Browsing by Author "Patek, Sheila N"

Elastic energy plays important roles in biology across scales, from the molecular to organismal level, and across the tree of life. The ubiquity of elastic systems in biology is partly due to the variety of useful functions they permit such as the simplification of motor control in running cockroaches and the efficient recycling of kinetic energy in hopping kangaroos. Elastic energy is also responsible for ultrafast movements; the fastest movements in animals are not powered directly by muscle, but instead by elastic energy stored in a spring. By demonstrating that the power required to generate ultrafast movements exceeds the limits of muscle, many studies conclude that energy storage is necessary; but, what these studies do not explain is how the properties of a biological structure affect its capacity for energy storage. In this dissertation, I test the general principles of energy storage by investigating elastic systems at three hierarchical levels of organization: a single structure, multiple connected structures, and a spring system connected to muscle. By using a multi-level approach, my aim is to demonstrate, at each of the mentioned levels, how properties of the spring system affect where or how much energy is stored in the system as well as how these conclusions can be combined to inform our understanding of the biomechanics of hierarchical elastic systems.

When considering spring systems at the level of a single structure, morphology is one major structural aspect that affects mechanics. Continuous changes in morphology are capable of dividing a structure into regions that are responsible for the two contradicting functions that are essential for spring function: energy storage (via deformation) and structural support (via resistance to deformation). Using high quality micro computed tomography scans, I quantify the morphology of the mantis shrimp (Stomatopoda) merus, a single structure of the raptorial appendage hypothesized to store the elastic energy that drives ultrafast strikes. Comparing the morphology among the species, I find that the merus in smashers, species that depend heavily on elastic energy storage, have relatively thicker ventral regions and more eccentric cross-sections than spearers, species that strike relatively slower. I also conclude that differential thickening of a region can provide structural support for resisting spring compression as well as facilitate structural deformation by inducing bending. This multi-level morphological analysis offers a foundation for understanding the evolution and mechanics of monolithic systems in biology.

When two or more structures are connected, their relative physical properties determine whether the structures store energy, provide structural support, or some combination of both. Although the majority of elastic energy is stored via large deformations of the merus in smashers, some spearer species show relatively little meral deformation, and it is unclear whether elastic energy is stored in these systems. To determine whether the apodeme (arthropod tendon) provides energy storage in species that exhibit low meral deformation, I measure the physical properties of the lateral extensor apodeme and the merus to which it is connected. Comparisons of these properties show that in the spearer species I tested, the merus has a relatively higher spring constant than the apodeme, which results in the merus providing structural support and the apodeme storing the majority of elastic energy. Comparing the material properties of the apodemes with those of other structures reveals that apodemes and other biological spring systems share similar material characteristics. This study demonstrates that in order to understand the biomechanics of spring systems comprised of connected structures, it is necessary to compare their relative mechanical properties.

Finally, because muscles are responsible for loading spring systems with potential energy, muscle dynamics can affect elastic energy storage in a spring system. Although spring systems can circumvent the limits imposed by muscle via power amplification, they are not entirely independent from muscle dynamics. For example, if an organism has relatively low time to prepare and stretch the spring prior to the onset of movement, the limits of muscle power can dominate energy storage. To test the effects of muscle dynamics on spring loading, I implement a mathematical model that connects a Hookean spring model to a Hill-type muscle model, representing the muscle-tendon complex of the hindlimbs of American bullfrogs, in which the muscle dynamics are well understood and the duration of spring loading is low. I find that the measured spring constants of the tendons nearly maximize energy storage within the duration of in vivo spring loading. Additionally, the measured spring constants are lower than those predicted to produce maximal energy storage when infinite time is available for spring loading. Together, these results suggest that the spring constants of the tendons of American bullfrogs are tuned to maximize elastic energy for small durations of spring loading. This study highlights the importance of assessing muscle dynamics and their effect on energy storage when assessing the functional significance of spring constants.

Recently, a framework of latch-mediated spring actuation (LaMSA) outlined the general mechanism shared by organisms across the tree of life that use springs and latches to generate motion. Specifically, the framework describes how motion is possible through the integration of a motor, spring, latch, and projectile. First, a motor stores elastic potential energy into a spring by deforming it. A latch then mediates the transformation of elastic potential energy in the spring into kinetic energy of the projectile. Comparative analyses within and across diverse organisms that use LaMSA have revealed the remarkable integration between components. For example, differences in how the spring is tuned to the motor can explain variations in the amount of energy stored in a spring. While the characteristics of the spring, such as its stiffness, define the limits of energy storage, the amount of energy that is stored in the spring also depends on how far it is deformed by the motor. Therefore, the characteristics of biological motors, such as the pennation angle of muscle fibers or the permeability of tissues to generate internal turgor pressures, also affect energy storage. Likewise, integration of the latch and projectile cause variations in the amount of energy released by a LaMSA system. Differences in the shape and speed of the latch as well as the mass and shape of the projectile can lead to differences in energy release. I investigate the integration between the spring and projectile in LaMSA systems by comparing how springs change as projectiles increase in mass. Additionally, I examine how the projectile is integrated with its environment. Variations in the materials or masses of the targets impacted by LaMSA systems may lead to differences in interactions, quantified through energy exchange. Likewise, variations in the projectile may affect interactions with the environment. Specifically, projectiles launched by LaMSA systems may have varying aerodynamics depending on the size of the projectile and its motion through the air. I address scaling across springs and projectiles through investigations of three seed-launching species in the witch hazel family (Hamamelidaceae). I examine the integration between the projectile and the environment through investigations of the mandible strikes of a trap-jaw ant (Odontomachus brunneus) and comparing the trajectories of seeds launched by Hamamelis virginiana. In chapter 2, I measured the transfer of energy from the mandibles of a trap-jaw ant, Odontomachus brunneus, into targets of various masses and materials. Using a device that I created and validated, I demonstrated that when the roughly 50 µg mandibles of O. brunneus moving at accelerations of 105 m s-2 impacted a target made of a compliant material, the energy losses were lower than expected from traditional drop tests on the same material (using much larger masses and lower accelerations). Additionally, I found that strikes against targets that weighed 0.4 grams had similar amounts of energy transfer as targets that were fixed in place suggesting that strikes against masses above 0.4 grams would be inertially similar. In chapter 3, I compared the amount of elastic potential energy stored in the springs of three seed-launching species in the witch hazel family (Hamamelidaceae). These three species share a similar seed launching mechanism. I revealed that across an order of magnitude in seed masses, launch speeds remained constant due to differences in the capacity of the springs to store elastic potential energy. As seed mass increased, spring mass increased along with the spring’s capacity to store elastic potential energy. Finally, as fruits increased in size, less elastic potential energy was converted to kinetic energy of the seed, suggesting a trend of increased energetic losses as spring-launch systems increase in size. In chapter 4, I discovered that the range of H. virginiana seeds was affected by launch angle, seed kinetic energy, drag, and lift. Individually, launch angle, seed kinetic energy, drag and lift did not explain the variance in the seed’s range. Instead, combinations of these parameters, specifically, the combination of launch angle and kinetic energy and the combination of drag and lift, better explained variations in range. Between these combinations of parameters, the ballistic range of seeds was most sensitive to changes in drag and lift. Additionally, I found that the periodic oscillations in the orientation of the seed throughout its trajectory were associated with the magnitude of drag and the magnitude and direction of lift. Overall, this dissertation presents new insights about the impact dynamics of small, high acceleration impacts, the scaling of springs and projectiles, and unexpected aerodynamics of spinning projectiles. LaMSA systems that impact targets may vary in energy release depending on the material and mass of the target. Additionally, differences in the mass of the projectile may lead to changes in the energy storage capacity of springs. Finally, the range that LaMSA systems can launch their seeds may depend on how the seed is launched as well as the interactions between the seed and air. Through this dissertation, I present how, through large datasets and comprehensive analyses, we can understand the integration between the spring, projectile, and environment.

Contests are essential parts of an animal’s life history, as they dictate access to critical resources like mates, food, or territory. Studying how animals efficiently assess competitive ability to resolve contests is a central goal of research in animal behavior. Additionally, studies of how animals use traits like signals and weapons in contests lends insight to the evolution of those traits. In this thesis, I study assessment and resolution of territorial contests – as well as the function of signals and weapons in contests – in the mantis shrimp Neogonodactylus bredini (Stomatopoda: Crustacea).

Behavioral theory predicts that animals may use visual or other displays to communicate reliable information on ability, resolving contests without the use of potentially costlier combat, such as biting, grasping, or striking with weapons. In Chapter 2, I show that N. bredini do not match these predictions – the size of structures presented during visual weapon displays did not correlate with strike performance, and almost all contests involved weapon use via high-force striking. Because most strikes were exchanged on the armored telson (tailplate), I hypothesized that the ritualized “telson sparring” behavior helps competitors avoid contest costs and functions as a signal, instead of dangerous combat.

Studies of assessment help show what information competitors use to make decisions during contests and can reveal the role specific behaviors play. In Chapter 3, I show that N. bredini use mutual assessment during both size-matched and non size-matched contests; that is, competitors gather information about both themselves and their opponent. I also show the role telson sparring and other behaviors play during this assessment.

Finally, in Chapter 4, I test how the energetic cost of delivering sparring strikes scales with body size. I find that larger competitors used proportionally more energy when striking, that this positive scaling of energy resulted in constant scaling of velocity across size, and that these results matched predictions from a mathematical model of the strike mechanism. Furthermore, I show that these scaling dynamics are different from those of strikes delivered in another behavioral context: feeding on hard-shelled prey.

Overall, this thesis shows that the use of deadly weapons in contests should not be assumed as dangerous combat; instead, I show how ritualized behaviors allow for weapon use to function in assessment. The approaches used and conclusions made from this thesis can inform work in contest behavior, functional morphology, and biomechanics.

Latch-mediated spring actuation (LaMSA) mechanisms allow a broad diversity of organisms to achieve ultrafast motion. Most research into biological LaMSA mechanisms focuses on a narrow size or age range of the organism when the LaMSA mechanism is fully developed. However, the emergence of LaMSA morphology and behavior during early life history offers novel insights into the scaling and ecology of ultrafast movement. In this thesis, I establish the emergence and kinematics of LaMSA morphology in two systems, the mantis shrimp Gonodactylaceus falcatus (Stomatopoda) and the snapping shrimp Alpheus heterochaelis (Alpheidae). I also examine the plasticity of LaMSA development in the snapping shrimp Alpheus heterochaelis. The mantis shrimp’s spring-actuated strike is one of the best-studied LaMSA mechanisms; however, we do not know when the LaMSA morphology or behavior emerges during development. In Chapter 2, I found that the mantis shrimp G. falcatus develop their LaMSA morphology in their fourth larval stage when they transition into the pelagic zone and begin feeding on plankton. Mathematical and physical models of LaMSA kinematics suggest that smaller mechanisms generate greater accelerations. Therefore, I hypothesized that larval mantis shrimp would accelerate their strikes faster than adult mantis shrimp. Larval kinematics showed that larvae achieve accelerations on par or lower than adult mantis shrimp species. However, the larval strikes are much faster than the swimming speeds of other small pelagic organisms. Snapping shrimp generate cavitation bubbles using a LaMSA mechanism in their major claw. However, we do not know when the snapping shrimp LaMSA morphology or behavior emerges during development, nor whether they can generate cavitation bubbles at that size. In Chapter 3, I establish that the snapping shrimp Alpheus heterochaelis develop LaMSA morphology and behavior between one- and two months after hatching, when their carapace is roughly four to five millimeters long. I again hypothesized that the juvenile snapping shrimp would generate accelerations much faster than adults. My data show that juvenile snapping shrimp can generate accelerations two orders of magnitude faster than adults when the juvenile is more than two orders of magnitude smaller in claw mass. Juvenile snapping shrimp struck so quickly that they generated and directed cavitation bubbles at the millimeter scale. Developmental stressors can affect how morphological traits grow across ontogeny. In some cases, resource allocation to specific body parts during development can mitigate the negative effects of stress. To our knowledge, the developmental plasticity of LaMSA morphology and kinematics has not been explored. In Chapter 4, I test whether the development of the snapping shrimp LaMSA morphology and kinematics is affected by changes in feeding frequency. Juvenile snapping shrimp fed less frequently during development grew more slowly than better-fed individuals. However, the snapping shrimp raised in the least frequently fed group developed slightly larger snapping claws relative to their body size than individuals in other food treatments. Feeding treatments did not appear to affect the scaling of LaMSA kinematics. This thesis shows that the emergence of LaMSA morphology and behavior inform ecological transitions across ontogeny. The findings from this work can provide novel insights into how size may constrain ultrafast motion. The methods and systems I developed offer new systems and approaches for learning about the scaling and plasticity of spring-actuated movement.

Animal weapons are morphologies used in contests over limited resources like food, shelter, and mates. Individuals with larger weapons tend to win contests, so evolution can favor large weaponry. Yet, the specific functional benefits that weaponry provides are often unclear. Further, the mechanisms that prevent individuals from growing arbitrarily large weapons remain hotly debated. In this thesis, I quantified the functional and competitive benefits of large weapons in snapping shrimp, Alpheus spp. Then, I resolved two apparent paradoxes that arise from this finding. First, if large weapons are beneficial, then what prevents individuals from growing arbitrarily large weapons? Second, if weapons are costly, then how can they scale with positive allometry? Taken in sum, my findings demonstrate that the costs and benefits of weaponry interact to explain how weapon size varies with body size, sex, and season.

In Chapter 2, I determined the competitive benefits of large weaponry. By performing behavioral experiments, I showed that weapons are used as armaments, not signals. Then, using high-speed videos with synchronous sound pressure measurements, I showed that as weapon size increases, the duration of the cavitation bubble and the pressure imposed by the snap also increase.

In Chapter 3, I showed that snapping shrimp also benefit from large weaponry by improving pairing success. Using field observations, I showed that for male snapping shrimp, larger weapons were positively correlated with the probability of being paired and the relative body length of their pair mate. Females exhibited neither trend. That indicates a male-specific paring benefit of large weaponry. Furthermore, using the same dataset, I showed that females exhibit sex-specific tradeoffs between egg production and weapon size. These sex-specific costs and benefits explain why snapping shrimp males have larger proportional weapon sizes than females. It can also explain why that sex difference amplifies during the breeding season.

Finally, in Chapter 4, I showed that snapping shrimp minimize their energetic maintenance costs to achieve positive allometry and weapon exaggeration. Energetic maintenance costs are the costs of maintaining homeostasis. Because tissues vary in their energetic maintenance costs, I used proportional tissue composition as a proxy. I discovered that as weapon size increased, the proportion of the claw comprised of energetically expensive soft tissue decreased. Thus, larger weapons had lower proportional energetic maintenance costs, which could facilitate positive allometry of weapon size. Additionally, exaggerated weapons, which I quantified using residuals from the weapon scaling relationship, had lower proportions of energetically expensive soft tissue compared to non-exaggerated counterparts.

Overall, the dissertation shows that the costs and benefits of weaponry underlie predictable variation in weapon size in snapping shrimp. Canonically, this logic has been used to explain honest scaling relationships based on size, condition, or quality. I extended these classic theories to explain sex differences, seasonal oscillations, and exaggeration in animal weapons.