NORTH-WESTERN JOURNAL OF ZOOLOGY International scientific research journal of zoology and animal ecology of the Herpetological Club - Oradea Univeristy of Oradea, Faculty of Sciences, Department of Biology Univeristatii str. No.1, Oradea – 410087, Romania Publisher: University of Oradea Publishing House Contact e-mail: [email protected], [email protected] NORTH – WESTERN JOURNAL OF ZOOLOGY (International journal of zoology and animal ecology) ACCEPTED PAPER - Online until proofing - Authors: Carina Carneiro De Melo MOURA; Geraldo Jorge Barbosa De MOURA; Leonardo Da Silva CHAVES; Sérgio Luíz Da Silva MUNIZ; Eliana Sofia Farjardo VEGA; Valter Eduardo JÚNIOR Title: Demography, sex ratio, and sexual dimorphism of Testudines in Araripe Bioregion, Ceará, Northeastern Brazil Journal: North-Western Journal of Zoology Article number: 141514 Status: awaiting proofing How to cite: Moura C.C.D.M., Moura G.J.B.D., Chaves L.D.S., Muniz S.L.D.S., Vega E.S.F., Júnior V.E. (2015): Demography, sex ratio, and sexual dimorphism of Testudines in Araripe Bioregion, Ceará, Northeastern Brazil. North-Western Journal of Zoology 11: art.141514 Date published: <2014-12-21> Citation as online first paper: North-western Journal of Zoology 11: art.141514 Demography, sex ratio, and sexual dimorphism of Testudines in Araripe Bioregion, Ceará, Northeastern Brazil N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y CARINA CARNEIRO DE MELO MOURA¹, GERALDO JORGE BARBOSA DE MOURA1, LEONARDO DA SILVA CHAVES¹, SÉRGIO LUÍZ DA SILVA MUNIZ¹, ELIANA SOFIA FARJARDO VEGA¹ & VALTER EDUARDO JÚNIOR² ¹ Universidade Federal Rural de Pernambuco, Department of Biology, Laboratory Herpetology and Paleoherpetology. UFRPE . ²Universidade Federal de Pernambuco, Department of Statistics. UFPE. Corresponding author: [email protected] Citation as online first paper: North-western Journal of Zoology 11: art.141514 Demography of Testudines in North East Brazil Abstract N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y In spite of the increasing number of demographic studies about freshwater turtles, very few have been focused on populations in semi-arid regions. Therefore, the aim of this study is to estimate the demographic parameters of testudine species in an area of Caatinga, North East Brazil, while focusing on the following objectives: (i) To estimate the size of the populations; (ii) to assess the sex ratio and sexual dimorphism; (iii) to correlate biological parameters with temperature and rainfall data. Sampling was carried out over 12 months, from August 2011 to July 2012, for a total of five days per month. Hoop traps and chicken bait were used for sampling. In total, 63 specimens from three different species were captured: 44 specimens of P. geoffroanus; nine specimens of Kinosternon scorpioides and 10 specimens of Mesoclemmys tuberculata. The population densities were as follows: approximately 9 turtles/ha to P. geoffroanus, 2 turtles/ha to M. tuberculata and 2 turtles/ha to K. scorpioides. 50% of recorded captures occurred in February and March 2012. P. geoffroanus exhibited a sex ratio of 1.53(♀):1(♂) (P=0.223), whereas the ratio for K. scorpioides was 1(♀):1.25(♂). Sexual dimorphism index, calculated using the mean number of male and female carapaces, was 1.06 (deviated for females) for P. geoffroanus and 1.04 (deviated for males) for K. scopioides. It was not possible to deduce the sexual dimorphism or the sex ratio for M. tuberculata as only female specimens were captured. The data reported herein will be useful in the composition of management and conservation plans for testudine species found in areas of Caatinga, as well as for further studies in this morphoclimatic domain, which minimally studied in Brazil. Key Words- Phrynops geoffroanus; Kinosternon scorpioides; Mesoclemmys tuberculata; Chelidae; Kinosternidae; Population structure. Citation as online first paper: North-western Journal of Zoology 11: art.141514 INTRODUCTION The Caatinga morphoclimatic domain is unique in that it is only found within the boundaries of Brazil (Andrade-Lima 1981, Vitt & Vangilder 1983). This domain is known for N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y high temperatures, low relative humidity, a hot and semi-arid climate (Velloso et al. 2002), which is typically seasonal, with a long dry season and short periods of variable rainfall (Reis 1976, Leal et al. 2003). The phytophysiognomic peculiarities found in flora, climate and geological characteristics of this biome sustain different microhabitats and consequently, exhibit rich flora and fauna (Rodrigues 2003). Testudines are part of the group of ectothermic Sauropsida that typically exhibit a long lifespan, delayed sexual maturity, and slow growth (Rueda-Almonacid et al. 2007). These characteristics have been associated with a low rate of individual substitution among populations, making this group more susceptible to anthropogenic threats and environmental weathering (Hickman et al. 2004, Rodrigues 2005, Moura et al. 2012). Demographic parameters are essential tools to evaluate the real status of conservation of testudine communities (Gibbons & Greene 1990, Smith et al. 2006). Demographic studies about neotropical freshwater turtles are limited (Souza 2004, Martins & Souza 2008), although a necessity for a better understanding of the population dynamics (Gibbons 1970, Brito et al. 2009). Strong relation between population dynamics of testudines and climatic variation are common, resulting in a seasonal reproductive cycle (Souza 2004). The duration and level of biological activities such as foraging, thermal regulation and migration are determined by genetic interactions and environmental conditions (Molina 1992, Roe & Georges 2008, Ferreira-Júnior 2009). Some freshwater turtles shown more activity during warmer months, that promote thermoregulatory activities (Souza 1999, Souza 2004, Forero-Medina et al. 2012). However some other species, such as those belonging to the Chelidae family show estivation behavior during long dry periods (Mittermeier 1978, Vogt 2008, Forero-Medina et al. 2012, Forero-Medina et al. 2013). Migration has also been Citation as online first paper: North-western Journal of Zoology 11: art.141514 observed in neotropical freshwater turtles searching for favorable environments (Fraxe-Neto et al. 2011). These aspects directly influence the population density and sex ratio, they form a set that is responsible for variations in the population dynamics of the group (Gibbons 1990, N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y Brito et al. 2009, Fraxe-Neto et al. 2011). The aim of this study is to describe the demography of a testudine community in the area of Caatinga (Araripe Bioregion), while focusing on the following specific objectives: (i) to estimate the density of the populations; (ii) to assess the sex ratio and sexual dimorphism; (iii) to correlate the number of monthly captures of the species with the monthly accumulated rainfall and mean monthly temperature. MATERIAL AND METHODS Study Area The study was conducted in the Environmental Protection Area (EPA) of Chapada do Araripe (7°38’10.70’S and 41°55'10.58"W; DATUM: WGS84; 700 m a.s.l.; Fig. 1), located in Araripe Bioregion. Data was collected in the city of Jardim, southern Ceará, a region that is characterized as “bushy Caatinga” (Mittermeier et al. 1982). Collections were performed in a weir (7°39'10.76" S and 39°16'20.52" W) with an irregular shape and an approximate perimeter of 3 km and area of 5.2 ha. Bushes and a large quantity of aquatic vegetation are found in the border of the weir. Sampling Sampling was performed between August 2011 and July 2012. Traps were placed in the water body and opened for five days in each month. The study lasted 12 months, totaling 60 days of sampling and eight hours of daily work, with a total of 480 hours. Two convergence hoop traps were used, with mean measurements of 100 cm in length, 70 cm in diameter, containing dual funnel, and 50cm of the diameter of opening, 1 cm2 of mesh size and were baited with pieces of chicken inside a net of resistant plastic and fine Citation as online first paper: North-western Journal of Zoology 11: art.141514 mesh (5 mm) to avoid animals ingesting the content (Vogt 1980). Traps were inspected twice daily (once during the day and once at night). Each individual captured was marked with slits on the marginal shields (Cagle 1939). N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y The gender was determined based on secondary sexual characteristics: tail length and coloration, this second characteristic was only inspected in Kinosternidae (Gibbons & Lovich 1990). All females were submitted to gentle manual inspection in the abdominal area, beside hind paws, to verify the presence of abdominal shelled eggs. Individuals, whose sex was not clearly identifiable through these characteristics, were considered juveniles (Forero-Medina et al. 2011). The biometric data were recorded using a 1 mm precision caliper and a portable digital scale to the nearest 0.1 g. The following biometric measurements were recorded: Rectilinear carapace length (CL): the distance between the anterior margin of the nuchal shield or the first marginal shield to the posterior extremity of the supracaudal shield. Rectilinear carapace width (CW): the distance between the most external marginal shields. Rectilinear plastron length (PL): the distance between the center of the gular shields and the center of the anal shield. Rectilinear plastron width (PW): maximum linear width of plastron. Bridge length (BL): distance between the inguinal and axillary shields. Tail length (TL): the distance between the cloaca and the end of the tail. Carapace height (CH): the distance between the central vertebral shield and the abdominal shield (Fig. 2). Abiotic data (monthly rainfall and monthly average air temperature) were provided by the ICMBio Meteorology Center in Barbalha, Ceará. Data analysis The population densities were calculated using the total number of specimens collected divided by the total area of the weir. Associations between monthly captures and recaptures and monthly rainfall, monthly average air temperature, and solar intensity data were analyzed using Pearson’s correlation. Citation as online first paper: North-western Journal of Zoology 11: art.141514 Biometric measurements and weight were compared by ANCOVA in an attempt to assess differences in morphometric variables between males and a female, using the R programming language (R Development Core Team 2008), CL was considered the main variable and CW, N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y PL, PW, BL, TL, CH and weight as co-variables. Juveniles were excluded for this analysis. The sexual dimorphism index was calculated using the ratio of the biometric mean values for the carapace of males and females. The numerator was the mean of the gender with the highest value. Biometric proportions were based on the mean, median, mode, the maximal value of the carapace and plastron length, as well as the mean values for 3 and 5 of the largest adult individuals of both genders (Gibbons & Lovich 1990). The chi-squared test (Zar 1999) was used to test whether the sex ratios differed to 1:1, testing the hypothesis that there would be no significant difference between the number of males and females, using the program Prism 5. RESULTS Three species were recorded in the community of testudines, two of which belonged to the Chelidae family, Phrynops geoffroanus (Schweigger, 1812) and Mesoclemmys tuberculata (Luederwaldt, 1926), and one of which belonged to the Kinosternidae family, Kinosternon scorpioides (Linnaeus 1766). The sampling efficiency was 2.13 individuals captured per day. In total, 44 specimens of P. geoffroanus were marked. Twenty (45.45%) were female, thirteen (29.54%) were male and eleven (25%) were juveniles. Nine individuals of K. scorpioides were captured, of which six (66%) were male and three (33%) were female. Ten individuals of M. tuberculata were captured, all of them were female. During this period, 11 females of P. geoffroanus, as well as one male and one juvenile, were recaptured. One of the females was recaptured on four separate occasions. The minimal interval between captures was two days and the maximal interval between captures was 220 days. For K. scorpioides, six males and one female were recaptured. One male specimen was recaptured twice. The minimal interval between captures was 21 days and the maximal Citation as online first paper: North-western Journal of Zoology 11: art.141514 interval between captures was 103 days. Among the female M. tuberculata captured, four were recaptured, the shortest time between captures was five days and the longest time between captures was 44 days. N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y The months with the largest amount of captures were February and March, with approximately 50% of all recorded captures. These are the two months correlated with low precipitation, according to the meteorological history of the region (Fig. 3). In September, M. tuberculata (Fig. 4) and K. scorpioides (Fig. 5) were the most captured species. September was the month with the highest recorded rainfall and the lowest temperatures. The recaptures occurred between January and July for P. geoffroanus, with the largest number of recaptures recorded in March, which had low accumulated rainfall and high temperatures. For K. scorpioides, the recaptures occurred between September and December, which were the months with the most rainfall. M. tuberculata were recaptured in August, September and November. During these months, temperatures were low and high rainfall was recorded. Population density was approximately 9 turtles/ha for P. geoffroanus, 2 turtles/ha for M. tuberculata and 2 turtles/ha for K. scorpioides. Among females of P. geoffroanus, the size of the CL was bigger than in males, and the females weighed on average 17% more than males. The CL of M. tuberculata ranged from 148.9 to 220.03mm and the mean weight was 750 grams, however only females were caught. K. scorpioides is one of the smallest testudines, for this species, the male specimens exhibited CL values bigger than observed in females (Table 1). The sexual dimorphism index, calculated using the mean carapace values for males and females, was 1.06 (deviated for females) for P. geoffroanus and 1.04 (deviated for males) for K. scopioides. Based on the biometric data, it was possible to observe sexual dimorphism in P. geoffroanus, the species, with the exception of the tail, were larger for females than for males, the measurements significantly different between males and females (parameter sex, Citation as online first paper: North-western Journal of Zoology 11: art.141514 p=0.038, F= 4.8491). For K. scorpioides, sexual dimorphism was observed and all of the biometric variables were larger for males than for females, however the measurements were not significantly different (parameter sex, p=0.071, F=0.0711). Regarding the species M. N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y tuberculata, only females were identified, no sexual dimorphism was noticed (Table 2). P. geoffroanus exhibited a sex ratio of 1.53(♀):1(♂), (P=0.223, X²=0.046), with no significant difference between the number of males and females. K. scorpioides exhibited a sex ratio of 1(♀):1.25(♂) (p= 0.222, X²=0.225). It was not possible to confirm the sex ratio of M. tuberculata as only females were captured. This indicates that the sex ratio of this species may be deviated for females (Table 2). A number of reproductive aspects were noted during the sampling period. In the months of May and July, one female of P. geoffroanus was recorded with eggs, indicating that nesting begins in these months. At the end of March, a newly-hatched juvenile was captured measuring 39.9 mm and 28.2 mm for the CL and CW, respectively. Low accumulated rainfall was recorded in this period (Table 1). Temperature was not correlated with the number of monthly captures for any of the species in question. However, rainfall had a negative correlation to the number of monthly captures of P. geoffroanus (coefficient of correlation= -0.63, Number of captures=54 and p= 0.028). DISCUSSION The populations sizes recorded here are possibly influenced by the limiting conditions of the area, particularly in relation to the availability of food and the adverse climatic conditions: a period of intense drought periodically eliminates a large percentage of the population or induces migration to more suitable places (Aguiar & Buriti 2009). In comparison with other studies, we recorded low densities for testudines in semi-arid areas of Citation as online first paper: North-western Journal of Zoology 11: art.141514 Brazil, these values may be justified because we used the number of individuals captured during the sampling to determine the density, which can be underestimated. Areas that offer more resources have density of P. geoffroanus around 170-230 N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y turtles/ha, in urban rivers, these results are related with abundant biomass, absence of predation pressure and plenty of nesting areas (Souza & Abe 2000). The density of K. scorpioides populations varied from 77 to 254 turtles/ha in mangrove forests (Forero-Medina et al. 2007) and about 272 turtles/ha found in a conserved pond in Chiapas, Mexico (Iverson 1982), furthermore in areas with potential predators 14 to 21 turtles/ha were recorded (Moll 1990). According to Gibbons et al. (1983) and Moll (1990) the species of Kinosternidae migrate regularly in response to drought and other environmental factors. Previous work with Mesoclemmys estimated, at different seasons in the same stream, a density range from 16 turtles/ha to 170 turtle/ha (Forero-Medina et al. 2011). The species M. dahli in water reservoirs presented density of 500 turtles/ha (Rueda-Almonacid et al. 2007). Brito et al. (2009) estimated the density of M. vanderhaegei to be between 12 and 36 individuals to five streams. Species of Mesoclemmys genus bury on land during drought season and aestivates, these behaviors could influence the population structure evaluation that oscillate according to the abiotic conditions (Rueda-Almonacid et al. 2007, Forero-Medina et al. 2011). Population density is higher in localities with greater availability of food and reproductive sites (Souza & Abe 2000, Rueda-Almonacid et al. 2007, Forero-Medina et al. 2007). Furthermore, human pressure influences the dynamic of populations; in the semi-arid regions of Brazil, several species of reptiles are used for human consumption and medical proposes, the records include the species K. scorpioides, M. tuberculata and P. tuberosus (Alves et al. 2012). Sex ratio in wild populations normally diverge from 1:1 (Gibbons 1990, Forero- Medina et al. 2007, Brito et al., 2009). Among the regulating factors of sex ratio there are a difference of mortality between sexes, different ages of sexual maturity and the sexual determination for temperature (Gibbons 1990). According to Bury (1979), the sex ratio of Citation as online first paper: North-western Journal of Zoology 11: art.141514 testudine populations differs among species and oscillations often occur as a result of different collection techniques, behavioral differences between genders or incubation temperatures that influence the sexual determination of some turtles (Gibbons 1970, Vogt 1980, Fachin-Téran N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y et al. 2003). Due to the fact that the specimens are more active during reproductive season when they seek a receptive partner for copulation (Berry & Shine 1980, Famelli et al. 2011). Sexual dimorphism is common in reptiles; males and females differ in multiple characters (Butler & Losos 2002, Bayrakci & Ayaz 2014), mainly in size and color variation according to the sex, these aspects are known among testudines (Berry & Shine 1980, Gibbons & Greene 1990, Brito et al. 2009). The sexual dimorphism is to be related with variable reproductive aspects as well as energy resource for breeding in females and also male combat (Gibbons 1990). Most of Chelidae species present a greater number of females than males; whereas males and females do not show evident differences among the carapace sizes in some other species (Ceballos et al. 2012). Within of genus Phrynops and Mesoclemmys, females are larger than males (Molina 1992, McCord et al. 2001, Moll & Moll 2004, Martins & Souza 2008, Brito et al. 2009, Molina et al. 2012, Forero-Medina et al. 2013, Marques et al. 2013). Iverson (2010) found no significant differences for the mean carapace length between male and female K. scorpioides, samples from the Yucatan peninsula in Belize, on the other hand, Berry & Shine (1980) and Ceballos et al. (2012) recorded males presenting larger size. Tail length measurements are commonly greater for males than females, as recorded by this study for the species found. This characteristic is due to the presence of the penis, which has been associated with longer tails (Gibbons & Lovich 1990). In addition, this characteristic has also been associated with the selection of the best males for mating (Vogt 1980). Males with longer tails have more success in the mating process (Moll 1980). In turtles, the reproductive cycle seems to be synchronized with abiotic variables, especially air temperature and precipitation levels (Souza 2004, Rueda-Almonacid et al. 2007, Citation as online first paper: North-western Journal of Zoology 11: art.141514 Schneider et al. 2011, Rodrigues & Silva 2014). Despite reproduction, abiotic variables can also affect the behavior of the specimens, e.g. the species P. geoffroanus present higher activity levels during warmer periods, promoting the forage activity, though presenting few N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y movements during rainy periods (Souza 1999), also observed in this study (Fig. 4). In conclusion, the data reported here can be used to subsidize conservation plans for the species in question and provides new data about demography aspects, sex ratio and sexual dimorphism of testudines in the semi-arid regions of Brazil. ACKNOWLEDGEMENTS Fundação de Amparo à Ciência e Tecnologia de Pernambuco-FACEPE (APQ-1264- 2.05/10), Coordenação de apoio ao ensino superior-CAPES, Instituto Chico Mendes-ICMBio (SISBIO), license number 27143-1. We thank Paulo Braga de Melo for assistance with the graphics, Alane A. V. 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Mean and Standard Deviation in millimeters of the CL, carapace length; CW, carapace width; PL, Plastron length; PW, Plastron Width; CH, carapace height; BL, bridge length; TL, tail length; and weight in grams. CW (mm) PL (mm) PW (mm) CH (mm) BL (mm) TL (mm) Weight (g) o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y CL (mm) P. geoffroanus J 114.06±38.09 F 233.63±27.36 170.84±22.64 181.84±19.99 100.81±20.46 55.59±5.7 M 220.9±23.05 M. tuberculata 89.36±27.6 94.66±31.32 55.71±22.34 156.52±17.38 167.76±19.46 94.40±32.23 35±11.42 51.78±8 30.08±5.98 12.66±4.9 55.9±9.05 200±13 22.03±2.86 1040±35 51.15±6.92 24.47±2.93 860±34 F 183.01±23.34 130.43±21.97 159.18±20.14 98.28±13.52 58.12±9.99 46.76±7.76 13.72±3.66 750±31 F 134.79±21.65 81.98±4.76 115.46±8.69 57.82±6.14 52.43±5.48 35.34±2.98 10.83±3.78 309±03 86.08±4.14 123.01±10.36 60.34±9.75 52.67±4.24 37.25±5.14 27.63±2.69 397±18 N K. scorpioides M 140.85±8.59 Citation as online first paper: North-western Journal of Zoology 11: art.141514 Table 2. Sexual dimorphism index (SDI; Lovich and Gibbons 1990) populations of P. geoffroanus, M. tuberculata, and K. scorpioides in the Environmental Protection Area of the Chapada Araripe. Values of carapace length (mean, median and mode) of females, males and juveniles. The measurement of the CL of the three largest specimens. Larger specimens N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y Carapace length N M. tuberculata P. geoffroanus K. scorpioides Mean Median Mode 1 3 5 SDI 0 Female 10 183.01 174.32 174 220.03 218.22 207.32 Male 0 - - - - - - Juveniles 0 - - - - - - SDI 1.06 Female 20 233.62 235 222 and 235 295.4 240.83 273.32 Male 13 220.91 218.5 197 and 215 255.6 250.36 243.64 Juveniles 11 114.05 118 128 181 151.86 140.5 SDI 1.04 Female 3 134.79 129.54 125 165 141.39 - Male 5 140.85 141.61 141 and 145 154.5 151.13 148.70 Juveniles 0 - - - - - - N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y Citation as online first paper: North-western Journal of Zoology 11: art.141514 Fig 1. Map of the Area of Environmental Protection of the Chapada do Araripe - Ceará. Coordinates: 7°38’10.70’S and 41°55'10.58"O/ DATUM –WGS84. N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y Citation as online first paper: North-western Journal of Zoology 11: art.141514 Fig. 2. Biometric measures collected: Carapace width (CW), carapace length (CL), Plastron length (PL), Plastron Width (PW), Bridge Length (BL). N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y Citation as online first paper: North-western Journal of Zoology 11: art.141514 Fig. 3. Monthly captures of the species Phrynops geoffroanus (bars), monthly accumulated rainfall (blue line) and mean monthly temperature (red line) in Araripe Bioregion between August 2011 and July 2012. N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y Citation as online first paper: North-western Journal of Zoology 11: art.141514 Fig. 4. Monthly captures of the species Mesoclemmys tuberculata (bars), monthly accumulated rainfall (blue line) and mean monthly temperature (red line) in Araripe Bioregion between August 2011 and July 2012. N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y Citation as online first paper: North-western Journal of Zoology 11: art.141514 Fig. 5. Monthly captures of the species Kinosternon scorpioides (bars), monthly accumulated rainfall (blue line) and mean monthly temperature (red line) in Araripe Bioregion between August 2011 and July 2012. N o Ac rth ce -w pt es ed te pa rn pe Jo r - urn un al til of pr Zo oo o fin log g y Citation as online first paper: North-western Journal of Zoology 11: art.141514
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