ORIGINAL Asian Herpetological Research 2020, 11(4): 342–349 ARTICLE DOI: 10.16373/j.cnki.ahr.200029

The Relationship between Shell Morphology and Crevice Size Affecting Retreat Selection of the Keeled Box Turtle (Cuora mouhotii)

Fanrong XIAO1#, Zhen HONG1#, Jichao WANG1, Taggert BUTTERFIELD2 and Haitao SHI1*

1 Key Laboratory for Ecology of Tropical Islands of Ministry of Education; Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province; College of Life Sciences, Hainan Normal University, Haikou 571158, Hainan, China 2 Escuela Nacional de Estudios Superiores Unidad Morelia, Universidad Nacional Autónoma de México, Morelia 58190, México

1. Introduction Abstract Rock crevices are important retreat sites for many reptiles. Unlike lizards and snakes, crevice- The distribution and abundance of organisms is closely related dwelling turtles have rigid shells which severely limit to the availability of suitable microhabitats in the environment, the size and shape of crevices they are able to use. Few especially retreat sites (Bustard, 1969; Price, 1978; Milne and studies have addressed the relationship between turtle’s Bull, 2000; Zhang et al., 2006). Retreat sites can provide refuge shell morphology, behavior, and crevice size. Here, we from predators and access to a stable microclimate (Pringle investigate the relationship between morphology and et al., 2003; Croak et al., 2008). Therefore, availability of retreat crevice size selection in the Keeled box turtle (Cuora sites may have a strong impact on individual fitness as well as mouhotii). We radio tracked turtles in the field to document population viability and it has been shown that organisms non- crevice dimensions and turtle behavior associated with randomly select retreat sites in the environment that can meet crevices, and we conducted a controlled experiment in the their immediate needs. However, retreat sites are not unlimited, lab to understand how a turtle’s morphology influences and the morphology of an organism influences the range of its decision to select crevices with different dimensions. retreat sites that it can utilize. Previous studies have focused Both laboratory and field experiments demonstrate that turtles select deep and moderately wide crevices that are on how the availability of microhabitats in the environment low enough to barely accommodate the carapace. Crevices influences retreat site selection (Milne and Bull, 2000; Pringle used by turtles tend to be about 2 times as wide, 1.2 times as et al., 2003; Croak et al., 2008; Cox et al., 2018), but few have high, and 3 times longer than the turtle’s shell. Moreover, investigated how an organisms morphology affects the retreat turtles tended to prefer crevices with horizontal openings sites they use. in the field and position themselves head first in the crevice. Rock crevices as retreat sites play a central role in the natural We conclude that morphology, especially carapace height, history of many reptile species (Pringle et al., 2003; Croak et influences the Keeled box turtles’ decision to select specific al., 2008). However, unlike snakes, lizards and geckos, crevice- sizes of crevice. We argue that the tendency for turtles to dwelling turtles face a significant challenge because they have select crevices that come into contact with their carapace a rigid shell that limits their ability to utilize crevices smaller contributes to successful defense against predators, as it than their shell. For this reason, rock crevices should be big would be more difficult for a predator to remove a turtle enough to allow turtles to enter and exit, but small enough to when the crevice is nearly touching the turtles shell. prevent predators from removing the turtle. Therefore, turtles’ shell shape likely determines the size of crevices that they can use. For instance, Jackson (1988) found that musk turtles Keywords antipredation, burrow, microhabitat, rock crevice, shelter (Sternotherus spp.) preferred crevices that were low enough to come into contact the carapace, demonstrating that a turtle’s # Both authors contribute equally to this work. shell height is correlated to the crevice height. Nevertheless, * Corresponding author: Dr. Haitao SHI, from College of Life Sciences, Hainan Normal University, Haikou, China, with his research mainly musk turtles are also aquatic and their compressed shell could focusing on ecology, classification, conservation, and captive breeding of reflect an adaptation to be more hydrodynamic in water and tortoises and freshwater turtles. E-mail: [email protected] not to occupy a specific sized crevice (Claude et al., 2003; Bonnet Received: 19 March 2020 Accepted: 15 July 2020 et al., 2010; Benson et al., 2011). In terrestrial turtles on the other Fanrong XIAO et al. Turtle Shell Morphology Predict Crevice Selection No. 4 343 hand, especially rock-dwelling turtles such as the pancake reserve is comprised of approximately 18 389 ha of intact tortoise (Malacochersus tornieri) or Namaqualand speckled rainforest. January is the coldest month, with an average padloper (Chersobius signatus), it is possible that compressed temperature of 15.4 oC, and the hottest month is July, with an shells are an adaptation to utilize a certain size of rock crevice average temperature of 28 oC. Rainfall in the reserve is plentiful, crevice but this remains to be seen (Ireland et al., 1972; Malonza, with 1 870–2 760 mm of precipitation falling annually, mostly 2003; Loehr et al., 2006). Previous studies, such as Shi et al. (1995) during the rainy season (May to October). Radio transmitters and Nasengbate et al. (2013) have investigated the size of soil (diameter ×height = 21 mm × 8 mm) were fitted to the last burrows that turtles select, but studies have not tested if there is pleural scute of the posterior end of the turtles’ carapace in a relationship between burrow size and shell shape. a location that did not inhibit turtles from entering shelters. The Keeled box turtle (Cuora mouhotii) is distributed Turtles were monitored on a regular basis during the study throughout southern China, including Hainan Province (Zhao period, and because they use many different types of shelters and Adler, 1993), and is typically found in moist evergreen we only include shelters that were occupied for more three forest (Wang et al., 2011). Previous work has already shown days into our analysis. For each shelter we recorded the type that the Keeled box turtle has a relatively compressed shell and of shelter (1 = rock crevice, 2 = tree hole, 3 = fallen log, 4 = grass prefers microhabitats with rock crevices in the field (Xiao et al., clump, 5 = bamboo clump, 6 = deciduous leaves) and measured 2017). However, it is not clear what features of rock crevices the maximum width (cm; same throughout), maximum depth, influence their selection, how shell shape determines selection, minimum height (inner crevice height at which the turtle was and what behavior they use when occupying crevices. We located), and maximum height (maximum height at crevice predict that 1) the observation that Keeled box turtles have a opening). We also recorded whether or not the opening of the more compressed shell compared to other turtles in the habitat crevice was horizontal or non-horizontal and how turtles were (e.g. Flower back box turtle Cuora galbiniforns; Xiao et al., 2017) positioned when found in rock crevices. For example, we noted is an adaptation to occupy rock crevices, and 2) that the Keeled if the turtle was positioned in the crevice tail first or head first, box turtle prefer crevices that come into contact with the top of and if the top of the carapace was in contact with the ceiling of their carapace to limit a predators ability to remove them from the rock crevice. crevices. Moreover, because the posterior edge of the Keeled box 2.3. Selection of artificial crevice size in the laboratory turtle’s carapace is serrated (Xiao et al., 2017), we hypothesize To determine if the dimensions of the Keeled box turtle’s 3) that the majority of turtles that we observe in rock crevices carapace influences the crevices it uses, we conducted a in the field will be oriented in the crevice head first, with the laboratory experiment in which we exposed turtles to crevices serrated carapace facing outward as a potential defense from with different depths, widths, and heights. We did these predators. To test these hypotheses, we documented the Keeled experiments in a rectangular enclosure (size: 145 cm ×65 cm; box turtles’ behavior in rock crevices, and the sizes of crevices Figure 1) from April to July 2016 and turtles were exposed to (width, depth, height) that they used in the field. In addition, o ambient temperatures during the experiment (19–22 C). This we did a laboratory experiment in which we manipulated the enclosure was located indoors, but was exposed to natural light dimensions of artificial crevices and documented the preference throughout the day through several windows. To remove any towards different crevices with different dimensions. potential obstacles that might influence a turtles decision to select a shelter, the habitat within the enclosure consisted of 2. Materials and Methods only bare ground and artificial shelters (no vegetation or plants were included within enclosure; Figure 1). All artificial shelters This study was approved by the Animal 2.1. Ethics statement had the same lighting conditions over the course of the day, Research Ethics Committee of Hainan Provincial Education which were consistent throughout the experiment. Turtles were Centre for Ecology and Environment, Hainan Normal fed before, but not during the experiments. University (HNECEE-2014-002) and was carried out in strict The rectangular enclosure was divided into four sections accordance with the institutional guidelines. Fieldwork was and we placed a different sized artificial shelter in three of the carried out with permission from the Diaoluoshan National four sections (Figure 1). No artificial shelter was included in Nature Reserve. No turtles were sacrificed for this study or the fourth section (bare ground) as a control and turtles could incurred injury. move freely between each section. Artificial crevices were 2.2. Size of rock crevice and behavior of turtles in the field assembled using bricks, and depending on the experiment, We tracked 7 adult Keeled box turtles using radio telemetry were designed to exceed the mean length, width, or height of from April 2015 to February 2016 in the Diaoluoshan Natural a turtle by 0.2, 1, and 2 times, respectively. In the crevice width Reserve in Hainan Province, People’s Republic of China. This experiment, for example, we wanted to know if the width of Asian Herpetological Research 344 Vol. 11 crevice influences a turtle’s decision to select a crevice. To do stressed immediately after being released into the enclosure. We this, we put three crevices in their own section of the arena, and reviewed the recordings for each experiment and calculated the each crevice exceed the mean carapace width (11.86 cm) of the amount of time that turtles spent inside each artificial crevice, Keeled box turtle by 0.2 (crevice width = 14.24 cm), 1 (crevice or on bare ground of the enclosure. At the end of experiments, width = 23.73 cm), and 2 (crevice width = 35.59 cm) times the elapsed time that each turtle in the three artificial crevices (Figure 1). The crevice dimensions that were not manipulated in and bare ground was used for subsequent data analysis. each experiment were set to exceed a turtle’s mean dimensions 2.4. Statistical analysis For the field experiment, Chi-squared by 0.5 times. The average measurements of the Keeled box turtle test was used to assess whether the Keeled box turtle differed that were used to determine crevice dimensions were based in its preference of type of shelter. We tested for normality in on the measurements of five individuals and include length = width, depth, and height of crevices used by the Keeled box 17.12 cm, width = 11.86 cm, and height = 6.85 cm. See Table 1 for turtle using a Kolmogorov-Smirnov test. A Chi-square test was dimensions and names of each crevice in each experiment. used to test turtles preference in crevice openings (horizontal During each experiment, five Keeled box turtles were vs. non-horizontal), orientation in the shelter (tail vs. head released individually into the arena and their behavior was first), and whether or not the carapace was in contact with the recorded for 84 hours using 24-hour video monitoring. These roof of the shelter (contact vs. no contact). For the laboratory turtles were the same individuals that were tracked in the experiment, we used generalized linear mixed model (GLMM) field. We only used the last 72 hours (three days) of video to test whether the amount of time (hours) that the Keeled box recordings to collect data because some turtles appeared turtles spent in a particular artificial crevice could be explained

Figure 1 The rectangular enclosure (145 cm × 65 cm) with four sections (three artificial crevices and bare ground) in the laboratory. This picture shows the layout of three artificial crevices with different widths (but with same depth and height) in the rectangular en- closure. All the remaining areas of the enclosure were classified as bare ground except for the artificial crevices.

Table 1 Dimensions of artificial crevices in the three experiments in which we manipulated the width, depth, or height of the crevice. These dimensions were selected to exceed the mean dimension of the Keeled box turtle (Cuora mouhotii) 0.2, 1, and 2 times, respectively. The two artificial crevice dimensions that were not being manipulated were set to exceed the same measurement of a turtle by 0.5 times. Mean carapace width, length, and height of the Keeled box turtle was 11.86 cm, 17.12 cm, and 6.85 cm, respectively (n = 5).

Experiment Crevice 1 Crevice 2 Crevice 3 14.24×30×10.65 cm 23.73×30×10.65 cm 35.59×30×10.65 cm Width (narrow) (medium-wide) (wide) 18.9×20.53×10.65 cm 18.9×34.23×10.65 cm 18.9×51.35×10.65 cm Depth (shallow) (medium-deep) (deep) 18.9×30×8.22 cm 18.9×30×13.7 cm 18.9×30×20.56 cm Height (low) (medium-high) (high) Fanrong XIAO et al. Turtle Shell Morphology Predict Crevice Selection No. 4 345 by the dimensions of the artificial crevice. The time spent inside each section (hours) was tested as a function of crevice type (including bare ground) which was defined as the fixed effect. Whereas, turtle individual number and size (i.e. carapace length, width or height, and each of them corresponds to its own experiment) were defined as random effects. A separate GLMM was done for each experiment. Pair wise comparison of time spent in different sections was tested in the GLMM using pair wise t-tests. All data were expressed as mean ± SE. For all statistical analyses, an alpha level of α = 0.05 was selected as criterion for statistical significance. All statistical analyses were carried out in SPSS 19.0.

3. Results

The seven turtles equipped with radio transmitters had the mean (± SD) carapace length, width, and height of 16.28 ± 0.71 cm (range 14.07–18.30 cm), 11.45 ± 0.19 cm (range 10.19–11.83 cm), and 6.63 ± 0.13 cm (range 6.00–7.10 cm), respectively. From April 2015 to February 2016, turtles were observed inactive in shelters for more than three days on 41 occasions. Of these shelters, 23 were rock crevices (56.10%), 6 were tree holes (14.46%), 5 were bamboo clumps (12.20%), 4 were fallen logs (9.76%), 2 were grass clumps (4.88 of time) and 1 was deciduous leaves (2.44%). Showing that turtles prefer rock crevices when compared to other shelter types (Chi-square test, x2 = 48.415, P < 0.0001). The maximum crevice width (40.74 ± 5.14 cm; range 13–110 cm), maximum crevice depth (57.55 ± 5.31 cm; range 15–110 cm) and the minimum crevice height (9.30 ± 1. 40 cm; range 7–12 cm) were normally distributed (Kolmogorov-Smirnov test, Z = 0.918, P = 0.368; Z = 0.728, P = 0.665; Z = 1.02, P = 0.249; Figures 2A, B, D). Whereas, the distribution of maximum crevice height (15.43 ± 6.29 cm; range 10–36 cm) was right-skewed (skewness = 1.982) and not normally distributed (Kolmogorov-Smirnov test, Z = 1.371, P = 0.047; Figure 2C). These data comprise of 204 independent observations of turtles using 23 different rock crevices, indicating that the Keeled box turtle frequents rock crevices that average 40 cm wide, 57 cm deep, 9 cm minimum height, and 15 cm maximum height. Chi-square test results show that the Keeled box turtles prefer crevices with horizontal openings (95.65%; n = 23, x2 = 19.17, P < 0.0001; Figures 3A, C), prefer to be oriented head first in the shelter (Table 2; Figure 3D), and to be touching the roof of the rock crevice with their carapace (Table 2; Figures 3B, D). In the lab, we analyzed 72 hours of recordings that correspond to 15 recording events (three experiments for each turtle). In each experiment, the GLMM revealed significant effect of treatment (crevice size) on time spent in crevices (width Figure 2 The frequency distribution of maximum crevice width experiment: F = 3.569, P = 0.047; depth experiment: F = (A), crevice depth (B), crevice height (C), and minimum crevice 3,16 3,16 height (D) in the field. 4.062, P = 0.029; height experiment: F3,16 = 3.458, P = 0.041). There Asian Herpetological Research 346 Vol. 11 was no inter-individual (width experiment: Z = 1.34, P = 0.18; that the Keeled box turtle prefers crevices that are about 2 depth experiment: Z = 1.528, P = 0.126; height experiment: Z = times as wide, 1.2 times as high, and 3 times as deep as the turtle. 1.766, P = 0.77) or effect of body size (width experiment: Z = 0.559, P = 0.576; depth experiment: Z = 1.146, P = 0.252; height 4. Discussion experiment: Z = 1.375, P = 0.169) in any of the experiments. In the width experiment, pair wise comparisons of mean time Our study revealed that the Keeled box turtle prefer crevices spent in crevices or bare ground were significantly different that are low enough to barely accommodate the carapace both between all sections, with most time being spent in medium- in the field and the laboratory. To the best of our knowledge, width crevices (Figure 4A). In the depth experiment, pair wise this study is the first to quantify the relationship between comparisons of mean time spent in each crevice or bare ground the crevice height and carapace height in a terrestrial turtle. reveal significance differences between all sections except bare Although some studies focus on how animal morphology ground, with most time being spent in deeper crevices (Figure affects the choice of crevice height ( Jackson, 1988), few studies 4B). In the height experiment, pair wise comparisons of mean have shown that amphibians or reptiles choose low rock time spent in each crevice or bare ground were significant crevices to prevent predators from approaching them (Cooper between all sections except bare ground, with most time was et al., 2000; Thompson and Withers, 2005; Smith et al., 2017). spent in low crevices (Figure 4C). In sum, these results suggest The civets (e.g. Paguma larvata and Paradoxurus hermaphroditus)

Table 2 Behavior of the Keeled box turtles (Cuora mouhotii) while hidden in the rock crevices in the field.

Behavior Frequency (%) Chi-square test Crevice-carapace contact Contact No contact x2 = 98.84, n = 204 173 (84.8) 31 (15.2) P < 0.0001 Orientation Head first Tail first x2 = 96.08, n = 204 172 (84.3) 32 (15.7) P < 0.0001

Figure 3 Two examples of a Keeled box turtle (Cuora mouhotii) in a typical rock crevice in the field. Location of the turtle from a distance can be seen on the left (A, C), inside white circles, whereas a photo of the same turtle inside the crevice (indicated with an arrow) on the right (B, D). All photos were taken by F. XIAO in 2015. Fanrong XIAO et al. Turtle Shell Morphology Predict Crevice Selection No. 4 347 are the predators of the Keeled box turtle in the wild, thereby, choosing a lower crevice helps turtles prevent being predated by these mammals. Our observation that a more compressed carapace allows turtles to fit in lower cervices suggests that the flatted carapace of the Keeled box turtle has evolved a more compressed carapace to fit into rock crevices. The Keeled box turtle preferred crevices with a medium width, indicating that there is a tradeoff between the space turtles needs to move and to avoid predation. Narrow crevices are effective against predators, but cannot be affectively used turtles if they cannot maneuver within the crevice (Schlesinger and Shine, 1994; Milne and Bull, 2000; Williams et al., 2016). Therefore, the medium width of the crevice not only ensures that the turtle has space to turn around and perform other movements, but combined with its small height, prevents predators from taking advantage of the larger space to enter or reach into the crevice. This study found that the Keeled box turtle selected medium-deep crevices in the field, but preferred deep crevices in the laboratory. This may be due to the fact that the medium- deep crevice (57.55 cm) in the field was deeper than the deepest crevice in the laboratory (51.35 cm), which results in the tendency of turtles to choose crevices with the maximum depth available in the laboratory. We have observed that the Keeled box turtle always hides as deep as possible into the rock crevices in the field. The medium-deep rock crevices in the wild are sufficient for protection. We suggest that the Keeled box turtles exhibit a preference for a deeper crevice to reduce the risk of being dragged out by the predators, and to avoid climatic extremes, similarly to other reptiles (Milne and Bull, 2000; Pike et al., 2010 ). In fact, the microclimate of rock crevices in general is an important factor that influences organisms decision to select specific crevices (Mile and Bull, 2000; Pringle et al., 2003; Cox et al., 2018). Therefore, future work should aim to understand how temperature and humidity inside and outside Figure 4 Bar graphs indicating the amount of time that the of rock crevices influences a Keeled box turtle’s decision to select Keeled box turtles (Cuora mouhotii) spent in each section of the specific crevices. rectangular enclosure in each experiment. A, B and C correspond to the experiment in which we manipulated crevice width, depth, Field observations have shown that Keeled box turtles often and height, respectively. Asterisks denote the difference (*P < 0.05) make their carapace touch to the roof of the crevice with the based on pair wise comparisons (all df = 16) in GLMM. help of their limbs. This is consistent with a previous study on musk turtles ( Jackson, 1988), and one explanation for this the carapace and the ceiling of crevice, thus increasing the behavior is that a turtle can better resist a predator trying friction. Many animals prefer this type of crevice because to force it out of a crevice by creating friction between the horizontal openings below big rocks are not easily found by carapace and the roof of the crevice when it extends its limbs ( Jackson, 1988). Our recent research confirmed that the Keeled predators (Schlesinger and Shine, 1994). Another explanation box turtles can produce more friction with their carapaces than is that the preference for the rock crevices which can touch the Flower back box turtles (Cuora galbinifrons) which do not carapace increases the likelihood that turtles will use the lowest utilize rock crevices (unpublished data). We also found that the crevices, because these rock crevices can reduce the available crevices used by the Keeled box turtle had mainly horizontal space for predators ( Jackson, 1988). Our field and laboratory openings in the wild, which increases the contact area between studies confirm that the Keeled box turtle preferred low rock Asian Herpetological Research 348 Vol. 11 crevices, showing that this kind of behavior and morphology References was correlated with the height of crevice. Therefore, the Keeled box turtle’s carapace height was the most important factor in Belleau P. 2008. Habitat selection, movement patterns, and determining the size of the rock crevice when compared with demography of Common Musk Turtles (Sternotherus odoratus) in the carapace length and width. southwestern Quebec. M.S. Thesis, McGill University, Montréal, Canada, 73pp Many aquatic turtles or semi-aquatic turtles, such as musk Benson R. J., Domokos G., Várkonyi P., Reisz R. 2011. Shell turtles, prefer mud or vegetation for shelter (Belleau, 2008; geometry and habitat determination in extinct and extant turtles Markle et al., 2018). Thus, Jackson’s (1988) study on musk (Reptilia: Testudinata). Paleobiology, 37: 547–56 turtles was a simplification of size selection of rock crevice Bonnet X., Delmas V., El-Mouden H., Slimani T., Sterijovski B., in a bottom-walking species. Unlike musk turtles, many Kuchling G. 2010. Is sexual body shape dimorphism consistent in aquatic and terrestrial chelonians? Zoology, 113: 213–220 evidences (Ly et al., 2013; Xiao et al., 2017), including this study, Bustard H. R. 1969. The population ecology of the gekkonid lizard have demonstrated that the Keeled box turtle prefers to take (Gehyra variegata (Dumeril and Bibron)) in exploited forests in refuge in rock crevices shelters in the field. Therefore, our study northern New South Wales. J Anim, 38: 35–51 strongly implies that shell morphology plays an important role Claude J., Paradis E., Tong H., Auffray J. C. 2003. A geometric in a crevice-dwelling turtle’s decision to select a shelter. morphometric assessment of the effects of environment and In addition, the Keeled box turtle’s carapace has a serrated cladogenesis on the evolution of the turtle shell. Biol J Linn Soc, 79: 485–501 posterior edge (Xiao et al., 2017) and we found that they most Cooper W. E., Van W. J., Mouton P., Al-Johany A. M., Lemos-Espinal often take refuge inside rock crevices with their posterior J. A., Paulissen M. A., Flowers M. 2000. Lizard antipredatory end of the carapace facing out (head first) in the field. Such behaviors preventing extraction from crevices. Herpetologica, a behavior might also help deter predators from attempting 394–401 to remove turtles from rock crevices. The Black-breasted leaf Cox C. L., Logan M. L., Bryan O., Kaur D., Leung E., McCormack J., turtle (Geoemyda spengleri) also has a carapace with prominent McGinn J., Miller L., Robinson C., Salem J., Scheid J., Warzinski T., Chung A. 2018. Do ring-necked snakes choose retreat sites serrated edges and prefers taking refuge inside rock crevices based upon thermal preferences? J Therm Biol, 71: 232–236 in the field, but whether it also adopts this kind of behavior to Croak B. M., Pike D. A., Webb J. K., Shine R. 2008. Three- defend against predators requires further research. dimensional crevice structure affects retreat site selection by In summary, we found that Keeled box turtles prefer reptiles. Anim Behav, 76(6): 1875–1884 crevices that have a similar height to their shells, and that Ireland L. C., Gans C. 1972. The adaptive significance of the flexible shell of the tortoise, . Anim Behav, 20: 778– turtles most frequently take refuge in the deepest parts of rock Malacochersus tornieri 781 crevices so that their carapaces are in close contact with the Jackson J. F. 1988. Crevice occupation by musk turtles: taxonomic ceilings of the crevices. There also seems to be a tradeoff in distribution and crevice attributes. Anim Behav, 36: 793–801 crevice width, in which Keeled box turtles select crevices that Loehr V. T., Henen B. T., Hofmeyr M. D. 2006. Shell characteristics are wide enough to move around, but not too wide to allow the and sexual dimorphism in the Namaqualand speckled padloper, predators to get in. We conclude that the tendency for Keeled Homopus signatus signatus: original article. Afr J Herpetol, 55: 1–11 Ly T., Hoang H. D., Stuart B. L. 2013. Occurrence of the endangered box turtles to select crevices with a similar height as their Keeled Box Turtle, Cuora mouhotii, in southern Vietnam. carapace, and to enter the crevices head first contributes to their Chelonian Conserv Bi, 12: 184–187 success in avoiding predators. It is likely that the compressed Markle C. E., Rutledge J. M., Chow-Fraser P. 2018. Factors affecting carapace in Keeled box turtles and the serrated posterior edge coastal wetland occupancy for eastern musk turtles (Sternotherus of their carapace are adaptations to life in rock crevices. This odoratus ) in georgian bay, lake huron. Herpetologica, 74: 236– seems even more evident when considered that the Keeled box 244 Malonza P. K. 2003. Ecology and distribution of the pancake turtle is sympatric with the flower back box turtle, which does tortoise, Malacochersus tornieri in Kenya. J East Afr Nat Hist, 92: not have similar shell characteristics or behavior (it does not use 81–96 rock crevices). Milne T., Bull C. M. 2000. Burrow choice by individuals of different sizes in the endangered pygmy blue tongue lizard Tiliqua Acknowledgements We are grateful to the Diaoluoshan adelaidensis. Biol Conserv, 95: 295–301 National Nature Reserve for access to the field site and Nasengbate., Zhang N., Jia F.Q. 2013. Habitat characteristic of tortoise turtle cave in nature reserve in Xinjiang. providing convenience for our works. Funding was provided Testudo horsfieldi J Yili Normal Univ: Nat Sci Ed, 7: 39–42 (In Chinese) by the National Natural Science Foundation of China Pike D. A., Croak B. M., Webb J. K., Shine R. 2010. Subtle but easily (No. 31772486) and the Hainan Provincial Natural Science reversible anthropogenic disturbance seriously degrades habitat Foundation of China (No. 319MS047). quality for rock dwelling reptiles. Anim Conserv, 13: 411–418 Fanrong XIAO et al. Turtle Shell Morphology Predict Crevice Selection No. 4 349

Price M. V. 1978. The role of microhabitat in structuring desert Wang J. C., Gong S. P., Shi H. T., Liu Y. X., Zhao E. M. 2011. rodent communities. Ecol, 59: 910–921 Reproduction and nesting of the endangered Keeled box turtle Pringle R. M., Webb J. K., Shine R. 2003. Canopy structure (Cuora mouhotii) on Hainan Island, China. Chelonian Conserv Bi, microclimate and habitat selection by a nocturnal snake, 10: 159-164 Hoplocephalus bungaroides. Ecol, 84: 2668–2679 Williams R., Pernetta A. P., Horrocks J. A. 2016. Outcompeted by Schlesinger C. A., Shine R. 1994. Selection of diurnal retreat sites by an invader? Interference and exploitative competition between the nocturnal gekkonid lizard . Herpetologica, Oedura lesueurii tropical house gecko (Hemidactylus mabouia) and Barbados 156–163 leaf‐toed gecko (Phyllodactylus pulcher) for diurnal refuges in Shi H. T., Xu S. K., Liu Z. X., Jia C. X., Luo Z. T. 1995. The activity anthropogenic coastal habitats. Integr Zool, 11: 229–238 rhythm of the Central Asian tortoise. Chin J Zool, 30: 40–45 (In Xiao F. R., Wang J. C., Shi H. T., Long Z. Z., Lin L., Wang W. 2017. Chinese) Ecomorphological correlates of microhabitat selection in two Smith W. H., Slemp S. L., Stanley C. D., Blackburn M. N., Wayland J. 2017. Rock crevice morphology and forest contexts drive sympatric Asian box turtle species (Geoemydidae: Cuora). Can J microhabitat preferences in the Green Salamander (Aneides Zool, 95: 753–758 aeneus). Can J Zool, 95: 353–358 Zhang H., Dou H., Zhai H., Wu M. 2006. Characteristics of dens in Thompson G., Withers P. 2005. The relationship between size- spring of three species of cands. Acta Ecologica Sin, 12: 3980– free body shape and choice of retreat for Western Australian 3988 Ctenophorus (Agamidae) dragon lizards. Amphibia-Reptilia, 26: Zhao E. M., Adler K. 1993. Herpetology of China. Society for the 65–72 Study of Amphibians and Reptiles, Athens, Oxford

Handling Editor: Heling Zhao

How to cite this article: Xiao F. R., Hong Z., Wang J. C., Butterfield T., Shi H. T. The Relationship between Shell Morphology and Crevice Size Affecting Retreat Selection of the Keeled Box Turtle (Cuora mouhotii). Asian Herpetol Res, 2020, 11(4): 342– 349. DOI: 10.16373/j.cnki.ahr.200029