Compensating for damage: the mechanical, behavioral, and ecological consequences of leg loss for harvestmen

All animals face environmental challenges throughout their lifetimes. Predation attempts and agonistic interactions, for instance, are common challenges across taxa. These pressures can lead to bodily damage. One form of damage arises from the common and widespread strategy to avoid predation known as ‘autotomy’, the voluntary loss of appendages to distract predators and escape. This strategy could come with costs as appendages are used for a variety of essential behaviors, and damage through leg loss may put individuals at a fitness disadvantage. Given the ubiquitous nature of predation, compensatory strategies could evolve to allow animals to ameliorate any fitness consequences associated with this defensive strategy./nThe main goal of my dissertation was to understand the evolution of autotomy as a defensive strategy by examining its consequences on locomotion, habitat use and survival. This approach allowed me to (1) explore the consequences of leg loss, (2) infer about the potential trade-offs between this defensive strategy and biomechanical processes, and (3) elucidate any strategy used to compensate for those consequences. I studied these aspects in several species of ‘harvestmen’ or ‘daddy long-legs’ (Arachnida: Opiliones). This widespread arachnid group shows high levels of leg loss in nature, do not regenerate legs, and their legs are crucial for many life-history traits, including locomotion, sensory perception and mating behavior. I used both field and lab experiments to test hypotheses regarding how the mechanisms of locomotion are impacted by leg loss, as well as the ecological effects of this defensive strategy./nTo start exploring the effect of leg loss on locomotion, in chapter 1 I describe and differentiate between putative locomotor gaits in harvestmen. In the Neotropical rainforest of Costa Rica, I recorded harvestmen of Prionostemma moving on a horizontal track with high-speed video. Then, I reconstructed their three-dimensional trajectories with custom software tools to measure locomotor performance and kinematics. I found four locomotor gaits: running, stotting, bobbing, and walking. Gaits differed in their (a) performance and postural kinematics, (b) body trajectory, (c) gait diagrams, and/or (d) kinetic and potential energy exchange. Using a specific gait was not predicted by leg length, body area, or sex. I then proposed testable hypotheses regarding the function of each gait and the factors that drive the evolution of different gaits./nStarting on chapter 2, I studied the implications of bodily damage on the mechanisms of locomotion described above. Although autotomy may enhance immediate survival, this self-imposed bodily damage may convey long-term consequences. Hence, compensatory strategies for this type of damage might exist. I experimentally induced autotomy in Prionostemma harvestmen. Using the custom video recording and software tools I developed, I found that individuals that lost either three legs total or two legs on the same side of the body showed an immediate and substantial decrease in velocity and acceleration. Surprisingly, harvestmen recovered initial performance after two days. This is the quickest locomotor recovery recorded for autotomizing animals. I also found post-autotomy changes in stride and postural metrics, suggesting a role for kinematic adjustments in recovery. Following leg loss, some animals also changed the gaits used during escape maneuvers, r recruited the ‘sensory’ legs for locomotion./nIn chapter 3 I studied how bodily damage –in the form of leg loss– can impose costs on the energetics of locomotion. For instance, moving with fewer legs may be more energetically costly. I tested if losing legs affects the endurance and the metabolic costs of locomotion in Nelima paessleri harvestmen from the coastal forest of California, USA. I used flow-through respirometry as animals moved on a treadmill inside a sealed chamber. I found that the total distance moved over time (endurance) decreased gradually with an increasing number of legs lost. Interestingly, oxygen consumption increased for harvestmen that had lost 3 legs, but not for individuals that had lost only a single leg. Thus, leg loss seems to differentially affect the two aspects of locomotion, which seem to have different ecological and evolutionary implications. The inability to sustain locomotion (endurance) may prevent animals to continue moving away from potential predators, while increased oxygen consumption makes movement more costly and compromises the animal’s overall physiological state. The relationship between the number of legs lost and oxygen consumption suggests that individuals have a threshold of a number of legs that can be lost before they experience energetic consequences of bodily damage./nLastly, in chapter 4 I studied the ecological and fitness implications of autotomy on this group of arachnids. Finding shelter and surviving encounters with predators are challenges that may be exacerbated for individuals that have experienced bodily damage. For example, autotomy may have immediate benefits for escaping death, but may have longer-term negative consequences for habitat use and survival. I studied these consequences in a harvestmen species of Prionostemma in the pre-montane forest of Costa Rica. Field revealed no difference in habitat use by intact versus autotomized harvestmen (53% of individuals); both types of individuals roosted with similar frequencies across tree bark, mossy tree, or fern. A mark-recapture field experiment showed that leg loss did not affect my ability to recapture those harvestmen, which ranged between 17 and 24%. Further, recapture rates did not differ between substrates./nAltogether, my findings suggest that harvestmen are mechanically robust to the bodily damage imposed by leg loss. Additionally, these animals could be performing kinematic and behavioral compensation that allows them to withstand the effects of morphological modifications that would otherwise affect the kinematics and physiology of locomotion./nMy research also shows that losing legs via autotomy does not have measurable effects on habitat use or survival in harvestmen, and by extension, fitness. These findings have implications for understanding how animals are able to cope with the effects of environmental pressures. Lastly, my findings might suggest how leg loss is selected and maintained over evolutionary time for defensive purposes.

Advisor: Elias, Damian O