Autotomy, the self-induced loss of a body part, occurs throughout Animalia. A lizard dropping its tail to escape predation is an iconic example, however, autotomy occurs in a diversity of other organisms. Octopuses can release their arms, crabs can drop their claws, and bugs can amputate their legs. The diversity of organisms that can autotomize body parts has led to a wealth of research and several taxonomically focused reviews. These reviews have played a crucial role in advancing our understanding of autotomy within their respective groups. However, because of their taxonomic focus, these reviews are constrained in their ability to enhance our understanding of autotomy. Here, we aim to synthesize research on the ecology and evolution of autotomy throughout Animalia, building a unified framework on which future studies can expand. We found that the ability to drop an appendage has evolved multiple times throughout Animalia and that once autotomy has evolved, selection appears to act on the removable appendage to increase the efficacy and/or efficiency of autotomy. This could explain why some autotomizable body parts are so elaborate (e.g. brightly coloured). We also show that there are multiple benefits, and variable costs, associated with autotomy. Given this variation, we generate an economic theory of autotomy (modified from the economic theory of escape) which makes predictions about when an individual should resort to autotomy. Finally, we show that the loss of an autotomizable appendage can have numerous consequences on population and community dynamics. By taking this broad taxonomic approach, we identified patterns of autotomy that transcend specific lineages and highlight clear directions for future research.
Autotomy, the strategy of voluntarily releasing a leg during an encounter with a potential predator or in agonistic interactions between conspecifics, is common in animals. The potential costs of this behavior have been scarcely studied. In addition, locomotion and substrate-dependent performance might be affected by autotomy. We did a comparative and observational study to investigate whether losing legs affects the escape speed and trajectory of harvestmen in the genus Prionostemma Pocock, 1903 (Eupnoi: Sclerosomatidae) on different substrates: soil (the least roughened), smooth bark and mossy bark (the most roughened) in a tropical premontane forest in Costa Rica. We observed that 71% of the individuals found were missing at least one leg. Harvestmen, regardless of leg condition, walked faster and made fewer turns in their trajectory in the soil. While climbing, they were faster on smooth bark than in moss. On all substrates, autotomized individuals were slower and had a more erratic trajectory than intact ones. The type of missing legs (sensory or locomotor) had no influence on the speed or trajectory. We experimentally induced autotomy and found that walking speed on soil decreases if individuals lose a leg. Our findings confirm that losing legs affects locomotion, and we provide novel insights on how locomotion in these harvestmen depends on surface roughness. Our data suggest that moss could be a type of substrate that requires more elaborate skills in balance, orientation and texture recognition than smooth bark.
In order to move successfully in variable conditions, many animals have evolved the ability to switch between several patterns of locomotion or gaits. Here, we describe and differentiate between putative locomotor gaits in the harvestman, an arachnid that uses a hexapod-like alternate tripod gait. We recorded Neotropical harvestmen of the genus Prionostemma moving across a flat surface using high-speed video. We reconstructed three-dimensional trajectories and associated kinematics and found four different locomotor gaits: running, stotting, bobbing and walking. Gaits differed in their performance and postural kinematics, body trajectory, gait diagrams and/or kinetic and potential energy exchange. Our approach points out the importance of using multiple kinematic features to differentiate gaits. The use of a specific gait was not predicted by leg length, body area or sex. We propose testable hypotheses regarding the function of each gait and the factors that drive the evolution of different gaits. Ultimately, the diversity of locomotory gaits can allow animals to respond to different environmental challenges and contexts.
Animals have evolved adaptations to deal with environmental challenges. for instance, voluntarily releasing appendages (autotomy) to escape potential predators. Although it may enhance immediate survival, this self-imposed bodily damage may convey long-term consequences. Hence, compensatory strategies for this type of damage might exist. We experimentally induced autotomy in Prionostemma harvestmen. these arachnids are ideal to examine this topic because they show high levels of leg loss in the field but do not regenerate their legs. We video-recorded animals moving on a horizontal track and reconstructed their 3D trajectories with custom software tools to measure locomotor performance. 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 2 days. This is the quickest locomotor recovery recorded for autotomizing animals. We also found post-autotomy changes in stride and postural kinematics, suggesting a role for kinematic adjustments in recovery. Additionally, following leg loss, some animals changed the gaits used during escape maneuvers, and/or recruited the 'sensory' legs for locomotion. Together, these findings suggest that harvestmen are mechanically robust to the bodily damage imposed by leg loss. Animals face a myriad of challenges during their lives, including predation, parasitism, navigating obstacles, and physiological stress. These challenges often lead to damage and many animals have evolved adaptations to compensate for these injuries. Compensation for damage often involves gradual improvements using developmental, morphological, or behavioral changes 1,2. For instance, animals such as lizards, crickets and damselfly larvae reduce their mobility and become more cryptic after damage from potential predators 3-6. While bodily damage is often unintended, in some species injury is self-imposed and potentially adaptive. For example, many animals voluntarily lose appendages when grabbed by potential predators, a defensive strategy known as autotomy 7. Although important for immediate survival 5,7-10 , the loss of body parts may compromise other aspects of organismal function and, by extension, an individual's long term fitness 11,12. Effects of autotomy include changes for locomotion, foraging, development, sensory biology, longevity, migration, and survival 13-15. With regards to locomotion, stability and maneuverability are altered by autotomy, as found for green anole lizards 16 and leopard geckos 17. Locomotor performance (i.e. acceleration or velocity), often interpreted as evidence of the ability to escape a potentially dangerous interaction, is also affected by autotomy 7. Accordingly, wolf spiders missing legs are slower than intact individuals when running 18,19. Besides performance metrics, another set of movement parameters (stride and posture kinematics) can change after autotomy. For instance, stride length and duty factor (th...
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