Robustness in Locomotion: The Energetic Cost of Perturbations

Animals must navigate a complex and ever-changing world to find mates, forage for food, and escape from predators. Consequently, the robustness of an animal’s locomotor system (i.e., the capacity for its locomotor system to function despite experiencing perturbations) can have major implications for the animal’s survival and fitness. Perturbations can take a variety of forms, and they may be internal or external to the locomotor system. An internal perturbation may be an injury or the total loss of a body part involved in movement, whereas an external perturbation may be an obstacle that an animal must overcome. Considering the frequency with which they encounter perturbations, terrestrial arthropods appear to have highly robust locomotor systems. They often lose legs, and because they are generally small in stature, they must frequently alter the mechanics of their movements during running to navigate obstacles and terrain variability. Still, terrestrial arthropods include animals with a variety of body plans and locomotor strategies, and the robustness of these animals relative to one another has not been well studied. Furthermore, the relative impacts of different types of internal and external perturbations on individual arthropod locomotor systems are not well studied. A better understanding of the factors that determine how capably locomotor systems overcome perturbations could lead to reveal deeper insights about the diversity of morphologies and behaviors that we observe in arthropods today. At the same time, features of arthropod locomotor systems that confer robustness to particular perturbations could inspire engineers seeking to design robust robots./nMy dissertation explores the costs and limits of robustness in the locomotor systems of cockroaches. Many species of cockroaches are remarkable runners, and they’ve been used extensively in studies about obstacle negotiation and leg loss. I use oxygen consumption to measure the energetic cost of locomotion, and I measure the cost of running before and after leg loss and with and without obstacles present. Initially, I focus on one species of cockroach as I compare the added costs associated with different types of leg loss and the interactive effects of leg loss and obstacle encounters. In the final chapter, I compare the consequences of leg loss among species of cockroach that display distinct morphologies and behaviors. This work emphasizes the context-dependent nature of robustness. Not all perturbations affect the same locomotor system in the same way, and not all locomotor systems experience the same perturbations in the same way./nChapter 1 explores the energetic cost associated with leg loss in the cockroach Blaberus discoidalis, a species which has been used frequently to study the energetics and mechanics of locomotion and has shown itself adept at overcoming perturbations. It seeks to determine if different types of internal perturbations have different consequences for the cockroach. I measured the energetic cost of running and endurance of these animals as they ran on a treadmill across a range of speeds. I looked at how these measurements changed for individuals after losing different pairs of legs, and I sought to relate any changes to observable differences in their stride kinematics. I found energetic costs associated with front and middle leg loss, but not hind leg loss. At the same time, I found reductions in endurance capacity after middle and hind leg loss, but not after front leg loss. Observed changes in the animals’ movements matched with expectations based on the role each pair of legs plays during locomotion. Animals missing front legs were destabilized in pitch, animals missing middle legs were destabilized in roll, and animals missing both middle and hind legs struggled to generate propulsive forces that would have allowed them to move forward in the chamber and extend their runs through intermediate locomotion. These results show that the costs of leg loss depend on the leg lost./nWhereas Chapter 1 focuses on the internal perturbation of leg loss, Chapter 2 considers the costs associated with an external perturbation: regular encounters with a hurdle. It seeks to determine if internal perturbations can affect a locomotor system’s response to external perturbations and vice versa. Again, I focused exclusively on the B. discoidalis cockroach. As in Chapter 1, I measured the energetic cost of running on a treadmill, and I compared that measurement for an individual before and after losing legs from a particular pair of legs. However, trials in Chapter 2 were limited to one speed. In addition, for each condition of leg loss (i.e., intact, five-legged, and four-legged), I measured the cost of running on a flat treadmill and on a treadmill with a hurdle present. Similarly to Chapter 1, I found that, during hurdle negotiation, the costs associated with leg loss also depended on the leg that was lost. Animals missing front legs often appeared out of control when climbing up and down hurdles, but there were no energetic costs associated with front leg loss. In contrast, animals missing middle legs rolled excessively as they clambered over hurdles, and middle leg loss exacerbated the cost of encountering hurdles. Finally, animals missing hind legs did not display an increased cost of encountering hurdles, but they showed they were incapable of overcoming the hurdle at the set speed of the treadmill. These results provide further evidence of the importance of considering a leg’s role in the locomotor system when predicting the impact of its loss. At the same time, the results are specific to the particularities of the experimental set up, and Chapter 2 raises questions about how results would if the speed of the animals varied and if the type and frequency of obstacle encounters varied. A true understanding of the robustness of a biological system requires not just an understanding of the system itself, but also a strong understanding of the ecological and behavioral context in which it operates./nChapter 3 examines how differences in the design of the locomotor system itself influences its robustness. It seeks to determine if an analogous internal perturbation has the same impact on different locomotor systems. It explores the costs of leg loss in three distinct species of cockroach: the gracile sprinter Periplaneta americana, the powerful runner B. discoidalis, and the lumbering burrower Gromphadorhina portentosa. These three species represent a continuum of running performance capabilities, with P. americana cockroaches being the fastest runners and G. portentosa cockroaches being the slowest. There is often a tradeoff between robustness and performance, so it was hypothesized that the species would also represent a continuum of robustness to leg loss, with G. portentosa cockroaches being the most robust and P. americana cockroaches being the least robust. As before, I measured the energetic cost of running on a treadmill, and I compared that measurement for an individual before and after leg loss from a particular pair of legs. P. americana and B. discoidalis cockroaches displayed similar response patterns to leg loss, with front leg loss causing pitch instability and middle leg loss causing roll instability. However, P. americana cockroaches exhibited more extreme responses, with higher energetic costs associated with front and middle leg loss. In addition, whereas B. discoidalis cockroaches maintained the capacity to run at all speeds included in the study, regardless of which legs they lost, most P. americana cockroaches missing their middle and hind legs failed to run at the highest speed in the study. Interestingly, although G. portentosa cockroaches showed a similar response to front leg loss as the other two species, they did not display consistently higher running costs after middle and hind leg loss. In fact, they readily switched to a new gait that minimized roll instability after the loss of two middle legs. These results suggest that, even if locomotor systems consist of superficially similar components that appear to operate in similar ways, the function and relative contribution of those components may vary from system to system. Understanding the impact of a perturbation on a locomotor system requires an understanding of the particularities of that system. The diversity of life represents both an enduring challenge for biologists who wish to understand all of its facets, and a limitless source of opportunity for engineers who seek new inspiration for their inventions.

Advisor: Full, Robert J