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Location of CoM in lizards with original, autotomized and fully regenerated tails. Error bars represent s.e.m. All three points are significantly different from one another (repeated measures ANOVA, P=0.017).
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Animals undergo significant weight change due to a variety of causes. Autotomy, the voluntary shedding of an appendage in response to a predator stimulus, provides an effective model for measuring the effects of rapid weight change on locomotor behavior and the responses to more gradual weight gain, particularly in lizards capable of both autotomiz...
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Context 1
... Journal of Experimental Biology (2014) doi:10.1242/jeb.110916 morphology resulted in a significant anterior shift in location of the CoM from a mean of 65.9±1.6% SVL with the original tail to 52.7±1.6% SVL with no tail and finally, a posterior shift to 60.5±1.3% SVL with a fully regenerated tail (repeated measures ANOVA, F 2,5 =10.174, P=0.017) (Fig. 2). A post hoc comparison indicated a significant difference in the location of the CoM with the original and the fully regenerated tail (t=3.306, d.f.=6, P=0.016), suggesting that the CoM was not restored to its original position. In running trials, geckos ran at speeds ranging from 0.23-2.4 SVL s −1 , and autotomy and regeneration did ...
Citations
... Not only does autotomy represent a rapid loss of body mass, but it also shifts the animal's center of mass forward. Individuals compensate for these changes by altering stride length (Jagnandan and Higham, 2017) and adopting a more sprawled position post-autotomy (Jagnandan et al., 2014;Vollin and Higham, 2021). Additionally, there are significant changes in neuromotor control of hindlimb muscles following autotomy in leopard geckos (Jagnandan and Higham, 2018b). ...
... When the gecko is engaging its hindlimbs to generate forward propulsive forces, the tail may be an important appendage for counterbalancing the body as it moves through the air (Vollin and Higham, 2021). The mechanism by which tail autotomy may cause a reduction in velocity during these lunge strikes is unknown, but we hypothesize that the change is a result of the more sprawled posture geckos adopt after autotomy (Jagnandan et al., 2014), as well as changes in lower hindlimb muscle recruitment during the lunge to avoid balance issues associated with the shifted center of balance (Vollin and Higham, 2021). Quantifying both motor activity, as well as leg function, when feeding on different prey types will be an important next step. ...
Prey capture and subjugation are complex behaviors affected by many factors including physiological and behavioral traits of both the predator and the prey. The western banded gecko ( Coleonyx variegatus ) is a small generalist predator that consumes both evasive prey items, such as spiders, wasps, and orthopterans, and non-evasive prey items, including larvae, pupae, and isopterans. When consuming certain prey (e.g., scorpions), banded geckos will capture and then rapidly oscillate, or shake, their head and anterior part of their body. Banded geckos also have large, active tails that can account for over 20% of their body weight and can be voluntarily severed through the process of caudal autotomy. However, how autotomy influences prey capture behavior in geckos is poorly understood. Using high-speed 3D videography, we studied the effects of both prey type (mealworms and crickets) and tail autotomy on prey capture and subjugation performance in banded geckos. Performance metrics included maximum velocity and distance of prey capture, as well as velocity and frequency of post-capture shaking. Maximum velocity and distance of prey capture were lower for mealworms than crickets regardless of tail state. However, after autotomy, maximum velocity increased for strikes on mealworms but significantly decreased for crickets. After capture, geckos always shook mealworms, but never crickets. The frequency of shaking mealworms decreased after autotomy and additional qualitative differences were observed. Our results highlight the complex and interactive effects of prey type and caudal autotomy on prey capture biomechanics.
... Lastly, reduced speed also occurs in lizards when gravid and when running uphill, after a big meal, or after voluntarily losing a body part (i.e. tail, leg, arm; Gilbert et al., 2023;Jagnandan et al., 2014;Shine, 2003). Despite this knowledge, the interaction between temperature fluctuations and this weight-induced effect on speeds is unknown. ...
Ectothermic animals depend on ambient temperature to regulate internal temperature. This dependence affects many aspects of their behaviour, including locomotion, foraging and reproduction. Additionally, ectotherms are more vulnerable in environments with extreme hourly temperature fluctuations and their activity patterns likely match those of favourable temperatures. Here, we studied Pardosa wolf spiders (Lycosidae) in the highland tropical paramos of Costa Rica. We tested two hypotheses to elucidate the factors that influence variation in locomotor behaviour. First, we tested whether locomotor behaviour is driven by temperature variation. Female spiders experimentally exposed to higher temperatures (30 C) moved approximately four times faster than those exposed to lower temperatures (7 C). Second, we tested whether locomotor behaviour is modulated by the maternal care strategy of these spiders. Females carry an eggsac externally by holding it with the distal spinnerets. The eggsac can represent up to 36% of the spider's body size. However, females moved at the same speed regardless of whether they carried an eggsac or not. This demonstrates that the maternal care strategy does not affect their loco-motor performance. In contrast, temperature plays a crucial role in driving locomotion. Our findings expand our understanding of how temperature fluctuations in extreme environments challenge ecto-therms' ability to move and, by extension, escape predators and locate mates and food.
... Only lizards that possessed original-growth or fully regenerated tails were considered eligible for experimentation because the tail influences locomotor performance and limb kinematics Jagnandan et al. 2014). Lizards were collected and tested in discrete batches to minimize time in captivity before experimentation. ...
Urbanization alters the environment along many dimensions, including changes to structural habitat and thermal regimes. These can present challenges, but may also provide suitable habitat for certain species. Importantly, the functional implications of these habitat shifts can be assessed through the morphology-performance-fitness paradigm, though these relationships are complicated by interactions among habitat choice, other abiotic factors, and morphology across scales (i.e., micromorphology and gross anatomy). The common wall lizard (Podarcis muralis) is one example of a cosmopolitan and successful urban colonizer. Quantifying both shifts in morphology over time and morphology-performance relationships under various ecological contexts can provide insight into the success of species in a novel environment. To examine how morphological variation influences performance, we measured seven gross morphological characteristics and utilized scanning electron microscopy to obtain high-resolution images of a claw from individuals living in established populations in Cincinnati, Ohio, USA. We used a geometric morphometric approach to describe variation in claw shape and then compared the claws of contemporary lizards to those of museum specimens collected approximately 40 years ago, finding that claw morphology has not shifted over this time. We then performed laboratory experiments to measure the clinging and climbing performance of lizards on materials that mimic ecologically relevant substrates. Each individual was tested for climbing performance on two substrates (cork and turf) and clinging performance on three substrates (cork, turf, and sandpaper) and at two temperatures (24ºC and 34ºC). Clinging performance was temperature insensitive, but determined by substrate-specific interactions between body dimensions and claw morphology. Conversely, the main determinant of climbing performance was temperature, though lizards with more elongate claws, as described by the primary axis of variation in claw morphology, climbed faster. Additionally, we found strong evidence for within-individual trade-offs between performance measures such that individuals who are better at clinging are worse at climbing and vice versa. These results elucidate the complex interactions shaping organismal performance in different contexts and may provide insight into how certain species are able to colonize novel urban environments.
... Locomotory disruption often results from directly altered biomechanics and gait following injury, as has been well established in diverse animals [e.g. crabs, lizards, dogs (Fuchs et al., 2015;Jagnandan, Russell & Higham, 2014;Pfeiffenberger & Hsieh, 2021)]. While this exact mechanism is not always established, a range of motor endpoints are often negatively affected by injury to various appendages, including reduced movement speed and/or acceleration [e.g. in aquatic insects, arachnids, crabs, fish, tadpoles, and lizards (Chapple & Swain, 2002b;Figiel & Semlitsch, 1991;Fu et al., 2013;Houghton, Townsend & Proud, 2011;Krause et al., 2017;Martín & Avery, 1998;Pfeiffenberger & Hsieh, 2021;Robinson, Hayworth & Harvey, 1991a; Townsend et al., 2017)], reduced sprint distance or stamina [e.g. in spiders, tadpoles, and lizards (Brown & Formanowicz, 2012;Chapple & Swain, 2002b;Figiel & Semlitsch, 1991;Martín & Avery, 1998)], and destabilized or eliminated ability to perform certain types of movements [e.g. in crabs and lizards (Fleming & Bateman, 2012;Gillis, Kuo & Irschick, 2013;Pfeiffenberger & Hsieh, 2021;Savvides et al., 2017)]. ...
Mechanical injury is a prevalent challenge in the lives of animals with myriad potential consequences for organisms, including reduced fitness and death. Research on animal injury has focused on many aspects, including the frequency and severity of wounding in wild populations, the short‐ and long‐term consequences of injury at different biological scales, and the variation in the response to injury within or among individuals, species, ontogenies, and environmental contexts. However, relevant research is scattered across diverse biological subdisciplines, and the study of the effects of injury has lacked synthesis and coherence. Furthermore, the depth of knowledge across injury biology is highly uneven in terms of scope and taxonomic coverage: much injury research is biomedical in focus, using mammalian model systems and investigating cellular and molecular processes, while research at organismal and higher scales, research that is explicitly comparative, and research on invertebrate and non‐mammalian vertebrate species is less common and often less well integrated into the core body of knowledge about injury. The current state of injury research presents an opportunity to unify conceptually work focusing on a range of relevant questions, to synthesize progress to date, and to identify fruitful avenues for future research. The central aim of this review is to synthesize research concerning the broad range of effects of mechanical injury in animals. We organize reviewed work by four broad and loosely defined levels of biological organization: molecular and cellular effects, physiological and organismal effects, behavioural effects, and ecological and evolutionary effects of injury. Throughout, we highlight the diversity of injury consequences within and among taxonomic groups while emphasizing the gaps in taxonomic coverage, causal understanding, and biological endpoints considered. We additionally discuss the importance of integrating knowledge within and across biological levels, including how initial, localized responses to injury can lead to long‐term consequences at the scale of the individual animal and beyond. We also suggest important avenues for future injury biology research, including distinguishing better between related yet distinct injury phenomena, expanding the subjects of injury research to include a greater variety of species, and testing how intrinsic and extrinsic conditions affect the scope and sensitivity of injury responses. It is our hope that this review will not only strengthen understanding of animal injury but will contribute to building a foundation for a more cohesive field of ‘injury biology’.
... Selection on robustness for behaviors in other contexts is also likely. For instance, the ability to compensate for autotomy on locomotion likely drives the multiple mechanical, behavioral, and morphological compensatory mechanisms that animal use to mitigate the effects of leg loss (Jagnandan et al. 2014;Jagnandan and Higham 2017;Wilshin et al. 2018;Escalante et al. 2020). ...
Defensive strategies, like other life-history traits favored by natural selection, may pose constraints on reproduction. A common anti-predator defense strategy that increases immediate survival is autotomy—the voluntary release of body parts. This type of morphological damage is considered to impose future costs for reproduction and fitness. We tested an alternative hypothesis that animals are robust (able to withstand and overcome perturbations) to this type of damage and do not experience any fitness costs in reproductive contexts. We explored the effects of experimental leg loss on the reproductive behavior of one species of Neotropical Prionostemma harvestmen. These arachnids undergo autotomy frequently, do not regenerate legs, and their courtship and mating necessitate the use of legs. We assessed the effect of losing different types of legs (locomotor or sensory) on courtship behavior and mating success in males. We found no differences in the mating success or in any measured aspect of reproductive behavior between eight-legged males and males that experienced loss of legs of any type. Additionally, we found that morphological traits related to body size did not predict mating success. Overall, our experimental findings support the null hypothesis that harvestmen are robust to the consequences of morphological damage and natural selection favors strategies that increase robustness.
Significance statement
In order to survive encounters with predators, animals have evolved many defensive strategies. Some of those behaviors, however, can come with a cost to their overall body condition. For example, some animals can voluntarily lose body parts (tails, legs, etc.) to escape. This process can then affect many aspects of an animal’s life, including reproduction. In a group of harvestmen (daddy long-legs) from Costa Rica, we tested the hypothesis that males are robust to the potential consequences of losing legs, and will not experience costs. We found that males that lost either legs used for locomotion or for sensory perception reproduced in the same way as animals with all of their legs. Consequently, we demonstrate that these arachnids are able to withstand the loss of legs with no effects on reproduction.
... These values correspond to the mean relative mass of the lost tail in individuals of each sex (see "Study species" above). Although tail loss probably promotes a forward displacement of the center of mass (see Jagnandan et al. 2014 for an example with lizards), by gluing the tail or the cylinder along the central axis of the mesosoma (Fig. 2), we tried to avoid further shifts on the center of mass of the individuals. For unloaded individuals of the intact and autotomized groups, we applied only a glue drop onto their dorsum. ...
... In lizards, for instance, tail loss shifts the center of body mass anteriorly, reducing hind limb propulsive force and consequently impairing locomotor performance (e.g. Ballinger et al. 1979;Jagnandan et al. 2014; see also Gillis et al. 2013). However, the data obtained in our short-term experiment do not provide support to the hypothesis that a shift in the center of body mass caused by tail autotomy decreases locomotor performance of male and female scorpions. ...
... Moreover, only a few studies accessed the long-term effects of tail autotomy. An example is a study with the leopard gecko Eublepharis macularius that showed that the running speed does not change over the 22 weeks required for tail regeneration, even though the body mass of the individuals shows a marked increase due to tail regeneration (Jagnandan et al. 2014). Thus, despite the difference in the mechanisms that promote an increase in body mass in A. balzani (constipation) and E. macularius (tail regeneration), the long-term consequences of tail autotomy on the locomotor performance seem to be dissociated of changes in body weight. ...
In many taxa, individuals voluntarily detach a body part as a form to increase their chances of escaping predation. This defense mechanism, known as autotomy, has several consequences, such as changes in locomotor performance, that may affect fitness. Scorpions of the genus Ananteris autotomize the ‘tail’, which in fact corresponds to the last abdominal segments. After autotomy, individuals lose nearly 25% of their body mass and the last portion of the digestive tract, including the anus, which prevents defecation and leads to constipation, because regeneration does not occur. Here, we experimentally investigated the short- and long-term effects of tail loss on the locomotor performance of Ananteris balzani. In a short-term experiment, the maximum running speed (MRS) of males and females did not change after autotomy. Moreover, the relative mass of the lost tail did not affect the change in MRS after autotomy. In a long-term experiment, autotomy had a negative effect on the MRS of males, but not of females. Autotomized over-fed individuals suffered from severe constipation but were not slower than autotomized normally fed individuals. In conclusion, tail loss has no immediate effect on the locomotor performance of scorpions. The long-term decrease in the locomotor performance of autotomized males may impair mate searching. However, because death by constipation takes several months, males have a long time to find mates and reproduce. Thus, the prolonged period between autotomy and death by constipation is crucial for understanding the evolution of one of the most extreme cases of autotomy in nature.
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... However, we found that sprint speed was unaffected by tail loss but by the relative length of the regenerated portion of the tail, i.e., the longer the regenerated tail, the higher the sprint speed. Still, this effect was meager, unlike patterns documented elsewhere for eublepharids, lacertids, and skinks, [46,[98][99][100]. Caudal autotomy has no impact on the locomotor performance of some lizard species [19,20]. ...
Caudal autotomy is a striking adaptation used by many lizard species to evade predators. Most studies to date indicate that caudal autotomy impairs lizard locomotor performance. Surprisingly, some species bearing the longest tails show negligible impacts of caudal autotomy on sprint speed. Part of this variation has been attributed to lineage effects. For the first time, we model the effects of caudal autotomy on the locomotor performance of a gymnophthalmid lizard, Micrablepharus atticolus, which has a long and bright blue tail. To improve model accuracy, we incorporated the effects of several covariates. We found that body temperature, pregnancy, mass, collection site, and the length of the regenerated portion of the tail were the most important predictors of locomotor performance. However, sprint speed was unaffected by tail loss. Apparently, the long tail of M. atticolus is more useful when using undulation amidst the leaf litter and not when using quadrupedal locomotion on a flat surface. Our findings highlight the intricate relationships among physiological, morphological, and behavioral traits. We suggest that future studies about the impacts of caudal autotomy among long-tailed lizards should consider the role of different microhabitats/substrates on locomotor performance, using laboratory conditions that closely mimic their natural environments.
... While salamanders' terrestrial movements are characterized by standing waves, leopard geckos initially generate a standing wave which changes to a traveling wave as it moves more posteriorly (Hamley 1990). It was previously thought that tail autotomy in lizards caused changes in locomotion because of a change in mass or shift in center of mass, but it appears that these changes are due to the loss of tail undulations during locomotion (Jagnandan et al. 2014). The loss of tail undulations caused the leopard geckos to adopt a more sprawling posture and decreased femur retraction and step length (Jagnandan and Higham 2017). ...
Lateral undulation and trunk flexibility offer performance benefits to maneuverability, stability, and stride length (via speed and distance traveled). These benefits make them key characteristics of the locomotion of tetrapods with sprawling posture, with the exception of turtles. Despite their bony carapace preventing lateral undulations, turtles are able to improve their locomotor performance by increasing stride length via greater limb protraction. The goal of this study was to quantify the effect of reduced lateral flexibility in a generalized sprawling tetrapod, the tiger salamander (Ambystoma tigrinum). We had two potential predictions: (1) either salamanders completely compensate by changing their limb kinematics, or (2) their performance (i.e., speed) will suffer due to the reduced lateral flexibility. This reduction was performed by artificially limiting trunk flexibility by attaching a 2-piece shell around the body between the pectoral and pelvic girdles. Adult tiger salamanders (n = 3, SVL = 9 cm-14.5 cm) walked on a 1 m trackway under three different conditions: unrestricted, flexible shell (Tygon tubing), and rigid shell (PVC tubing). Trials were filmed in a single, dorsal view, and kinematics of entire midline and specific body regions (head, trunk, tail), as well as the fore and hindlimbs, were calculated. Tygon individuals had significantly higher curvature than both PVC and unrestricted individuals for the body, but this trend was primarily driven by changes in tail movements. PVC individuals had significantly lower curvature in the trunk region compared to unrestricted individuals or Tygon; however, there was no difference between unrestricted and Tygon individuals suggesting the shells performed as expected. PVC and Tygon individuals had significantly higher curvature in the tails compared to unrestricted individuals. There were no significant differences for any limb kinematic variables among treatments including average, minimum, maximum angles. Thus, salamanders respond to decreased lateral movement in their trunk by increasing movements in their tail, without changes in limb kinematics. These results suggest that tail undulations may be a more critical component to sprawling-postured tetrapod locomotion than previously recognized.
... For most lizards including gekkonids, an intact tail plays a vital role in locomotion, e.g., balance, locomotor performance, ecological flexibility, foraging, predation avoidance, obstacle evasion (Ballinger 1973;Garland and Losos 1994;Iverson et al. 2004;Ofori et al. 2018), storage of nutrients (Daniels 1984), and intraspecific interaction, e.g., courtship, mating, social status, territory defense (Bateman and Fleming 2009;McElroy and Bergmann 2013;Jagnandan et al. 2014). However, their ability to shed the tail and regenerate it does not always function perfectly and may result in unusual tail malformation during regeneration. ...
This study highlights the ecology, natural history, and a new distribution record by providing a unique habitat occurrence record in karst ecosystem and describes a tail anomaly of the endemic Mamanwa Bent-toed Gecko Cyrtodactylus mamanwa in the province of Dinagat. The detection of a new population on Unib Island in the southwestern Dinagat extends the previously known distribution of this gekkonid by approximately 100 km south from its known distribution.
... However, we found that sprint speed was unaffected by tail loss but by the relative length of the regenerated portion of the tail, i.e., the longer the regenerated tail, the higher the sprint speed. Still, this effect was meager, unlike patterns documented elsewhere for eublepharids, lacertids, and skinks, [46,[98][99][100]. Caudal autotomy has no impact on the locomotor performance of some lizard species [19,20]. ...
Caudal autotomy is a dramatic adaptation used by many lizard species to evade predators. Most studies to date indicate that caudal autotomy impairs lizard locomotor performance. Surprisingly, some species bearing the longest tails show negligible impacts of caudal autotomy on sprint speed. Part of this variation has been attributed to lineage effects. For the first time, we model the effects of caudal autotomy on the locomotor performance of a gymnophthalmid lizard, Micrablepharus atticolus, characterized by a long and bright blue tail. To improve model accuracy, we incorporated the effects of several covariates. We found that body temperature, pregnancy, mass, collection site, and the length of the regenerated portion of the tail were the most important predictors of locomotor performance in Micrablepharus atticolus. However, sprint speed was unaffected by tail loss. Apparently, the long tail of M. atticolus is more useful when using undulation amidst the leaf litter and not when using quadrupedal locomotion on a flat surface. Our findings highlight the intricate relationships among physiological, morphological, and behavioral traits. We suggest that future studies about the impacts of caudal autotomy among long-tailed lizards should consider the role of different microhabitats/substrates on locomotor performance, using laboratory conditions that closely mimic their natural environments.
