Results provide strong evidence that butterfly wing scale geometry and surface patterning improve butterfly climbing efficiency. The authors hypothesize that the wing scales effect in measured climbing efficiency may be due to an improved aerodynamic efficiency of the butterfly and could similarly be used on flapping wing micro air vehicles to potentially achieve similar gains in efficiency.