Ontogenetic Scaling of the Olfactory Antennae and Flicking Behavior of the Shore Crab, \u3cem\u3eHemigrapsus oregonensis\u3c/em\u3e

Malacostracan crustaceans such as crabs flick antennae with arrays of olfactory sensilla called aesthetascs through the water to sense odors. Flicking by crabs consists of a quick downstroke, in which aesthetascs are deflected laterally (splayed), and a slower, reversed return stroke, in which aesthetascs clump together. This motion causes water to be flushed within and then held in between aesthetascs to deliver odor molecules to olfactory receptors. Although this odor sampling method relies on a narrow range of speeds, sizes, and specific arrangements of aesthetascs, most crabs dramatically change these during ontogeny. In this study, the morphometrics of the aesthetascs, array, and antennae and the flicking kinematics of the Oregon shore crab, Hemigrapsus oregonensis (Decapoda: Brachyura), are examined to determine their scaling relationships during ontogeny. The morphometrics of the array and antennae increase more slowly than would be predicted by isometry. Juvenile crabs’ aesthetascs splay relatively further apart than adults, likely due to changing material properties of aesthetasc cuticle during growth. These results suggest that disproportionate growth and altered aesthetasc splay during flicking will mediate the size changes due to growth that would otherwise lead to a loss of function

The Role of the Pericardium in the Valveless, Tubular Heart of the Tunicate, \u3cem\u3eCiona savignyi\u3c/em\u3e

Tunicates, small invertebrates within the phylum Chordata, possess a robust tubular heart which pumps blood through their open circulatory systems without the use of valves. This heart consists of two major components: the tubular myocardium, a flexible layer of myocardial cells that actively contracts to drive fluid down the length of the tube; and the pericardium, a stiff, outer layer of cells that surrounds the myocardium and creates a fluid-filled space between the myocardium and the pericardium. We investigated the role of the pericardium through in vivo manipulations on tunicate hearts and computational simulations of the myocardium and pericardium using the immersed boundary method. Experimental manipulations reveal that damage to the pericardium results in aneurysm-like bulging of the myocardium and major reductions in the net blood flow and percentage closure of the heart\u27s lumen during contraction. In addition, varying the pericardium-to-myocardium (PM) diameter ratio by increasing damage severity was positively correlated with peak dye flow in the heart. Computational simulations mirror the results of varying the PM ratio experimentally. Reducing the stiffness of the myocardium in the simulations reduced mean blood flow only for simulations without a pericardium. These results indicate that the pericardium has the ability to functionally increase the stiffness of the myocardium and limit myocardial aneurysms. The pericardium\u27s function is likely to enhance flow through the highly resistive circulatory system by acting as a support structure in the absence of connective tissue within the myocardium

Large Amplitude, Short Wave Peristalsis and Its Implications for Transport

Valveless, tubular pumps are widespread in the animal kingdom, but the mechanism by which these pumps generate fluid flow is often in dispute. Where the pumping mechanism of many organs was once described as peristalsis, other mechanisms, such as dynamic suction pumping, have been suggested as possible alternative mechanisms. Peristalsis is often evaluated using criteria established in a technical definition for mechanical pumps, but this definition is based on a small-amplitude, long-wave approximation which biological pumps often violate. In this study, we use a direct numerical simulation of large-amplitude, short-wave peristalsis to investigate the relationships between fluid flow, compression frequency, compression wave speed, and tube occlusion. We also explore how the flows produced differ from the criteria outlined in the technical definition of peristalsis. We find that many of the technical criteria are violated by our model: Fluid flow speeds produced by peristalsis are greater than the speeds of the compression wave; fluid flow is pulsatile; and flow speed have a nonlinear relationship with compression frequency when compression wave speed is held constant. We suggest that the technical definition is inappropriate for evaluating peristalsis as a pumping mechanism for biological pumps because they too frequently violate the assumptions inherent in these criteria. Instead, we recommend that a simpler, more inclusive definition be used for assessing peristalsis as a pumping mechanism based on the presence of non-stationary compression sites that propagate unidirectionally along a tube without the need for a structurally fixed flow direction

What Can Computational Modeling Tell Us About the Diversity of Odor-Capture Structures in the Pancrustacea?

A major transition in the history of the Pancrustacea was the invasion of several lineages of these animals onto land. We investigated the functional performance of odor-capture organs, antennae with olfactory sensilla arrays, through the use of a computational model of advection and diffusion of odorants to olfactory sensilla while varying three parameters thought to be important to odor capture (Reynolds number, gap-width-to-sensillum-diameter ratio, and angle of the sensilla array with respect to oncoming flow). We also performed a sensitivity analysis on these parameters using uncertainty quantification to analyze their relative contributions to odor-capture performance. The results of this analysis indicate that odor capture in water and in air are fundamentally different. Odor capture in water and leakiness of the array are highly sensitive to Reynolds number and moderately sensitive to angle, whereas odor capture in air is highly sensitive to gap widths between sensilla and moderately sensitive to angle. Leakiness is not a good predictor of odor capture in air, likely due to the relative importance of diffusion to odor transport in air compared to water. We also used the sensitivity analysis to make predictions about morphological and kinematic diversity in extant groups of aquatic and terrestrial crustaceans. Aquatic crustaceans will likely exhibit denser arrays and induce flow within the arrays, whereas terrestrial crustaceans will rely on more sparse arrays with wider gaps and little-to-no animal-induced currents

A Tale of Two Antennules: The Performance of Crab Odor-Capture Organs in Air and Water

Odour capture is an important part of olfaction, where dissolved chemical cues (odours) are brought into contact with chemosensory structures. Antennule flicking by marine crabs is an example of discrete odour capture (sniffing) where an array of chemosensory hairs is waved through the water to create a flow–no flow pattern based on a narrow range of speeds, diameters of and spacings between hairs. Changing the speed of movement and spacing of hairs at this scale to manipulate flow represents a complicated fluid dynamics problem. In this study, we use numerical simulation of the advection and diffusion of a chemical gradient to reveal how morphological differences of the hair arrays affect odour capture. Specifically, we simulate odour capture by a marine crab (Callinectes sapidus) and a terrestrial crab (Coenobita rugosus) in both air and water to compare performance. We find that the antennule morphologies of each species are adaptions to capturing odours in their native habitats. Sniffing is an important part of odour capture for marine crabs in water where the diffusivity of odorant molecules is low and flow through the array is necessary. On the other hand, flow within the hair array diminishes odour-capture performance in air where diffusivities are high. This study highlights some of the adaptations necessary to transition from water to air

Modeling Action Potential Reversals in Tunicate Hearts

Tunicates are small invertebrates which possess a unique ability to reverse flow in their hearts. Scientists have debated various theories regarding how and why flow reversals occur. Here we explore the electrophysiological basis for reversals by simulating action potential propagation in an idealized model of the tubelike tunicate heart. Using asymptotic formulas for action potential duration and conduction velocity, we propose tunicate-specific parameters for a two-current ionic model of the action potential. Then, using a kinematic model, we derive analytical criteria for reversals to occur. These criteria inform subsequent numerical simulations of action potential propagation in a fiber paced at both ends. In particular, we explore the role that variability of pacemaker firing rates plays in generating reversals, and we identify various favorable conditions for triggering retrograde propagation. Our analytical framework extends to other species; for instance, it can be used to model competition between the sinoatrial node and abnormal ectopic foci in human heart tissue

Scaling of Olfactory Antennae of the Terrestrial Hermit Crabs \u3cem\u3eCoenobita rugosus\u3c/em\u3e and \u3cem\u3eCoenobita perlatus\u3c/em\u3e During Ontogeny

Although many lineages of terrestrial crustaceans have poor olfactory capabilities, crabs in the family Coenobitidae, including the terrestrial hermit crabs in the genus Coenobita, are able to locate food and water using olfactory antennae (antennules) to capture odors from the surrounding air. Terrestrial hermit crabs begin their lives as small marine larvae and must find a suitable place to undergo metamorphosis into a juvenile form, which initiates their transition to land. Juveniles increase in size by more than an order of magnitude to reach adult size. Since odor capture is a process heavily dependent on the size and speed of the antennules and physical properties of the fluid, both the transition from water to air and the large increase in size during ontogeny could impact odor capture. In this study, we examine two species of terrestrial hermit crabs, Coenobita perlatus H. Milne-Edwards and Coenobita rugosus H. Milne-Edwards, to determine how the antennule morphometrics and kinematics of flicking change in comparison to body size during ontogeny, and how this scaling relationship could impact odor capture by using a simple model of mass transport in flow. Many features of the antennules, including the chemosensory sensilla, scaled allometrically with carapace width and increased slower than expected by isometry, resulting in relatively larger antennules on juvenile animals. Flicking speed scaled as expected with isometry. Our mass-transport model showed that allometric scaling of antennule morphometrics and kinematics leads to thinner boundary layers of attached fluid around the antennule during flicking and higher odorant capture rates as compared to antennules which scaled isometrically. There were no significant differences in morphometric or kinematic measurements between the two species

Flexibility of Crab Chemosensory Hairs Enables Flicking Antennules to Sniff

The first step in smelling is capture of odorant molecules from the surrounding fluid. We used lateral flagella of olfactory antennules of crabs Callinectes sapidus to study the physical process of odor capture by antennae bearing dense tufts of hair-like chemosensory sensilla (aesthetascs). Fluid flow around and through aesthetasc arrays on dynamically scaled models of lateral flagella of C. sapidus was measured by particle image velocimetry to determine how antennules sample the surrounding water when they flick. Models enabled separate evaluation of the effects of flicking speed, aesthetasc spacing, and antennule orientation. We found that crab antennules, like those of other malacostracan crustaceans, take a discrete water sample during each flick by having a rapid downstroke, during which water flows into the aesthetasc array, and a slow recovery stroke, when water is trapped in the array and odorants have time to diffuse to aesthetascs. However, unlike antennules of crustaceans with sparse aesthetasc arrays, crabs enhance sniffing via additional mechanisms: 1) Aesthetascs are flexible and splay as a result of the hydrodynamic drag during downstrokes, then clump together during return strokes; and 2) antennules flick with aesthetascs on the upstream side of the stalk during downstrokes, but are hidden downstream during return strokes. Aiming aesthetascs into ambient flow maintains sniffing. When gaps between aesthetascs are wide, changes in antennule speed are more effective at altering flow through the array than when gaps are narrow. Nonetheless, if crabs had fixed gap widths, their ability to take discrete samples of their odorant environment would be diminished

Functional Morphology of Gliding Flight I. Modeling Reveals Distinct Performance Landscapes Based on Soaring Strategies

The physics of flight influences the morphology of bird wings through natural selection on flight performance. The connection between wing morphology and performance is unclear due to the complex relationships between various parameters of flight. In order to better understand this connection, we present a holistic analysis of gliding flight that preserves complex relationships between parameters. We use a computational model of gliding flight, along with analysis by uncertainty quantification, to 1) create performance landscapes of gliding based on output metrics (maximum lift-to-drag ratio, minimum gliding angle, minimum sinking speed, lift coefficient at minimum sinking speed); and 2) predict what parameters of flight (chordwise camber, wing aspect ratio, Reynolds number) would differ between gliding and non-gliding species of birds. We also examine performance based on soaring strategy for possible differences in morphology within gliding birds. Gliding birds likely have greater aspect ratios than non-gliding birds, due the high sensitivity of aspect ratio on most metrics of gliding performance. Furthermore, gliding birds can use two distinct soaring strategies based on performance landscapes. First, maximizing distance traveled (maximizing lift-to-drag ratio and minimizing gliding angle) should result in wings with high aspect ratios and middling-to-low wing chordwise camber. Second, maximizing lift extracted from updrafts should result in wings with middling aspect ratios and high wing chordwise camber. Following studies can test these hypotheses using morphological measurements

Functional Morphology of Gliding Flight II. Morphology Follows Predictions of Gliding Performance

The evolution of wing morphology among birds, and its functional consequences, remains an open question, despite much attention. This is in part because the connection between form and function is difficult to test directly. To address this deficit, in prior work we used computational modeling and sensitivity analysis to interrogate the impact of altering wing aspect ratio, camber, and Reynolds number on aerodynamic performance, revealing the performance landscapes that avian evolution has explored. In the present work, we used a dataset of three-dimensionally scanned bird wings coupled with the performance landscapes to test two hypotheses regarding the evolutionary diversification of wing morphology associated with gliding flight behavior: 1) gliding birds would exhibit higher wing aspect ratio and greater chordwise camber than their non-gliding counterparts; and 2) that two strategies for gliding flight exist, with divergent morphological conformations. In support of our first hypothesis, we found evidence of morphological divergence in both wing aspect ratio and camber between gliders and non-gliders, suggesting that wing morphology of birds that utilize gliding flight is under different selective pressures than the wings of non-gliding taxa. Furthermore, we found that these morphological differences also yielded differences in coefficient of lift measured both at the maximum lift to drag ratio and at minimum sinking speed, with gliding taxa exhibiting higher coefficient of lift in both cases. Minimum sinking speed was also lower in gliders than non-gliders. However, contrary to our hypothesis, we found that the maximum ratio of the coefficient of lift to the coefficient of drag differed between gliders and non-gliders. This may point to the need for gliders to maintain high lift capability for takeoff and landing independent of gliding performance, or could be due to the divergence in flight styles among gliders, as not all gliders are predicted to optimize either quantity. However, direct evidence for the existence of two morphologically defined gliding flight strategies was equivocal, with only slightly stronger support for an evolutionary model positing separate morphological optima for these strategies than an alternative model positing a single peak. The absence of a clear result may be an artifact of low statistical power owing to a relatively small sample size of gliding flyers expected to follow the “aerial search” strategy