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Ecomorphological correlates of microhabitat selection in

two sympatric Asian box turtle species (Geoemydidae: Cuora)

Journal: Canadian Journal of Zoology

Manuscript ID cjz-2016-0218.R2

Manuscript Type: Article

Date Submitted by the Author: 23-May-2017

Complete List of Authors: Xiao, Fanrong; Hainan Normal University, College of Life Sciences

Wang, Jichao; Hainan Normal University, College of Life Sciences Shi, Haitao; Hainan Normal University, College of Life Sciences Long, Zaizhong; Hainan Normal University, College of Life Sciences Lin, Liu; Hainan Normal University, College of Life Sciences Wang, Wei; Hainan Normal University, College of Life Sciences

Keyword: keeled box turtle, Cuora mouhotii, Indochinese box turtle, Cuora galbinifrons, leaf litter, microhabitat, rock crevice

https://mc06.manuscriptcentral.com/cjz-pubs

Canadian Journal of Zoology

Draft

Ecomorphological correlates of microhabitat selection in two

sympatric Asian box turtle species (Geoemydidae: Cuora)

Fanrong Xiao, Jichao Wang, Haitao Shi, Zaizhong Long, Liu Lin, and Wei Wang

F. Xiao, J. Wang, H. Shi, Z. Long, L. Lin, W. Wang:

College of Life Sciences, Hainan Normal University, Haikou 571158, China

H. Shi:

Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China

(e-mail: haitao-shi@ 263. net)

Corresponding authors: H. Shi, Hainan Normal University, Longkun south road no.

99, Haikou, Hainan province, China. Tel: 0898-65803298 (e-mail: haitao-shi@ 263.

net)

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Ecomorphological correlates of microhabitat selection in two

sympatric Asian box turtle species (Geoemydidae: Cuora)

F. Xiao, J. Wang, H. Shi, Z. Long, L. Lin, and W. Wang

Abstract: Closely related species that co-occur in homogeneous environments often

possess differing morphologies, which can result in niche divergence that minimizes

interspecific competition. In the present study, we examined the relationship between

the ecomorphological characteristics and microhabitat selection of two Asian box

turtle species, the keeled box turtle Cuora mouhotii (Gray, 1862) and Indochinese box

turtle C. galbinifrons (Bourret, 1939), which have sympatric distributions in the

rainforest of Hainan, China. We found that C. mouhotii had a relatively flat shell and

preferred microhabitats with rock crevices and steep slopes in the field, whereas C.

galbinifrons had a domed shell and was restricted to microhabitats of deciduous

leaves under bamboo growing on gentle slopes. We conclude that morphological

divergence allows the two Cuora spp. to use different microhabitats and, thereby, to

successfully co-occur.

Key words: keeled box turtle, Cuora mouhotii, Indochinese box turtle, Cuora

galbinifrons, leaf litter, microhabitat, rock crevice.

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Introduction

One of the most important objectives of ecomorphology is to determine the

underlying mechanisms of species co-occurrence in relation to their morphological

and ecological characteristics, both in the present and over evolutionary time (Motta

and Kotrschal 1992; Vanhooydonck et al. 2000). Generally, co-occurring species

either possess similar morphologies, owing to convergent evolution from adaptation

to the same habitat (Grant 1972), or divergent morphologies that result in niche

divergence and minimize interspecific competition (Hutchinson 1959; Brown and

Bowers 1985). In particular, closely related species that co-occur in homogeneous

environments should be morphologically distinct to partition limited resources, such

as microhabitats, and, thus, to reduce competitive interactions and, ultimately, achieve

co-occurrence. Numerous studies on vertebrate taxa have shown that ecomorphology

correlates with habitat selection among sympatric species (e.g., mammals: Davies et

al. 2007; birds: Guillemain 2002; reptiles: Pounds 1988; Lindeman 2000;

Vanhooydonck et al. 2000; Higham and Russell 2010; and fish: Robinson and Wilson

1994). However, such studies have typically correlated morphological features with

habitat classes, and only a few have quantified ecological characteristics, such as

microhabitat (Lindeman 2000; Vanhooydonck et al. 2000).

Both the keeled box turtle (C. mouhotii Gray, 1862; formerly Pyxidea mouhotii)

and Indochinese box turtle (C. galbinifrons Bourret, 1939) are distributed in south

China, including Hainan Province (Zhao and Adler 1993). C. mouhotii is typically

found in moist evergreen forests at low altitude (Wang et al. 2011a; Wangyal et al.

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2012; Struijk et al. 2016), whereas C. galbinifrons is found in similar forests but at

high altitude (Wang et al. 2011b). Previous studies have reported the occurrence of

natural hybrids in Hainan Province (Shi et al. 2005), which implies that, in some areas,

the distributions of the two species overlap, and the species have since been reported

to co-occur at 700–914 m in the Hainan Diaoluoshan Natural Reserve by Wang et al.

(2011a,b).

Interestingly, the morphology of C. mouhotii is extremely divergent from its

sympatric species, C. galbinifrons, as well as from all other species in the genus. For

example, C. mouhotii possesses a relatively flat carapace for a member of Cuora, with

a flattened top, whereas C. galbinifrons has a highly domed carapace. In general,

carapace shape is correlated with the habitat preference of turtles: aquatic turtles have

flattened carapaces, whereas terrestrial turtles have highly domed carapaces, and

semiaquatic turtles have carapaces with intermediate morphology (Romer 1967;

Claude et al. 2003; Bonnet et al. 2010; Benson et al. 2011). However, previous studies

about the microhabitat preference of flat-topped turtle species remain scarce, such as

C. mouhotii. Additionally, although C. galbinifrons has been considered to exhibit a

semiaquatic habit (Ernst and Barbour 1989), Wang (2007) and Wang (2008) tracked

nine individuals in Diaoluoshan Natural Reserve for two years, using radio telemetry,

and found that the species never entered the water. Therefore, the ecological function

of the two species’ divergent morphologies has been unclear.

Recently, one individual of C. mouhotii was found in a rock crevice at the Deo

Ca Protected Forest, Phu Yen Province, Vietnam (Ly et al. 2013). In contrast, C.

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galbinifrons is more frequently observed in microhabitats of deciduous leaves under

dense bamboo (Wang et al. 2011b). Therefore, in the present study, we quantified the

microhabitat use of co-occurring C. mouhotii and C. galbinifrons at Diaoluoshan

Natural Reserve. We hypothesized that the two species would occupy different

microhabitats, owing to their divergent shell morphology.

Materials and methods

Ethics statement

This study was approved by the Animal Research Ethics Committee of Hainan

Provincial Education Centre for Ecology and Environment, Hainan Normal

University (HNECEE-2014-002), and was carried out in strict accordance with the

institutional guidelines. Fieldwork was carried out with permission from the

Diaoluoshan Forest Bureau. No turtles were sacrificed for this study or incurred injury

or death while in the traps.

Microhabitat selection

We studied the microhabitat selection of C. mouhotii and C. galbinifrons at the

Diaoluoshan Natural Reserve in Hainan Province, China (18°43′53″N, 109°52′10″E)

from April 2015 to February 2016. The field site was located in a rainforest between

860 and 914 m in altitude, where the average highest temperature is 28 °C in July, the

average lowest temperature is 15.4 °C in January, and the annual rainfall ranges from

1870 to 2760 mm.

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The turtles were captured in traps baited with salty fish or rancid pork skin;

thereafter, a radio-tracking transmitter (RI-2B, 216.000–216.999 MHz; Holohil

Systems, Ltd., Caro Ontario, Canada) was fitted to the last costal scute of each turtle.

The size (diameter × height = 21 × 8 mm), mass (6 g), and location of the transmitters

would not have prevented turtles from using any of the microhabitats. Then the turtles

were released at the site of capture. The turtles were tracked daily from 09:00 to 16:00,

using a handheld receiver (TRX-1000S, 216.000–216.999 MHz; Wildlife Materials

International, Inc., Murphysboro, Illinois, USA) with a three-element folding antenna

(Wildlife Materials, Inc.), and the locations were recorded using a handheld Magellan

Triton 400 Global Positioning System (Magellan Navigation, Inc., Santa Clara, USA).

Radio-tracked turtles were tracked for an average of 164 days. All radio-tracking

transmitters were carefully removed from the turtles’ shells when the tracking study

was complete.

We hypothesized that the locations at which the turtles remained for >3 d

indicated preferred microhabitats and quantified 14 microhabitat characteristics within

two different-sized quadrats (10 × 10 m and 1 × 1 m) at each preferred site. In the

large quadrats, we quantified (1) slope gradient (°), (2) slope position (1 = upper slope,

2 = middle slope, 3 = lower slope; slope position refers to the location of slope

occupied by turtle in the mountain, which was classified as upper slope, middle slope

or lower slope when the turtle occur near peak, middle or low position of the

mountain, respectively), (3) canopy cover (%), (4) number of fallen logs, (5) number

of bamboo clumps, (6) number of tree holes, and (7) number of rock crevices; and in

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the small quadrats, we quantified (8) bamboo density (plants/m2), (9) herbage height

(cm), (10) herbage density (plants/m2), (11) deciduous leaf cover (%), (12) deciduous

leaf thickness (cm), (13) stone cover (%), and (14) type of concealment (1 = rock

crevice, 2 = tree hole, 3 = fallen log, 4 = grass, 5 = bamboo clump, 6 = deciduous

leaves, 7 = bare ground). In total, we collected data from 44 preferred sites from seven

C. mouhotii individuals and from 27 preferred sites from five C. galbinifrons

individuals.

Chi-squared tests (SPSS 16.0; SPSS, Inc., Chicago, IL, USA; same below) were

used to assess whether the two species differed in their preference of slope position

and type of concealment. The Kolmogorov-Smirnov test was performed to test the

normality of the 12 numeric microhabitat variables. One-way analysis of variance

(ANOVA) was subsequently used to test whether the two species differed in slope

gradient, herbage height, and deciduous leaf cover, and the Mann-Whitney U test was

used to determine whether the two species differed in any the nine remaining

microhabitat variables. Furthermore, discriminant function analysis (DFA) was

performed to assess the differences in the 12 numeric microhabitat variables between

the two species. The stepwise method of DFA was performed to determine the best

variables significantly separating the two species.

In addition, we measured the slope gradient at stopover sites at which the turtles

remained for <1 d, using a clinometer. Whether the two species differed in slope

gradient was examined using one-way ANOVA.

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Morphological measurements

Morphological measurements were taken from all the experimental individuals

(n = 9 for C. mouhotii, n = 8 for C. galbinifrons), as well as from other individuals

that were more recently encountered in the field (nine individuals for C. mouhotii and

five individuals for C. galbinifrons), using a Vernier caliper (accuracy to 0.02 mm).

For each individual, we measured carapace length, carapace width (measured at the

sixth marginal scute), and carapace height (measured at the sixth marginal scute). In

addition, we also calculated the ratio of carapace height to width (R) as a measure of

shell contour (Domokos and Várkonyi 2008).

After the normality and homogeneity of variance were tested for all

morphological measurements, one-way ANOVA was used to test whether the two

species differed in carapace length, and to remove the effect of body size, one-way

analysis of covariance (ANCOVA; carapace length as the covariate) was performed to

test whether the two species differed in any of the other morphological variables.

Results

Microhabitat selection

No individuals of either C. mouhotii or C. galbinifrons were found in the water

during the field study. Among the 14 microhabitat variables, slope gradient, number

of rock crevices, deciduous leaf cover, deciduous leaf thickness, stone cover (Table 1),

and type of concealment (χ2 = 69.69, df = 6, P < 0.0001) significantly differed

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between the two species . This finding indicates that C. mouhotii was more commonly

observed on rocky substrates and steep slopes (Table 1) and typically selected rock

crevices for concealment (56.82%; Fig. 1B), whereas C. galbinifrons was usually

observed in deciduous leaves on gentle slopes (Table 1) and selected deciduous leaves

for concealment (93.93%; Fig. 1C).

The stepwise DFA indicated that three variables were selected which

significantly discriminate C. mouhotii and C. galbinifrons (stone cover, slope gradient,

and bamboo density; Table 2), and the efficiency of the analysis was high (62 of 71

quadrats - 87.3% were correctly classified). The distribution of the quadrats on the

DFA axis showed that the microhabitats selected by C. mouhotii were mostly distinct

from those selected by C. galbinifrons, and only a small overlap between the two

species (Fig. 2). For instance, both C. mouhotii and C. galbinifrons selected the same

terrestrial habitat with high-canopy cover (Table 1; Fig. 1A).

In addition, the slope gradients of the stopover sites of the two species differed

significantly (one-way ANOVA; F1, 324 = 128.214; P < 0.0001), with C. mouhotii

(mean ± SD: 30.3 ± 8.7°, range: 5 – 60°) occurring on steeper slopes than C.

galbinifrons (22.3 ± 7.5°, 5 – 40). This result was in accordance with the slope

gradients from the preferred sites.

Morphological measurements

The carapace length of the two species did not differ significantly (one-way

ANOVA; Table 3). However, one-way ANCOVA, with carapace length as the

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covariate, indicated that the carapace height and ratio of carapace height to width of

the two species all differed significantly, whereas the carapace width of the two

species was similar (Table 3). These findings indicated that C. mouhotii had a

relatively flat shell, whereas C. galbinifrons had a highly domed one. In addition, the

plastron hinge of C. mouhotii only allowed the shell to close partially, whereas that of

C. galbinifrons allowed the shell to close completely; and C. mouhotii also possessed

a carapace with serrated posterior edges and a flattened top, whereas C. galbinifrons

possessed a carapace with smooth edges.

Discussion

In agreement with previous studies, we found that both adult C. mouhotii and C.

galbinifrons were terrestrial species and selected the same high-canopy cover habitat

(Wang 2007; Lian 2009); however, we also observed that the microhabitats of the two

species were significantly different. Notably, C. mouhotii individuals were mostly

observed in areas with greater stone cover and often selected rock crevices for

concealment, where they hid for up to 20 d, whereas C. galbinifrons individuals were

mostly observed in deciduous leaf litter under bamboos, where they often hid for long

periods, as well. In addition, C. mouhotii also occupied microhabitats with slopes that

were much steeper than those of the microhabitats occupied by C. galbinifrons. This

suggests that the two species co-occur by occupying different niches.

Understanding the relationship between microhabitat selection and morphology

is critical for understanding ecomorphological adaption (Vanhooydonck et al. 2000;

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Rivera 2008; Rivera et al. 2014). In the present study, we found that body size

(carapace length) did not differ between C. mouhotii and C. galbinifrons, but the shell

of C. mouhotii was significantly more flat than that of C. galbinifrons. Our

microhabitat experiment confirmed that C. mouhotii prefers and selects microhabitats

with rock crevices, and since flattened bodies often allow animals to fit into narrow

crevices (Miles 1994) and because previous studies have reported that terrestrial

turtles with flat carapaces, such as the African pancake tortoise (Malacochersus

tornieri Siebenrock, 1903), are adapted to lifestyles in rocky crevices (Ireland and

Gans 1972; Malonza 2003), we believe that the relatively flat shell of C. mouhotii is

an adaptation for using microhabitats with rock crevices. In addition to possessing a

flatter shell than C. galbinifrons, the flat-topped carapace of C. mouhotii was

important in its adaptation to the rock crevice microhabitats, as in several species of

the genus Homopus Duméril and Bibron, 1835 (Ernst and Barbour 1989; Bonin et al.

2006).

We also observed that C. mouhotii has a posteriorly serrated carapace, which

might help prevent the turtles from being dragged out of rocky crevice by predators.

In addition, C. mouhotii occupied microhabitats with slopes that were much steeper

than those of the microhabitats occupied by C. galbinifrons. This difference may be

correlated with the shell shapes of the two species. Since flat shells impart a lower

center of gravity (Domokos and Várkonyi 2008) and thus increase stability on steeper

surfaces, the relatively flat shell of C. mouhotii could also be an adaptation for

climbing on smooth rocks and inclined substrates; however, this morphofunctional

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hypothesis should be confirmed by further investigation.

In contrast to the relatively flat shell of C. mouhotii, the highly domed shell of C.

galbinifrons is typical of terrestrial turtles, and both the present and previous studies

(Wang 2007) have reported that C. galbinifrons inhabits terrestrial habitats. Indeed,

the species is well adapted to terrestrial environments, since its shell can tolerate

much stronger mechanical forces, such as those from terrestrial predators (Greene

1988; Stayton 2011); and although the highly domed shell may also restrict the

species to hiding in soft leaves and to microhabitats with relatively gentle slopes, the

species possesses several alternative defensive features. For example, C. galbinifrons

also has a single transverse hinge across the middle of its plastron that allows

complete retraction and protection of its extremities from predators (Pritchard 2008),

and the color and pattern of the species’ carapace is similar to that of deciduous leaves,

which may function to reduce predator detection via camouflage (Fig. 1C; Stevens

and Merilaita 2009; Xiao et al. 2016). Moreover, the smooth marginal scutes of C.

galbinifrons allow it to burrow deeper than C. mouhotii under deciduous leaves.

Notably, we found that C. galbinifrons was a leaf-dwelling species. However,

many terrestrial species that hide under leaf litter, such as the black-breasted leaf

turtle (Geoemyda spengleri Gmelin, 1789; R = 0.54; Benson et al. 2011), forest cane

turtle (Vijayachelys silvatica Henderson, 1912; R = 0.51; Whitaker and Vijaya 2009),

and spiny turtle (Heosemys spinosa Gray, 1831; R = 0.53; Spinks et al. 2012), have

flat shells. Therefore, it is actually quite surprising that the highly domed C.

galbinifrons also uses this microhabitat. One possible way in which C. galbinifrons

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can mitigate the disadvantage of its tall shell is that the coloration of C. galbinifrons is

somewhat similar to that of other leaf-dwelling species, as well as to that of leaves

(i.e., camouflage). It is also possible that the leaf litter in the habitat of C. galbinifrons

affords high cover and is thick enough to hide its highly domed shell.

Intriguingly, other Cuora spp. possess different shell morphologies and occupy

diverse habitats. For example, both C. galbinifrons (R = 0.70) and the

yellow-margined box turtle (C. flavomarginata Gray, 1863; R = 0.65; Benson et al.

2011) have highly domed shells and occupy terrestrial habitats, i.e., evergreen forests

(Lue and Chen 1999), whereas the Malayan box turtle (C. amboinensis Daudin, 1802),

which also has a relatively domed shell (R = 0.61; Benson et al. 2011), is aquatic

(Ernst 1989; Joyce and Gauthier 2004). Similarly, C. mouhotii, which has a relatively

flat shell (R = 0.58), occupies terrestrial environments with rocky crevices; whereas,

the Chinese three-striped box turtle (C. trifasciata Bell, 1825), golden-headed box

turtle (C. aurocapitata Luo and Zong, 1988), and Pan’s box turtle (C. pani Song,

1984), which are morphologically similar and possess very flat and streamlined shells

(R = 0.48, 0.45, and 0.47, respectively; Zhang et al. 1998) that are typical of aquatic

species (R under approx. 0.6; Domokos and Várkonyi 2008), are completely aquatic

(Zhang et al. 1998; Cheung 2007). Phylogenetic analysis will be needed to elucidate

the patterns of shell evolution and habitat diversification of Cuora spp. in the future.

In summary, we found that the two species occupy different niches. C. mouhotii

prefers microhabitats with rock crevices and was more commonly observed on slopes

with steep inclines in the field, for which its flattened shell is well suited, whereas the

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dome-shelled of C. galbinifrons restricts the species to hiding in deciduous leaves

with bamboos and to microhabitats with relatively gentle slopes. Therefore, we

conclude that morphological divergence allows the two Cuora spp. to partition the

available microhabitats, and, thereby, to successfully co-occur.

Acknowledgements

We are grateful to F. Kong, Z. Zhao, and Q. Wang for assistance with field work.

We are also grateful to the editors, R.M. Brigham and H. Guderley, and an anonymous

reviewer for comments that improved this article. This study was supported by the

National Natural Science Foundation of China (nos. 31260518 to J.W. and 31372228

to H.S.).

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Table 1 Characteristics of microhabitat used by C. mouhotii and C. galbinifrons. Values indicate

the mean ± SD measurements for each species, as well as the statistical significance of their

difference.

Quadrat size C. mouhotii C. galbinifrons

one-way ANOVA

or Mann- Whitney U test

Slope gradient (°) 10 × 10 m 33.55 ± 8.5 26.81 ± 6.25 F = 12.679, P = 0.001

Canopy (%) 10 × 10 m 75.45 ± 10.39 80.19 ± 6.12 Z = -1.74, P = 0.082

No. fallen logs 10 × 10 m 2.84 ± 1.78 2.85 ± 1.23 Z =-0.491, P = 0.623

No. bamboo clumps 10 × 10 m 4.95 ± 2.47 4.00 ± 2.62 Z = -1.791, P = 0.073

No. tree holes 10 × 10 m 1.25 ± 0.87 0.89 ± 0.75 Z =-1.759, P = 0.079

No. rock crevices 10 × 10 m 5.45 ± 4.81 0.19 ± 0.48 Z = -5.846, P < 0.0001

Bamboo density (plants/m2) 1 × 1 m 4.43 ± 4.37 3.85 ± 5.19 Z =-1.007, P = 0.314

Herbage height (cm) 1 × 1 m 41.01 ± 23.59 38.70 ± 16.68 F = 0.203, P = 0.654

Herbage density (plants/m2) 1 × 1 m 4.41 ± 2.49 4.33 ± 2.97 Z = -0.552, P = 0.581

Decid. leaf cover (%) 1 × 1 m 48.07 ± 20.78 80.93 ± 14.08 F = 52.566, P < 0.0001

Decid. leaf thickness (cm) 1 × 1 m 6.18 ± 3.38 17.56 ± 24.88 Z = -5.779, P < 0.0001

Stone cover (%) 1 × 1 m 58.48 ± 35.21 2.78 ± 2.25 Z = -6.185, P < 0.0001

Table 2 Stepwise discriminant analysis of microhabitat variables of two Cuora spp.

Variable No. Variables Discriminant coefficients Wilk’s λ F P

1 Stone cover 0.962 0.51 66.29 < 0.0001

2 Slope gradient 0.424 0.463 39.429 < 0.0001

3 Bamboo density 0.36 0.432 29.382 < 0.0001

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Table 3 Difference in the morphology of two Cuora spp. Values indicate the mean ± SD

measurements for each species, as well as the statistical significance of their difference (one-way

ANOVA for carapace length and one-way ANCOVA for the remaining parameters, with carapace

length as the covariate).

C. mouhotii C. galbinifrons F P

Sample size 18 13

Carapace length (mm) 162.91 ± 18.47 168.77 ± 8.61 1.12 0.298

Carapace width (mm) 114.24 ± 7.82 113.98 ± 4.73 1.77 0.194

Carapace height (mm) 65.81 ± 4.19 79.26 ± 3.67 101.53 < 0.0001

Carapace height / width 0.58 ± 0.03 0.70 ± 0.03 113.65 < 0.0001

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Figure Legends

Fig. 1 The shared macrohabitat and divergent preferred microhabitats of two sympatric Cuora spp.

in Hainan, China. A, the high-canopy cover habitat shared by both C. mouhotii and C.

galbinifrons. B, the preferred microhabitat of C. mouhotii (rock crevices), with a turtle visible in

the crevice (arrow). C, the preferred microhabitat of C. galbinifrons (deciduous leave litter under

bamboo clumps), with a turtle visible under the leaf litter (arrow). All photos were taken by F.

Xiao.

Fig. 2 Distribution of the quadrats on the DFA axis.

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Fig. 1 The shared macrohabitat and divergent preferred microhabitats of two sympatric Cuora spp. in Hainan, China.

382x821mm (300 x 300 DPI)

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Fig. 2 Distribution of the quadrats on the DFA axis

105x75mm (300 x 300 DPI)

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draft - university of toronto t-spaceshell contour (domokos and várkonyi 2008). after the normality...

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