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Do Substrate Type and Gap Distance Impact Gap-Bridging Strategies in Arboreal 2 Chameleons? 3 4 Running Title: Prehensile Tail Use Chameleons

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Do Substrate Type and Gap Distance Impact Gap-Bridging Strategies in Arboreal 2 Chameleons? 3 4 Running Title: Prehensile Tail Use Chameleons bioRxiv preprint doi: https://doi.org/10.1101/2020.08.21.260596; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Do substrate type and gap distance impact gap-bridging strategies in arboreal 2 chameleons? 3 4 Running title: Prehensile tail use chameleons 5 Authors: Allison M. Luger1, Vincent Vermeylen1, Anthony Herrel1,2, Dominique Adriaens1 6 1: Ghent University, Evolutionary Morphology of Vertebrates. K.L. Ledeganckstraat 35, 9000 7 Ghent, Belgium. 8 2 : UMR 7179 C.N.R.S/M.N.H.N., Département Adaptations du Vivant, Bâtiment d'Anatomie 9 Comparée, 55 rue Buffon, 75005, Paris, France. 10 Corresponding author: Allison M. Luger: [email protected] 11 Keywords: Chameleons, Prehensility, gap bridging, substrate type 12 Summary statement 13 Chameleons use their prehensile tail more often when crossing greater distances and switch 14 strategies on when and how they use their tails. Males are able to cross relatively greater 15 distances than females. 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.21.260596; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 16 Abstract 17 Chameleons are well-equipped for an arboreal lifestyle, having zygodactylous hands and feet as 18 well as a fully prehensile tail. However, to what degree tail use is preferred over autopod 19 prehension has not been studied to date. Using an experimental set-up, where chameleons had 20 to cross gaps of varying distances, we tested the effect of substrate diameter and type on tail use 21 in Chamaeleo calyptratus. Our results show that when crossing greater distances, C. calyptratus 22 is more likely to use its tail for additional stability. The animals were able to cross greater distances 23 (up to 1.75 times the shoulder-hip length) on perches with a rougher material. We saw that 24 depending on the distance of the gap, chameleons would change their crossing strategy on how 25 they use their prehensile tails. With shorter gaps the tails either do not or only touch the perch 26 without coiling around it. With larger distances the tails are fully coiled, and with the largest 27 distances the tails are fully coiled around the perch and after repositioning the hind legs, shifted 28 towards the end of the perch. Males were able to cross relatively greater distances than females, 29 likely due to their larger size and strength. 30 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.21.260596; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 31 Introduction 32 Arboreal habitats consist of complex three-dimensional structures with discontinuities, thus 33 leaving gaps between solid surfaces (Cartmill, 1974). Animals living in such arboreal 34 environments may be challenged with the task of crossing these gaps in order to create a more 35 direct path through the forest, avoiding long and possibly dangerous and costly detours to reach 36 their destination. When crossing, an animal will either have to reach for the other branch, leaving 37 a portion of the body unsupported, leap, glide, or fly to reach the other side of the gap. These 38 strategies all impose different mechanical demands on the locomotor system of the animal. While 39 most studies have focused on the horizontal movement over branches, there have been some 40 studies done focusing on the movement between branches, such as in arboreal snakes (Hoefer 41 et al., 2013; Byrnes et al., 2012) or primates (Thorpe et al., 2009). An extensive study on the 42 various methods of gap crossing was performed by Graham et al. (2020), though this did not 43 include the use of prehensile tails. Peterson (1984) studied the locomotion of chameleons, 44 focusing on the adaptations of the limbs and tail. Chameleons, which are not known for their 45 leaping abilities, move between perches by extending their front limbs, relying on their hind limbs 46 and tail for support. The pectoral girdle is not fixed relative to the body wall allowing it to slide and 47 rotate further in the sagittal plane, giving it a greater reach allowing chameleons to cross larger 48 distances compared to other arboreal squamates such as anoles (Peterson, 1984). 49 Several morphological and functional adaptations have evolved in chameleons to accommodate 50 an arboreal lifestyle including zygodactylous hands and feet and a fully prehensile tail (Gans, 51 1967). Their zygodactylous hands and feet form grasping appendages that can hold onto narrow 52 branches, while their tail has modifications both in the musculature and the caudal vertebrae (Ali, 53 1948; Zippel et al., 1999; Bergmann et al., 2003; Luger et al., 2020). These characteristics serve 54 multiple purposes for arboreal chameleons and are not only restricted to movement on narrow 55 perches in the forest canopy, climbing, or bridging gaps but are also important during social 56 behavior. Indeed, when males encounter each other, this often results in fighting during which a 57 male will attempt to toss the other from their shared branch (Measey et al., 2009). 58 Long tails are often thought to be adaptations for an arboreal lifestyle in chameleons (Bickel and 59 Losos, 2002). Prehensile-tailed arboreal chameleons have longer tails with more vertebrae, 60 compared to terrestrial chameleon species. This allows them to coil their tail multiple times around 61 a perch, thereby increasing the contact area and thus friction. This results in an improved tail 62 gripping performance compared to non-prehensile-tailed chameleon species (Herrel et al., 2012; 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.21.260596; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 63 Luger et al., 2020). While the effect of hand/feet size and tail length on gripping abilities has been 64 studied, little is known, however, on how chameleons use their prehensile tail on different 65 substrates or perches of different diameters. The use of the tail to increase gripping performance 66 can be expected when bridging large gaps between branches, or when having to grip onto 67 smooth, low-friction substrates. Therefore, we studied how chameleons change the way they use 68 their when confronted with different conditions including gaps of different sizes, different substrate 69 diameters, or different substrate roughness. We also wanted to compare sexual differences in 70 this behavior. 71 Chamaeleo calyptratus (Duméril and Bibron, 1851) a large-sized arboreal chameleon, was used 72 for this study. We first quantified whether chameleons changed the use of their tail when substrate 73 roughness, perch diameter, and gap distance were modified. We predicted an increase in tail use 74 on smoother substrates as this would also decrease the grasping ability of the hands and feet. 75 We further predicted that when bridging greater gaps animals would have to suspend their body 76 while gripping the perch with their hind legs and tail. When crossing greater gaps, the center of 77 mass of the animal is being suspended further from the points of attachment in the feet and tail. 78 We therefore also predicted that as gap distance increases that the animals would resort to more 79 often use their tail as an anchor. We further predicted that when on perches with a rougher 80 surface, chameleons should be able to cross greater gap distances. Many chameleons, including 81 C. calyptratus are sexually dimorphic in body size, tail length and hand and feet span (Bickel and 82 Losos, 2002). In dwarf chameleons of the species Bradypodion males also have larger hands and 83 feet and longer tails resulting in a higher gripping force compared to females (Herrel et al., 2011; 84 Da Silva et al., 2014). Consequently, we predicted differences in how chameleons use their 85 prehensile tail based on sex-related size variation. We specifically predict that males would be 86 able to cross greater distances as their increased hand and foot length gives them a higher 87 gripping strength, increasing friction and stability, at least on larger perches. We also predicted 88 males to make more successful crossings without using their tail due to their higher grip strength. 89 Materials and methods 90 Animals 91 Chamaeleo calyptratus specimens (N = 9; five males and four females) were obtained via a 92 private breeder in Paris, France at 10 weeks of age. The animals were at least one year old and 93 sexually mature at the start of the experiments. We chose to use C. calyptratus because of their 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.21.260596; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
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