Current Research and Scholarly Interests
Biomechanics, ecology, and ecological physiology
Biomechanics, ecology, and ecological physiology
Lignified cell walls are widely considered to be key innovations in the evolution of terrestrial plants from aquatic ancestors some 475 million years ago. Lignins, complex aromatic heteropolymers, stiffen and fortify secondary cell walls within xylem tissues, creating a dense matrix that binds cellulose microfibrils and crosslinks other wall components, thereby preventing the collapse of conductive vessels, lending biomechanical support to stems, and allowing plants to adopt an erect-growth habit in air. Although "lignin-like" compounds have been identified in primitive green algae, the presence of true lignins in nonvascular organisms, such as aquatic algae, has not been confirmed. Here, we report the discovery of secondary walls and lignin within cells of the intertidal red alga Calliarthron cheilosporioides. Until now, such developmentally specialized cell walls have been described only in vascular plants. The finding of secondary walls and lignin in red algae raises many questions about the convergent or deeply conserved evolutionary history of these traits, given that red algae and vascular plants probably diverged more than 1 billion years ago.
View details for DOI 10.1016/j.cub.2008.12.031
View details for Web of Science ID 000263012600030
View details for PubMedID 19167225
Are there absolute limits to the speed at which animals can run? If so, how close are present-day individuals to these limits? I approach these questions by using three statistical models and data from competitive races to estimate maximum running speeds for greyhounds, thoroughbred horses and elite human athletes. In each case, an absolute speed limit is definable, and the current record approaches that predicted maximum. While all such extrapolations must be used cautiously, these data suggest that there are limits to the ability of either natural or artificial selection to produce ever faster dogs, horses and humans. Quantification of the limits to running speed may aid in formulating and testing models of locomotion.
View details for DOI 10.1242/jeb.024968
View details for Web of Science ID 000261260500013
View details for PubMedID 19043056
Previous studies have demonstrated that fleshy seaweeds resist wave-induced drag forces in part by being flexible. Flexibility allows fronds to 'go with the flow', reconfiguring into streamlined shapes and reducing frond area projected into flow. This paradigm extends even to articulated coralline algae, which produce calcified fronds that are flexible only because they have distinct joints (genicula). The evolution of flexibility through genicula was a major event that allowed articulated coralline algae to grow elaborate erect fronds in wave-exposed habitats. Here we describe the mechanics of genicula in the articulated coralline Calliarthron and demonstrate how segmentation affects bending performance and amplifies bending stresses within genicula. A numerical model successfully predicted deflections of articulated fronds by assuming genicula to be assemblages of cables connecting adjacent calcified segments (intergenicula). By varying the dimensions of genicula in the model, we predicted the optimal genicular morphology that maximizes flexibility while minimizing stress amplification. Morphological dimensions of genicula most prone to bending stresses (i.e. genicula near the base of fronds) match model predictions.
View details for DOI 10.1242/jeb.020479
View details for Web of Science ID 000260165100017
View details for PubMedID 18931315
Previous studies have hypothesized that wave-induced drag forces may constrain the size of intertidal organisms by dislodging or breaking organisms that exceed some critical dimension. In this study, we explored constraints on the size of the articulated coralline alga Calliarthron, which thrives in wave-exposed intertidal habitats. Its ability to survive depends critically upon its segmented morphology (calcified segments separated by flexible joints or ;genicula'), which allows otherwise rigid fronds to bend and thereby reduce drag. However, bending also amplifies stress within genicula near the base of fronds. We quantified breakage of genicula in bending by applying known forces to fronds until they broke. Using a mathematical model, we demonstrate the mitigating effect of neighboring fronds on breakage and show that fronds growing within dense populations are no more likely to break in bending than in tension, suggesting that genicular morphology approaches an engineering optimum, possibly reflecting adaptation to hydrodynamic stress. We measured drag in a re-circulating water flume (0.23-3.6 m s(-1)) and a gravity-accelerated water flume, which generates jets of water that mimic the impact of breaking waves (6-10 m s(-1)). We used frond Reynolds number to extrapolate drag coefficients in the field and to predict water velocities necessary to break fronds of given sizes. Laboratory data successfully predicted frond sizes found in the field, suggesting that, although Calliarthron is well adapted to resist breakage, wave forces may ultimately limit the size of intertidal fronds.
View details for DOI 10.1242/jeb.020495
View details for Web of Science ID 000260165100018
View details for PubMedID 18931316
Biomechanical analyses of intertidal and shallow subtidal seaweeds have elucidated ways in which these organisms avoid breakage in the presence of exceptional hydrodynamic forces imposed by pounding surf. However, comparison of algal material properties to maximum hydrodynamic forces predicts lower rates of breakage and dislodgment than are actually observed. Why the disparity between prediction and reality? Most previous research has measured algal material properties during a single application of force, equivalent to a single wave rushing past an alga. In contrast, intertidal macroalgae may experience more than 8000 waves a day. This repeated loading can cause cracks - introduced, for example, by herbivory or abrasion - to grow and eventually cause breakage, yet fatigue crack growth has not previously been taken into account. Here, we present methods from the engineering field of fracture mechanics that can be used to assess consequences of repeated force imposition for seaweeds. These techniques allow quantification of crack growth in wave-swept macroalgae, a first step towards considering macroalgal breakage in the realistic context of repeated force imposition. These analyses can also be applied to many other soft materials.
View details for DOI 10.1242/jeb.001560
View details for Web of Science ID 000248304900009
View details for PubMedID 17575028
Wave-swept macroalgae are subjected to large hydrodynamic forces as each wave breaks on shore, loads that are repeated thousands of times per day. Previous studies have shown that macroalgae can easily withstand isolated impositions of maximal field forces. Nonetheless, macroalgae break frequently. Here we investigate the possibility that repeated loading by sub-lethal forces can eventually cause fracture by fatigue. We determine fracture toughness, in the form of critical strain energy release rate, for several flat-bladed macroalgae, thereby assessing their resistance to complete fracture in the presence of cracks. Critical energy release rates are evaluated through single-edge-notch, pull-to-break tests and single-edge-notch, repeated-loading tests. Crack growth at sub-critical energy release rates is measured in repeated-loading tests, providing a first assessment of algal breakage under conditions of repeated loading. We then estimate the number of imposed waves required for un-notched algal blades to reach the point of complete fracture. We find that, if not checked by repair, fatigue crack growth from repeated sub-lethal stresses may completely fracture individuals within days. Our results suggest that fatigue may play an important role in macroalgal breakage.
View details for DOI 10.1242/jeb.001578
View details for Web of Science ID 000248304900010
View details for PubMedID 17575029
Unlike most bivalves, scallops are able to swim, relying on a shell with reduced mass and streamlined proportions, a large fast-twitch adductor muscle and the elastic characteristics of the shell's hinge. Despite these adaptations, swimming in scallops is never far from failure, and it is surprising to find a swimming scallop in Antarctica, where low temperature increases the viscosity of seawater, decreases the power output of the adductor muscle and potentially compromises the energy storage capability of the hinge material (abductin, a protein rubber). How does the Antarctic scallop, Adamussium colbecki, cope with the cold? Its shell mass is substantially reduced relative to that of temperate and tropical scallops, but this potential advantage is more than offset by a drastic reduction in adductor-muscle mass. By contrast, A. colbecki's abductin maintains a higher resilience at low temperatures than does the abductin of a temperate scallop. This resilience may help to compensate for reduced muscle mass, assisting the Antarctic scallop to maintain its marginal swimming ability. However, theory suggests that this assistance should be slight, so the adaptive value of increased resilience remains open to question. The high resilience of A. colbecki abductin at low temperatures may be of interest to materials engineers.
View details for DOI 10.1242/jeb.02538
View details for Web of Science ID 000242132800015
View details for PubMedID 17079720
Living at the interface between the marine and terrestrial environments, intertidal organisms may serve as a bellwether for environmental change and a test of our ability to predict its biological consequences. However, current models do not allow us to predict the body temperature of intertidal organisms whose heat budgets are strongly affected by conduction to and from the substratum. Here, we propose a simple heat-budget model of one such animal, the limpet Lottia gigantea, and test the model against measurements made in the field. Working solely from easily measured physical and meteorological inputs, the model predicts the daily maximal body temperatures of live limpets within a fraction of a degree, suggesting that it may be a useful tool for exploring the thermal biology of limpets and for predicting effects of climate change. The model can easily be adapted to predict the temperatures of chitons, acorn barnacles, keyhole limpets, and encrusting animals and plants.
View details for DOI 10.1242/jeb.02257
View details for Web of Science ID 000238421800011
View details for PubMedID 16788024
When coupled with long-term meteorological records, a heat-budget model for the limpet, Lottia gigantea, provides a wealth of information regarding environmental and topographic controls of body temperature in this ecologically important species. (1) The maximum body temperature predicted for any site (37.5 degrees C) is insufficient to kill all limpets, suggesting that acute thermal stress does not set an absolute upper limit to the elevation of L. gigantea on the shore. Therefore, the upper limit must be set by behavioral responses, sublethal effects or ecological interactions. (2) Temperatures sufficient to kill limpets are reached at only a small fraction of substratum orientations and elevations and on only three occasions in 5 years. These rare predicted lethal temperatures could easily be missed in field measurements, thereby influencing the interpretation of thermal stress. (3) Body temperature is typically higher than air temperature, but maximum air temperature can nonetheless be used as an accurate predictor of maximum body temperature. Warmer air temperatures in the future may thus cause increased mortality in this intertidal species. Interpretation of the ecological effects of elevated body temperature depends strongly on laboratory measurements of thermal stress, highlighting the need for additional research on the temporal and spatial variability of thermal limits and sublethal stress. The lengthy time series of body temperatures calculated from the heat-budget model provides insight into how these physiological measurements should be conducted.
View details for DOI 10.1242/jeb.02258
View details for Web of Science ID 000238421800012
View details for PubMedID 16788025
Intertidal algae are exposed to the potentially severe drag forces generated by crashing waves, and several species of brown algae respond, in part, by varying the strength of their stipe material. In contrast, previous measurements have suggested that the material strength of red algae is constant across wave exposures. Here, we reexamine the responses to drag of the intertidal red alga Mastocarpus papillatus Kutzing. By measuring individuals at multiple sites along a known force gradient, we discern responses overlooked by previous methods, which compared groups of individuals between "exposed" and "protected" sites. This improved resolution reveals that material strength and stipe cross-sectional area are both positively correlated with drag, suggesting that individual blades or populations can adjust either or both of these parameters in response to their mechanical environment. The combined effect of this variation is a stipe breaking force that is positively correlated with locally imposed drag. Owing to this response to drag, the estimated wave-imposed limit to thallus size in M. papillatus is larger than previously predicted and larger than sizes observed in the field, indicating that factors other than wave force alone constrain the size of this alga on wave-swept shores.
View details for Web of Science ID 000228618100005
View details for PubMedID 15837960
Phenotypic plasticity, the capacity of a given genotype to produce differing morphologies in response to the environment, is widespread among marine organisms (1). For example, acorn barnacles feed by extending specialized appendages (the cirral legs) into flow, and the length of the cirri is plastic: the higher the velocity, the shorter the feeding legs (2,3). However, this effect has been explored only for flows less than 4.6 m/s, slow compared to typical flows measured at sites on wave-exposed shores. What happens at faster speeds? Leg lengths of Balanus glandula Darwin, 1854, an acorn barnacle, were measured at 15 sites in Monterey, California, across flows ranging from 0.5 to 14.0 m/s. Similar to previous findings, a plastic response in leg length was noted for the four sites with water velocities less than 3 m/s. However, no plastic response was present at the 11 sites exposed to faster velocities, despite a 4-fold variation in speed. We conclude that the velocity at which the plastic response occurs has an upper limit of 2-4 m/s, a velocity commonly exceeded within the typical habitat of this species.
View details for Web of Science ID 000222318600001
View details for PubMedID 15198937
The mechanism by which surface tension allows water striders (members of the genus Gerris) to stand on the surface of a pond or stream is a classic example for introductory classes in animal mechanics. Until recently, however, the question of how these insects propelled themselves remained open. One plausible mechanism-creating momentum in the water via the production of capillary waves-led to a paradox: juvenile water striders move their limbs too slowly to produce waves, but nonetheless travel across the water's surface. Two recent papers demonstrate that both water striders and water-walking spiders circumvent this paradox by foregoing any reliance on waves to gain purchase on the water. Instead they use their legs as oars, and the capillary 'dimple' formed by each leg acts as the oar's blade. The resulting hydrodynamic drag produces vortices in the water, and the motion of these vortices imparts the necessary fluid momentum. These studies pave the way for a more thorough understanding of the complex mechanics of walking on water, and an exploration of how this intriguing form of locomotion scales with the size of the organism.
View details for DOI 10.1242/jeb.00908
View details for Web of Science ID 000221571100006
View details for PubMedID 15073192
Biomechanical models come in a variety of forms: conceptual models; physical models; and mathematical models (both of the sort written down on paper and the sort carried out on computers). There are model structures (such as insect flight muscle and the tendons of rats' tails), model organisms (such as the flying insect, Manduca sexta), even model systems of organisms (such as the communities that live on wave-swept rocky shores). These different types of models are typically employed separately, but their value often can be enhanced if their insights are integrated. In this brief report we explore a particular example of such integration among models, as applied to flexible marine algae. A conceptual model serves as a template for the construction of a mathematical model of a model species of giant kelp, and the validity of this numerical model is tested using physical models. The validated mathematical model is then used in conjunction with a computer-controlled tensile testing apparatus to simulate the loading regime placed on algal materials. The resulting information can be used to create a more precise mathematical model.
View details for DOI 10.1098/rstb.2003.1341
View details for Web of Science ID 000185739500013
View details for PubMedID 14561344
Marine algae rely on currents and waves to replenish the nutrients required for photosynthesis. The interaction of algal blades with flow often involves dynamic reorientations of the blade surface (pitching and flapping) that may in turn affect nutrient flux. As a first step toward understanding the consequences of blade motion, we explore the effect of oscillatory pitching on the flux to a flat plate and to two morphologies of the kelp Eisenia arborea. In slow flow (equivalent to a water velocity of 2.7 cm s(-1)), pitching increases the time-averaged flux to both kelp morphologies, but not to the plate. In fast flow (equivalent to 20 cm s(-1) in water), pitching has negligible effect on flux regardless of shape. For many aspects of flux, the flat plate is a reliable model for the flow-protected algal blade, but predictions made from the plate would substantially underestimate the flux to the flow-exposed blade. These measurements highlight the complexities of flow-related nutrient transport and the need to understand better the dynamic interactions among nutrient flux, blade motion, blade morphology, and water flow.
View details for Web of Science ID 000177717100001
View details for PubMedID 12200251
Wave-swept marine algae must contend with the hydrodynamic forces imposed by extreme water velocities. Nonetheless, they seldom have a shape that appears streamlined and they are constructed of weak, compliant materials. How do they survive? The answer is complex, but a coherent story is beginning to emerge. The combined effect of frond shape and material properties ensures that algae are flexible. In small individuals, flexibility allows the plant to reorient and reconfigure in flow, thereby assuming a streamlined shape and reducing the applied hydrodynamic force. In large individuals, flexibility allows fronds to 'go with the flow', a strategy that can at times allow the plant to avoid hydrodynamic forces but may at other times impose inertial loads. Our understanding of algal mechanics is such that we can begin to predict the survivorship of algae as a function of size, spatial distribution and wave climate.
View details for Web of Science ID 000176013300001
View details for PubMedID 11976348
On wave-swept rocky shores, limpets are subjected to water velocities in excess of 20 m s(-1), which may impose large hydrodynamic forces. Despite the extreme severity of this flow environment, predictions from conical models suggest that limpets' shells are typically far from the optimal shape that would minimize the risk of dislodgment, a deviation that is allowed by the high tenacity of the limpets' adhesive system. In this study, we test this conclusion using an actual limpet. The shell of Lottia gigantea differs substantially from the hydrodynamic optimum in that its apex is displaced anteriorly to form a plough, which is used to defend the limpet's territory. The hydrodynamic effects of this shape are similar to those observed in conical models: the animal experiences an increased lift when facing into the flow and a decreased lift when the flow is at its back. However, neither effect has a substantial impact on the risk of dislodgment. When the animal is stationary, its adhesion to the substratum is very strong, and its risk of being dislodged is small regardless of its orientation to the flow and despite its sub-optimal shape. In contrast, when the animal is crawling rapidly, its adhesion is substantially decreased, and it would probably be dislodged by rapid flow even if the shell were shaped optimally. The risk of dislodgment by waves is therefore functionally independent of shell shape. In essence, despite the extremely high water velocities to which this species is subjected, its shell has had the 'permission' of the flow environment to respond to other selective factors, in particular those associated with its aggressive, territorial behavior. The result is a shell that is both a potent territorial weapon and a functional (albeit less than optimal) hydrodynamic shape.
View details for Web of Science ID 000089453500009
View details for PubMedID 10934004
Limpets are commonly found on wave-swept rocky shores, where they may be subjected to water velocities in excess of 20 m s(-1). These extreme flows can impose large forces (lift and drag), challenging the animal's ability to adhere to the substratum. It is commonly thought that the conical shape of limpet shells has evolved in part to reduce these hydrodynamic forces while providing a large aperture for adhesion. This study documents how lift and drag actually vary with the shape of limpet-like models and uses these data to explore the potential of hydrodynamic forces to serve as a selective factor in the evolution of limpet shell morphology. At a low ratio of shell height to shell radius, lift is the dominant force, while at high ratios of height to radius drag is dominant. The risk of dislodgment is minimized when the ratio of height to radius is 1.06 and the apex is in the center of the shell. Real limpets are seldom optimally shaped, however, with a typical height-to-radius ratio of 0.68 and an apex well anterior of the shell's center. The disparity between the actual and the hydrodynamically optimal shape of shells may be due to the high tenacity of limpets' adhesive system. Most limpets adhere to the substratum so strongly that they are unlikely to be dislodged by lift or drag regardless of the shape of their shell. The evolution of a tenacious adhesion system (perhaps in response to predation) has thus preempted selection for a hydrodynamically optimal shell, allowing the shell to respond to alternative selective factors.
View details for Web of Science ID 000089453500008
View details for PubMedID 10934003
Hydrodynamic forces imposed by ocean waves are thought to limit the size of nearshore plants and animals, but it has proved difficult to determine the mechanism. Explanations based on the scaling mismatch between hydrodynamic accelerational forces and the strength of organisms do not work. Mechanisms that incorporate the allometry of drag and strength accurately predict the maximal size of intertidal algae but not of animals, and internally imposed inertial forces may explain the limits to size in large kelps. The general question of size in wave-swept organisms remains open and intriguing.
View details for Web of Science ID 000084691600024
View details for PubMedID 10562529
Life in the highly turbulent surf zone poses a severe challenge to reproduction in free-spawning animals. Not only can breaking waves quickly dilute the gametes shed by spawning organisms, but turbulence-induced shear stresses may limit fertilization and interfere with normal development. A Couette cell was used to re-create some of the effects of turbulent water motion to study effects of environmentally relevant shear stresses on fertilization in the purple sea urchin (Strongylocentrotus purpuratus). Although low shear stresses improved fertilization success (presumably by increasing mixing), exposure to high shear stresses (of the magnitude found in the surf zone) substantially decreased fertilization success, probably by interfering with contact between egg and sperm. Furthermore, eggs fertilized at high shear stresses often showed abnormal development and low survival of eggs through the blastula stage.
View details for Web of Science ID A1995QH33900007
View details for PubMedID 7696387
Invertebrates use mucus in a far broader spectrum of functions than do vertebrates. Examples include: 1. Navigation. The slime trails of grastropods often contain directional information that is used in homing, mating, and predation. 2. Defense. Many invertebrates coat themselves with slippery, distasteful mucus secretions to ward off predators. 3. Desiccation resistance. Limpets and terrestrial snails use a thin barrier of dry mucus as a mechanism for minimizing desiccation. 4. Structural support. Mucus functions as a tensile structural element in feeding nets and mating ropes. A preliminary analysis of these structures indicates that tensile stiffnesses of 10(4)-10(5) N/m2 may be common. 5. Food. The production of mucus can account for up to 80% of the total energy expenditure of some invertebrates. Mucus is often used as a food source, and in some cases is used to enhance the growth of food items. 6. Locomotion. The adhesive locomotion of gastropods is dependent on the unusual mechanical properties of pedal mucus. These properties may set limits to the size and speed of snails and slugs.
View details for Web of Science ID A1989BR39N00029
View details for PubMedID 2701483