NORTH-WESTERN JOURNAL OF ZOOLOGY 11 (2): 204-212 ©NwjZ, Oradea, Romania, 2015 Article No.: 141514 http://biozoojournals.ro/nwjz/index.html

Demography, sex ratio, and sexual dimorphism of Testudines in Araripe Bioregion, Ceará, Northeastern

Carina MOURA1,*, Geraldo MOURA1, Leonardo CHAVES1, Sérgio MUNIZ1, Eliana-Sofia VEGA1 and Valter JÚNIOR2

1. Universidade Federal Rural de Pernambuco, Department of Biology, Laboratory Herpetology and Paleoherpetology, UFRPE, Brazil. 2. Universidade Federal de Pernambuco, Department of Statistics, UFPE, Brazil. *Corresponding author, C. Moura, E-mail: [email protected]

Received: 03. July 2014 / Accepted: 19. November 2014 / Available online: 03. August 2015 / Printed: December 2015

Abstract. In spite of the increasing number of demographic studies about freshwater , 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 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 scorpioides and 10 specimens of 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: geoffroanus, Kinosternon scorpioides, Mesoclemmys tuberculata, , , Population structure.

Introduction Demographic parameters are essential tools to evaluate the real status of conservation of testu- The Caatinga morphoclimatic domain is unique in dine communities (Gibbons & Greene 1990, Smith that it is only found within the boundaries of Bra- et al. 2006). Demographic studies about neotropi- zil (Andrade-Lima 1981, Vitt & Vangilder 1983). cal freshwater turtles are limited (Souza 2004, This domain is known for high temperatures, low Martins & Souza 2008), although a necessity for a relative humidity, a hot and semi-arid climate better understanding of the population dynamics (Velloso et al. 2002), which is typically seasonal, (Gibbons 1970, Brito et al. 2009). Strong relation with a long dry season and short periods of vari- between population dynamics of testudines and able rainfall (Reis 1976, Leal et al. 2003). The phy- climatic variation are common, resulting in a sea- tophysiognomic peculiarities found in flora, cli- sonal reproductive cycle (Souza 2004). mate and geological characteristics of this biome The duration and level of biological activities sustain different microhabitats and consequently, such as foraging, thermal regulation and migra- exhibit rich flora and fauna (Rodrigues 2003). tion are determined by genetic interactions and Testudines are part of the group of ectother- environmental conditions (Molina 1992, Roe & mic Sauropsida that typically exhibit a long life- Georges 2008, Ferreira-Júnior 2009). Some fresh- span, delayed sexual maturity, and slow growth water turtles shown more activity during warmer (Rueda-Almonacid et al. 2007). These characteris- months, that promote thermoregulatory activities tics have been associated with a low rate of indi- (Souza 2004, Forero-Medina et al. 2012). However vidual substitution among populations, making some other species, such as those belonging to the this group more susceptible to anthropogenic Chelidae show estivation behavior during threats and environmental weathering (Rodrigues long dry periods (Mittermeier 1978, Vogt 2008, 2005, Moura et al. 2012). Forero-Medina et al. 2012, Forero-Medina et al. Demography of Testudines in North East of Brazil 205

2013). Migration has also been observed in totaling 60 days of sampling and eight hours of daily neotropical freshwater turtles searching for favor- work, with a total of 480 hours. able environments (Fraxe-Neto et al. 2011). These Two convergence hoop traps were used, with mean measurements of 100 cm in length, 70 cm in diameter, aspects directly influence the population density containing dual funnel, and 50cm of the diameter of and sex ratio, they form a set that is responsible opening, 1 cm2 of mesh size and were baited with pieces for variations in the population dynamics of the of chicken inside a net of resistant plastic and fine mesh (5 group (Gibbons 1990, Brito et al. 2009, Fraxe-Neto mm) to avoid ingesting the content (Vogt 1980). et al. 2011). Traps were inspected twice daily (once during the day The aim of this study is to describe the de- and once at night). mography of a testudine community in the area of Each individual captured was marked with slits on the marginal shields (Cagle 1939). The gender was deter- Caatinga (Araripe Bioregion), while focusing on mined based on secondary sexual characteristics: tail the following specific objectives: (i) to estimate the length and coloration, this second characteristic was only density of the populations; (ii) to assess the sex ra- inspected in Kinosternidae (Gibbons & Lovich 1990). All tio and sexual dimorphism; (iii) to correlate the females were submitted to gentle manual inspection in number of monthly captures of the species with the abdominal area, beside hind paws, to verify the pres- the monthly accumulated rainfall and mean ence of abdominal shelled eggs. Individuals, whose sex monthly temperature. was not clearly identifiable through these characteristics, were considered juveniles (Forero-Medina et al. 2011).

The biometric data were recorded using a 1 mm pre-

cision caliper and a portable digital scale to the nearest 0.1 Materials and Methods g. The following biometric measurements were recorded: Study Area Rectilinear carapace length (CL): the distance between the The study was conducted in the Environmental Protec- anterior margin of the nuchal shield or the first marginal tion Area (EPA) of Chapada do Araripe (7°38’10.70’S and shield to the posterior extremity of the supracaudal shield. 41°55'10.58"W; DATUM: WGS84; 700 m a.s.l.; Fig. 1), lo- Rectilinear carapace width (CW): the distance between cated in Araripe Bioregion. Data was collected in the city the most external marginal shields. Rectilinear plastron of Jardim, southern Ceará, a region that is characterized length (PL): the distance between the center of the gular as “bushy Caatinga” (Mittermeier et al. 1982). Collections shields and the center of the anal shield. Rectilinear plas- were performed in a weir (7°39'10.76" S and 39°16'20.52" tron width (PW): maximum linear width of plastron. W) with an irregular shape and an approximate perimeter Bridge length (BL): distance between the inguinal and of 3 km and area of 5.2 ha. Bushes and a large quantity of axillary shields. Tail length (TL): the distance between the aquatic vegetation are found in the border of the weir. cloaca and the end of the tail. Carapace height (CH): the distance between the central vertebral shield and the ab- Sampling dominal shield (Fig. 2). Sampling was performed between August 2011 and July Abiotic data (monthly rainfall and monthly average 2012. Traps were placed in the water body and opened air temperature) were provided by the ICMBio Meteorol- for five days in each month. The study lasted 12 months, ogy Center in Barbalha, Ceará.

Figure 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. 206 C. Moura et al.

Figure 2. Biometric measures collected: Carapace width (CW), carapace length (CL), Plastron length (PL), Plastron Width (PW), Bridge Length (BL).

Data analysis tured, of which six (66%) were male and three The population densities were calculated using the total (33%) were female. Ten individuals of M. tubercu- number of specimens collected divided by the total area lata were captured, all of them were female. of the weir. During this period, 11 females of P. geoffroanus, Associations between monthly captures and recap- tures and monthly rainfall, monthly average air tempera- as well as one male and one juvenile, were recap- ture, and solar intensity data were analyzed using Pear- tured. One of the females was recaptured on four son’s correlation. separate occasions. The minimal interval between Biometric measurements and weight were compared captures was two days and the maximal interval by ANCOVA in an attempt to assess differences in mor- between captures was 220 days. For K. scorpioides, phometric variables between males and a female, using six males and one female were recaptured. One the R programming language (R Development Core Team male specimen was recaptured twice. The minimal 2008), CL was considered the main variable and CW, PL, PW, BL, TL, CH and weight as co-variables. Juveniles interval between captures was 21 days and the were excluded for this analysis. maximal interval between captures was 103 days. The sexual dimorphism index was calculated using Among the female M. tuberculata captured, four the ratio of the biometric mean values for the carapace of were recaptured, the shortest time between cap- males and females. The numerator was the mean of the tures was five days and the longest time between gender with the highest value. Biometric proportions captures was 44 days. were based on the mean, median, mode, the maximal The months with the largest amount of cap- value of the carapace and plastron length, as well as the mean values for 3 and 5 of the largest adult individuals of tures were February and March, with approxi- both genders (Gibbons & Lovich 1990). The chi-squared mately 50% of all recorded captures. These are the test (Zar 1999) was used to test whether the sex ratios dif- two months correlated with low precipitation, ac- fered to 1:1, testing the hypothesis that there would be no cording to the meteorological history of the region significant difference between the number of males and (Fig. 3). In September, M. tuberculata (Fig. 4) and K. females, using the program Prism 5. scorpioides (Fig. 5) were the most captured species.

September was the month with the highest re-

Results corded rainfall and the lowest temperatures. The recaptures occurred between January and Three species were recorded in the community of July for P. geoffroanus, with the largest number of testudines, two of which belonged to the Chelidae recaptures recorded in March, which had low ac- family, (Schweigger, 1812) cumulated rainfall and high temperatures. For K. and Mesoclemmys tuberculata (Luederwaldt, 1926), scorpioides, the recaptures occurred between Sep- and one of which belonged to the Kinosternidae tember and December, which were the months family, Kinosternon scorpioides (Linnaeus 1766). The with the most rainfall. M. tuberculata were recap- sampling efficiency was 2.13 individuals captured tured in August, September and November. Dur- per day. ing these months, temperatures were low and In total, 44 specimens of P. geoffroanus were high rainfall was recorded. marked. Twenty (45.45%) were female, thirteen Population density was approximately 9 tur- (29.54%) were male and eleven (25%) were juve- tles/ha for P. geoffroanus, 2 turtles/ha for M. tuber- culata and 2 turtles/ha for K. scorpioides.

niles. Nine individuals of K. scorpioides were cap- Demography of Testudines in North East of Brazil 207

Figure 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.

Figure 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.

Among females of P. geoffroanus, the size of and the mean weight was 750 grams, however the CL was bigger than in males, and the females only females were caught. K. scorpioides is one of weighed on average 17% more than males. The CL the smallest testudines, for this species, the male of M. tuberculata ranged from 148.9 to 220.03mm specimens exhibited CL values bigger than ob- 208 C. Moura et al. served in females (Table 1). phism was noticed (Table 2). The sexual dimorphism index, calculated us- P. geoffroanus exhibited a sex ratio of ing the mean carapace values for males and fe- 1.53(♀):1(♂), (P=0.223, X²=0.046), with no signifi- males, was 1.06 (deviated for females) for P. geof- cant difference between the number of males and froanus and 1.04 (deviated for males) for K. sco- females. K. scorpioides exhibited a sex ratio of pioides. Based on the biometric data, it was possi- 1(♀):1.25(♂) (p= 0.222, X²=0.225). It was not possi- ble to observe sexual dimorphism in P. geoffroanus, ble to confirm the sex ratio of M. tuberculata as the species, with the exception of the tail, were only females were captured. This indicates that the larger for females than for males, the measure- sex ratio of this species may be deviated for fe- ments significantly different between males and males (Table 2). females (parameter sex, p=0.038, F= 4.8491). For K. A number of reproductive aspects were noted scorpioides, sexual dimorphism was observed and during the sampling period. In the months of May all of the biometric variables were larger for males and July, one female of P. geoffroanus was recorded than for females, however the measurements were with eggs, indicating that nesting begins in these not significantly different (parameter sex, p=0.071, months. At the end of March, a newly-hatched ju- F=0.0711). Regarding the species M. tuberculata, venile was captured measuring 39.9 mm and 28.2 only females were identified, no sexual dimor- mm for the CL and CW, respectively. Low accu-

Figure 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.

Table 1. Biometric data of P. geoffroanus, M. tuberculata and K. scorpioides sampled in the Araripe Bioregion. 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.

CL (mm) CW (mm) PL (mm) PW (mm) CH (mm) BL (mm) TL (mm) Weight (g) J 114.06±38.09 89.36±27.6 94.66±31.32 55.71±22.34 35±11.42 30.08±5.98 12.66±4.9 200±13 P. geoffroanus F 233.63±27.36 170.84±22.64 181.84±19.99 100.81±20.46 55.59±5.7 55.9±9.05 22.03±2.86 1040±35 M 220.9±23.05 156.52±17.38 167.76±19.46 94.40±32.23 51.78±8 51.15±6.92 24.47±2.93 860±34 M. tuberculata 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 K. scorpioides M 140.85±8.59 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

Demography of Testudines in North East of Brazil 209

Table 2. Sexual dimorphism index (SDI; Lovich and Gibbons 1990) populations of P. geoffroanus, M. tu- berculata, 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.

Carapace length Larger specimens N Mean Median Mode 1 3 5 M. tuberculata SDI 0 Female 10 183.01 174.32 174 220.03 218.22 207.32 Male 0 ------Juveniles 0 ------P. geoffroanus 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 K. scorpioides 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 ------

mulated rainfall was recorded in this period (Ta- 21 turtles/ha were recorded (Moll 1990). Accord- ble 1). ing to Gibbons et al. (1983) and Moll (1990) the Temperature was not correlated with the species of Kinosternidae migrate regularly in re- number of monthly captures for any of the species sponse to drought and other environmental fac- in question. However, rainfall had a negative cor- tors. Previous work with Mesoclemmys estimated, relation to the number of monthly captures of P. at different seasons in the same stream, a density geoffroanus (coefficient of correlation= -0.63, Num- range from 16 turtles/ha to 170 /ha (Forero- ber of captures=54 and p= 0.028). 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) Discussion estimated the density of M. vanderhaegei to be be- tween 12 and 36 individuals to five streams. Spe- The populations sizes recorded here are possibly cies of Mesoclemmys bury on land during influenced by the limiting conditions of the area, drought season and aestivates, these behaviors particularly in relation to the availability of food could influence the population structure evalua- and the adverse climatic conditions: a period of in- tion that oscillate according to the abiotic condi- tense drought periodically eliminates a large per- tions (Rueda-Almonacid et al. 2007, Forero- centage of the population or induces migration to Medina et al. 2011). Population density is higher in more suitable places (Aguiar & Buriti 2009). In localities with greater availability of food and re- comparison with other studies, we recorded low productive sites (Souza & Abe 2000, Rueda- densities for testudines in semi-arid areas of Brazil, Almonacid et al. 2007, Forero-Medina et al. 2007). these values may be justified because we used the Furthermore, human pressure influences the dy- number of individuals captured during the sam- namic of populations; in the semi-arid regions of pling to determine the density, which can be un- Brazil, several species of are used for hu- derestimated. man consumption and medical proposes, the re- Areas that offer more resources have density cords include the species K. scorpioides, M. tubercu- of P. geoffroanus around 170-230 turtles/ha, in ur- lata and P. tuberosus (Alves et al. 2012). ban rivers, these results are related with abundant Sex ratio in wild populations normally diverge biomass, absence of predation pressure and plenty from 1:1 (Gibbons 1990, Forero-Medina et al. 2007, of nesting areas (Souza & Abe 2000). The density Brito et al., 2009). Among the regulating factors of of K. scorpioides populations varied from 77 to 254 sex ratio there are a difference of mortality be- turtles/ha in mangrove forests (Forero-Medina et tween sexes, different ages of sexual maturity and al. 2007) and about 272 turtles/ha found in a con- the sexual determination for temperature (Gib- served pond in Chiapas, Mexico (Iverson 1982), bons 1990). According to Bury (1979), the sex ratio furthermore in areas with potential predators 14 to of testudine populations differs among species 210 C. Moura et al. and oscillations often occur as a result of different few movements during rainy periods (Souza 1999), collection techniques, behavioral differences be- also observed in this study (Fig. 4). tween genders or incubation temperatures that in- In conclusion, the data reported here can be fluence the sexual determination of some turtles used to subsidize conservation plans for the spe- (Gibbons 1970, Vogt 1980, Fachin-Téran et al. 2003). cies in question and provides new data about de- Due to the fact that the specimens are more active mography aspects, sex ratio and sexual dimor- during reproductive season when they seek a re- phism of testudines in the semi-arid regions of ceptive partner for copulation (Berry & Shine 1980, Brazil. Famelli et al. 2011). Sexual dimorphism is common in reptiles; males and females differ in multiple characters (Butler & Losos 2002, Bayrakci & Ayaz 2014), Acknowledgements. Fundação de Amparo à Ciência e mainly in size and color variation according to the Tecnologia de Pernambuco-FACEPE (APQ-1264-2.05/10), sex, these aspects are known among testudines Coordenação de apoio ao ensino superior-CAPES, Instituto Chico Mendes-ICMBio (SISBIO), license number (Berry & Shine 1980, Gibbons & Greene 1990, Brito 27143-1. We thank Paulo Braga de Melo for assistance et al. 2009). The sexual dimorphism is to be re- with the graphics, Alane A. V. Oliveira Couto for lated with variable reproductive aspects as well as providing help with the statistical analysis and Alisa energy resource for breeding in females and also Samoylova for improving the english of this paper. 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 References the carapace sizes in some other species (Ceballos Andrade-Lima, D. (1981): The caatinga dominium. Revista et al. 2012). Within of genus Phrynops and Meso- Brasileira Botânica, 2: 149-153. clemmys, females are larger than males (Molina Aguiar, J.O., Buriti, C.O. (2009): Revisitando o Semiárido: Cenários de Vidas e de Sol. Revista Territórios e Fronteiras 2: 271-201. 1992, McCord et al. 2001, Martins & Souza 2008, Alves, R.R.N., Pereira-Filho, G.A., Vieira, K.S., Souto, W.M.S., Brito et al. 2009, Molina et al. 2012, Forero-Medina Mendonca, L.E.T., Montenegro, P.F.G.P., Almeida, W.O., Vieira, et al. 2013, Marques et al. 2013). Iverson (2010) W.L.S. (2012): A zoological catalogue of hunted reptiles in the semiarid region of Brazil. Journal of Ethnobiology and found no significant differences for the mean Etnomedicine 8: 1-19. carapace length between male and female K. scor- Bayrakci, Y., Ayaz, D. (2014): Dynamics of a Central Anatolian pioides, samples from the Yucatan peninsula in Be- population of orbicularis (Linnaeus, 1758) (Testudines: ). Herpetozoa 27(1/2): 29-37. lize, on the other hand, Berry & Shine (1980) and Berry, J.F., Shine, R. (1980): Sexual size and sexual selection in Ceballos et al. (2012) recorded males presenting turtles (, Testudinata). Oecologia 44: 185–191. larger size. Bury, R.B. (1979): Population ecology of freshwater turtles. pp. 571– 604. In: Harless, M. and Morlock, H. (eds.). Turtles: Perspectives Tail length measurements are commonly and Research. New York: John Wiley and Sons. greater for males than females, as recorded by this Butler, M.A., Losos, J.B. (2002): Multivariate sexual dimorphism, study for the species found. This characteristic is sexual selection, and adaptation in Greater Antillean Anolis lizards. Ecological Monographs 72: 541-559. due to the presence of the penis, which has been Brito, E.S., Strussmann, C., Penha, J.M.F. (2009): Population associated with longer tails (Gibbons & Lovich Structure of Mesoclemmys vanderhaegei (Bour, 1973) (Testudines: 1990). In addition, this characteristic has also been Chelidae) in the Cerrado of Chapada dos Guimarães, Mato Grosso, Brazil. Biota Neotropica 9(4): 1-4. associated with the selection of the best males for Cagle, F.R. (1939): A system of marking turtles for future mating (Vogt 1980). Males with longer tails have identification. Copeia. pp. 170-173. more success in the mating process (Moll 1980). Ceballos, C.P., Adams, D.C., Iverson, J.B., Valenzuela, N. (2012). Phylogenetic Patterns of Sexual Size Dimorphism in Turtles and In turtles, the reproductive cycle seems to be Their Implications for Rensch’s Rule. Evolutionary Biology synchronized with abiotic variables, especially air 40:194-208. temperature and precipitation levels (Souza 2004, Fachin-Téran, A., Vogt, R. C., Thorbjarnarson, J.B. (2003): Estrutura populacional, razão sexual e abundância de Rueda-Almonacid et al. 2007, Schneider et al. 2011, sextuberculata (Testudines, ) na Reserva de Rodrigues & Silva 2014). Despite reproduction, Desenvolvimento Sustentável Mamirauá, Amazonas, Brasil. abiotic variables can also affect the behavior of the Phyllomedusa, Belo Horizonte 2: 43-63. Famelli, S., Bertoluci, J., Molina, F.B., Matarazzo-Neuberger, W.M. specimens, e.g. the species P. geoffroanus present (2011): Structure of a Population of maximiliani higher activity levels during warmer periods, (Testudines, Chelidae) from Parque Estadual da Serra do Mar, promoting the forage activity, though presenting an Atlantic Rainforest Preserve in Southeastern Brazil. Chelonian Conservation and Biology 10(1): 132-137. Demography of Testudines in North East of Brazil 211

Ferreira-Júnior, P.D. (2009): Efeitos de Fatores Ambientais na Mesoclemmys vanderhaegei (Testudines, Chelidae) in a Reprodução de Tartarugas. Acta Amazônica 2: 319–334. silvicultural system in southeastern Brazil. Herpetology Notes 6: Forero-Medina, G., Castaño-Mora, O.V., Montenegro, O. (2007): 179-182. Abundance, Population Structure, and Conservation of Martins, F.I., Souza, F.L. (2008): Estimates of growth of the Atlantic Kinosternon scorpioides albogulareon the Caribbean Island of San rain forest freshwater turtle Hydromedusa maximiliani (Chelidae). Andrés, . Chelonian Conservation and Biology 2: 163- Journal of Herpetology 41: 54-60. 169. McCord, W.P., Joseph-Ouni, M., Lamar, W.W. (2001): A taxonomic Forero-Medina, G., Cardenas-Arevalo, G., Castaño-Mora, O.V. reevaluation of Phrynops (Testudines: Chelidae) with the (2011): Abundance, home range, and movement patterns of the description of two new genera and a new species of Batrachemys. endemic species Dahl’s Toad-headed Turtle (Mesoclemmys dahli) Revista de Biología Tropical 49(2): 715-764. in Cesar, Colombia. Chelonian Conservation and Biology 10(2): Mittermeier, R.A., Rhodin, A.G.J., Medem, F., Soini, P., Hoogmoed, 228–236. M.S., Espinoza, N.C. (1978): Distribution of the South American Forero-Medina, G., Iverson, J.B., Carr, J.L., Castaño-Mora, O.V., Chelid Turtle Phrynops gibbus, with observations on habitat and Galviz-Rizo, C.A., Renteria-Moreno, L.E. (2012): Familia reproduction. Herpetologica 34: 94-100. Kinosternidae. pp. 327–331. In: Páez, V.P., Morales-Betancourt, Mittermeier, R.A., Coimbra-Filho, A.F., Constable, I.D., Rylands, M.A., Lasso, C.A., Castaño-Mora, O.V., aBock, B. (eds.). Biología A.B., Valle, C.M. (1982): Conservation of primates in the Atlantic y Conservación de las Tortugas Continentales de Colombia. Forests of Brazil. International Zoological Yearbook 22: 2-17. Serie Editorial Recursos Hidrobiológicos y Pesqueros Molina, F.B. (1992): Observações Sobre Os Hábitos Alimentares e o Continentales de Colombia. Instituto de Investigacion de los Comportamento Alimentar de Phrynops geoffroanus (Schweigger, Recursos Biológicos Alexander von Humboldt, Bogotá, 1812) em cativeiro (Reptilia, Testudines, Chelidae). Revista Colombia. Brasileira de Zoologia 7(3): 319-326. Forero-Medina, G., Castaño-Mora, O.V., Cárdenas-Arevalo, G., and Molina, F.B., Machado, F.A., Zaher, H. (2012): Taxonomic validity Medina-Rangel, G.F. (2013): Biología y Conservación de las of (McCord, Joseph-Ouni &Lamar, Tortugas Continentales de Colombia. Biología y Conservación 2001) (Testudines, Chelidae) inferred from morphological de las Tortugas Continentales de Colombia. Mesoclemmys dahli analysis. Zootaxa 3575: 63-77. (Zangerl and Medem 1958) – Dahl’s Toad-Headed Turtle, Moll, E.O. (1980): Natural history of the river terrapin, baska Carranchina, Tortuga Montañera 5: 069.1–069.8. In: Rhodin, (Gray) in Malaysia (Testudines: Emydidae). Malaysian Journal A.G.J., Pritchard, P.C.H., van Dijk, P.P., Saumure, R.A., of Science 6: 23-62. Buhlmann, K.A., Iverson, J.B., and Mittermeier, R.A. (eds.). Moll, D. (1990): Population sizes and foraging ecology in atropical Conservation Biology of Freshwater Turtles and : A freshwater stream turtle community. Journal of Herpetology 24: Compilation Project of the IUCN/SSC and Freshwater 48–53. Turtle Specialist Group. Chelonian Research Monographs. Moura, C.C.M., Vega, E.S.F., Muniz, S.L.S., Silva, J.S., Couto, Fraxe-Neto, H.J., Brasil, M.A., Horta, G.F., Barros, T.O., Falcon, A.A.V.O., Arruda, A.R., Araújo, E.L., Moura, G.J.B. (2012): G.B., Colli, G.R. (2011): Demography of spixii Predação de ninhos de Phrynops geoffroanus (Schweigger, 1812) (Testudines, Chelidae) in the Brazilian Cerrado. Chelonian (Testudines: Chelidae) em remanescente de mata atlântica Conservation and Biology 10(1): 82-90. Nordeste do Brasil. Revista Brasileira de Zoociências 14(1,2,3): Gibbons, J.W. (1970): Reproductive dynamics of a turtle ( 147-153. scripta) population in a reservoir receiving heated effluent from Reis, A.C. (1976): Clima da Caatinga. Anais da Academia Brasileira a nuclear reator. Canadian Journalof Zoology 48: 881-885. de Ciências, São Paulo 48: 325-335. Gibbons, J.W. (1983): Reproductive characteristics and ecology of Rodrigues, M.T. (2003): Herpetofauna Da Caatinga. pp. 181-286. In: the mud turtle, Kinosternon subrubrum (Lacepede). Leal, I. R., Tabarelli, M. and Silva, J.M.C. (eds.), Ecologia e Herpetologica 39: 254–271. Conservação da Caatinga. Recife: UFPE. Gibbons, J.W. (1990): Sex ratios and their significance among turtle Rodrigues, M.T. (2005): Conservação dos répteis brasileiros: os populations. pp.171-182. In: Life history and ecology of the desafios de um país megadiverso. Megadiversidade 1: 88-94. slider turtle (J.W. Gibbons, ed.). Smithsonian Institution Press, Rodrigues, J.F.M., Silva, J.R.F. (2014): How Washington. (Testudines: Chelidae) reproduce in the Brazilian Caatinga? Gibbons, J.W., Greene, J.L. (1990): Reproduction in the slider and North-Western Journal of Zoology 10(1): 143-148. other species of turtles. pp. 124-134. In: Gibbons, J.W. (ed.) Life Roe, J., Georges, A. (2008): Terrestrial activity, movements and History and Ecology of the slider Turtle. Smithsonian Institution spatial ecology of an Australian freshwater turtle, Press, Washington, Dc. longicollis, in a temporally dynamic wetland system. Austral Gibbons, J.W., Lovich, J.E. (1990): Sexual dimorphism in turtles Ecology 33: 1045–1056. with emphasis on the slider turtle ( scripta). Rueda-Almonacid, J.V., Carr, J.L., Mittermeier, R.A., Rodriguez, Herpetetological Monographs 4: 1-20. J.V., Mahecha, S.T.R.B., Vogt, R.C., Rhodin, A.G.J., Iverson, J.B. (1982): Biomass in turtle populations: a neglected Ossavelasquez, J., Rueda, J.N., Mittermeier, C.G. (2007): Las subject. Oecologia (Berlin) 55: 69–76. tortugas e los crocodilianos de los países andinos del Trópico. Iverson, J.B. (2010): Reproduction in the Red-Cheeked Mud Turtle Bogotá, Conservación Internacional. 538 pp. (Kinosternon scorpioides cruentatum) in Southeastern Mexico and Schneider, L., Ferrara, C.R., Vogt, R.C., Guilhon, A.V. (2011): Belize, with Comparisons Across the Species Range. Chelonian Nesting ecology and nest predation of Phrynops geoffroanus Conservation and Biology 9(2): 250-261. (Testudines, Chelidae) in the Guaporé River of the Brazilian and Leal, I.R., Tabarelli, M., Silva, J.M.C. (2003): Ecologia e Conservação Bolivian Amazon. Chelonian Conservation and Biology 10: 206- da Caatinga: Uma introdução ao desafio. pp. 13-16. In: Leal, I. R., 212. Tabarelli, M. and Silva, J.M.C. (Eds.). Ecologia e Conservação da Schweigger, A.F. (1812): Prodromus Monographia Cheloniorum Caatinga. Recife: UFPE. auctore Schweigger. Königsberg. Archiv für Naturwissenschaft Linnaeus, C. (1766): Systema naturæ per regna tria naturæ, und Mathematik 1: 271-368. secundum classes, ordines, genera, species, cum characteribus, Smith, G.R., Iverson, J.B., Rettig, J.E. (2006): Changes in a turtle differentiis, synonymis, locis. Tomus I. Editio duodecima, community from a Northern Indiana lake: a long-term study. reformata. Laurentii Salvii, Stockholm, Holmiae pp. 1-532. Journal of Herpetology 40(2): 180-185. Luederwaldt, H. (1926): Os chelonios brasileiros. Revista Museo Souza, F.L. (1999): Ecologia do cagado Phrynops geoffroanus Paulista 14: 403–470. (Schweigger, 1812) em ambiente urbano poluído (Reptilia, Marques, T.S., Lara, N.R.F., Bassetti, L.A.B., Ferronato, B.O., Testudines, Chelidae). PhD thesis, Universidade Estadual Malvásio, A., Verdade, L.M. (2013): Population structure of Paulista, Rio Claro, Sao Paulo, Brazil. 212 C. Moura et al.

Souza, F.L. (2004): Uma revisão sobre os padrões de atividade, Vogt, R.C. (1980): New methods for trapping aquatic turtles. reprodução e alimentação de cágados brasileiros (Testudines, Copeia 2: 368-371. Chelidae). Phyllomedusa 3: 15-27. Vogt, R.C. (2008): Tartarugas da Amazônia. Lima, , Gráfica Souza, F.L., Abe, A.S. (2000): Feeding ecology, density and biomass Biblos. of the freshwater turtle, Phrynops geoffroanus, inhabiting a Zar, J.H. (1999): Biostatistical Analysis. Prentice Hall, New Jersey. polluted urban river in south-eastern Brazil. Journal of the Zoological Society of London 252: 437-446. Velloso, A.L., Sampaio, V.S.B., Pareyn, F.G.C. (2002): Ecorregiões propostas para o Bioma Caatinga. – APNE / Nature Conservancy do Brasil, Recife. Vitt, L.J., Vangilder, L.D. (1983): Ecology of a Snake Community in Northeastern Brazil. Amphibia-Reptilia 4: 273-296.