NORTH-WESTERN JOURNAL OF ZOOLOGY 11 (1): 127-132 ©NwjZ, Oradea, Romania, 2015 Article No.: 141511 http://biozoojournals.ro/nwjz/index.html
Population structure, activity, and sex ratio of Phrynops tuberosus (Testudines: Chelidae) in Caatinga, Brazil
João Fabrício Mota RODRIGUES 1,2,* and José Roberto Feitosa SILVA1,3
1. Programa de Pós-Graduação em Ecologia e Recursos Naturais – Universidade Federal do Ceará, Centro de Ciências, Avenida Humberto Monte S/N, Campus do Pici, Fortaleza, CE, Brazil CEP 60455-760. 2. Núcleo Regional de Ofiologia da Universidade Federal do Ceará (NUROF-UFC). Avenida Humberto Monte S/N, Universidade Federal do Ceará, Departamento de Biologia, Bloco 902, Campus do Pici, Fortaleza, CE, Brazil CEP 60455-760. 3. Laboratório de Histologia Animal – Universidade Federal do Ceará, Centro de Ciências. Avenida Humberto Monte S/N, Campus do Pici, Fortaleza, CE, Brazil CEP 60451-970. *Corresponding author, J.F.M. Rodrigues, E-mail: [email protected]
Received: 11. August 2014 / Accepted: 22. October 2014 / Available online: 04. January 2015 / Printed: June 2015
Abstract. We describe and discuss the population structure and activity pattern of the poorly known species Phrynops tuberosus, the Cotinga River Toad-headed Turtle, in the Banabuiú River in the semi-arid Caatinga, Ceará. Animals were captured by snorkelling between December 2011 and November 2012. We captured 134 animals (94 males, 24 females and 16 juveniles), a sex ratio of 3.92:1 males/females was found, and the population of P. tuberosus consisted mainly of medium to large sized adults. Air temperature and monthly precipitation did not influence the number of captured individuals, which was similar throughout the year.
Key words: ecology, semi-arid environment, Phrynops geoffroanus complex, size-class distribution, turtles.
Introduction plexa; McCord et al. 2001, Bour & Zaher 2005, Rueda-Almonacid et al. 2007), but most data Population studies of turtles describe sex ratio, available for these species are from studies in sexual dimorphism, age or size structure, and south-eastern and north-western Brazil (Souza & population density (Gibbons 1990, Verdon & Abe 2001, Rueda-Almonacid et al. 2007). Hence, Donnelly 2005, Germano & Rathbun 2008, Lescano this study is one of the few describing population et al. 2008, Bujes et al. 2011). Comparative analyses aspects of a turtle species in the Caatinga. of these biological aspects and natural history data Phrynops tuberosus is a species commonly allow us to test hypotheses related to various eco- found in northern and north-eastern Brazil in ar- logical theories, improving species risk evaluation, eas of Caatinga and Tropical Rain Forest, occur- which are important for conservation purposes in ring also in Venezuela, Suriname, and the Guy- areas where animals share space with human anas, and taxonomically, it is considered part of populations (Bury 2006, Bernardes et al. 2014). the Phrynops geoffroanus complex (McCord et al. Turtle activity may follow a seasonal pattern, 2001, Rueda-Almonacid et al. 2007). Phrynops tube- which can be influenced by weather conditions rosus is similar in colour to the congeneric P. geof- such as air temperature, water temperature, and froanus, but females are larger than males (Rueda- precipitation (Souza & Abe 2001, Souza 2004, Almonacid et al. 2007). Knowledge of the activity Litzgus & Mousseau 2004, Lescano et al. 2008). Ac- pattern of the species is scarce (Souza 2004) and tivity may be assessed using capture data from the available data only relate to reproductive ecol- which it is possible to estimate when animals are ogy of this species (Rueda-Almonacid et al. 2007, more active and consequently more likely to be Rodrigues & Silva 2014) and natural history notes captured (Souza & Abe 2001, Lescano et al. 2008, (Rodrigues & Silva 2013a, 2013b). Germano 2014). Freshwater turtle activity is an This study aimed to describe the population important ecological characteristic that is poorly structure, activity, and sex ratio of Phrynops tubero- understood for Brazilian chelids (Souza 2004). sus in the Banabuiú River, a Brazilian semi-arid Caatinga areas have a dry seasonal forest with environment. We investigated sex ratio, density, xerophytic characteristics, having more than eight activity pattern, and size-class distribution of this dry months per year (annual precipitation < 1000 population. mm), and are found in north-eastern Brazil (Rodal et al. 2008). Four species of chelid freshwater tur- Materials and methods tles are found in Caatinga (Phrynops tuberosus, P. geoffroanus, Mesoclemmys tuberculata, and M. per- The study was conducted on the Banabuiú River on a 128 J.F.M. Rodrigues & J.R.F. Silva stretch near the village of Laranjeiras (5º17’45” S; tained from a weather station of Fundação Cearense de 38º51’54’’W, WGS84), Banabuiú, Ceará, Brazil (Fig. 1). The Meteorologia e Recursos Hídricos, 40 km away from study site has a small beach area and constant water flow study site. and depth throughout the year. Neustonic vegetation, The sex of each turtle was determined based on tail popularly known as “aguapé”, was abundant in the shal- length and vent position following Rueda-Almonacid et low portions of the river. Riparian vegetation was pre- al. (2007). Individuals with CL smaller than 12 cm were served, and there was a small bridge crossing the river classified as juveniles, because this was the size of the next to the sampling point. The river bottom was com- smallest male that could be confidently sexed based on posed of sand or stone, and its depth reached 2.5 m in tail characteristics. some deep parts. The sampled area was a river section We estimated population size and its confidence in- with dimensions of 41 m x 100 m (4,100 m2). Climate in terval with the POPAN method (open population) using the region is tropical and semi-arid with a mean tempera- MARK 7.1 software (White & Burnham 1999). We also ture of 26° to 28° C and rainfall of about 815.4 mm annu- present minimum (observed) population size, which was ally, mainly occurring from February to April (Instituto used to calculate turtle density (individuals per ha) in the de Pesquisa e Estratégia Econômica do Ceará 2012). The sampled area (4,100 m2) because the population size esti- Banabuiú River basin has a drainage area of 19,647 km2, mate from mark-recapture had a large confidence inter- comprising 13.37% of Ceará state (Companhia de Gestão val. We also calculated biomass (kg of turtle per ha) using dos Recursos Hídricos 2009). No other species of freshwa- the total mass of captured turtles. Despite not being the ter turtles was found in this site besides Phrynops tubero- ideal measurements, we believe it is also important to re- sus. port such minimum or observed estimates because no data are available for the size of any turtle population in the biome where the study was developed. A minimum estimate may be an important starting point to be applied in conservation actions. We used a Chi-square test to evaluate the sex ratio of the population, and a Spearman correlation test to relate the number of individuals captured monthly to the mean air temperature and also the total monthly precipitation (Souza & Abe 2001, Lescano et al. 2008). We recorded the total number of turtles captured in each hour of the day across the whole study as a measure of their daily activ- ity. Turtles were also classified into size class bands of 25mm (e.g. 0-25, 26-50, 51-75mm) in order to describe population size structure. We evaluated annual activity using the variation in the number of captures throughout the year. In order to construct a null model for this evaluation, in which cap-
tures in each month were directly proportional to the cap- Figure 1. Map of the study site, the Banabuiú River, ture effort of each month, we first obtained the total Ceará, Brazil. Black circle (●) indicates the sampling site. number of captures across the year. Next, we calculated the proportion of the effort performed in each month compared to the total effort of the study (250 person- We hand-captured animals by diving with mask and hours). The expected number of captures for each month snorkel between December 2011 and November 2012. was then calculated as the product of the total number of This is an efficient method to capture turtles and in gen- captures by the proportional effort in each month. The re- eral it shows no bias for the sex of captured animals (Ster- sults of this null model were compared with the actual ret et al. 2010). The sampling period was one day per data using a Chi-square test (Lescano et al. 2008). If there month, usually over eight hours (08:00 – 16:00), and con- were a significant variation in the activity between stant throughout the entire study duration. A group of months during the year, we would expect to find a devia- three people conducted hand-captures, and a total cap- tion from this null model. Analyses were performed in ture effort of 250 person-hours was performed. the software R ver. 2.13.0 (R Development Core Team We measured straight carapace length (CL) using a 2013). 300 mm analogue calliper (accuracy of 0.05 mm). The cap- tured turtles were also weighed on a digital scale with an accuracy of 1.0 g. The animals were marked in accordance Results with Cagle (1939) and released at the point of capture at the end of each survey day. We also recorded air tem- We captured 134 individuals, 94 males, 24 females, perature (taken 1 m above the ground) for each capture using a thermohygrometer. This recording was per- and 16 juveniles; the total number of captures was formed as soon as we left the water with a captured tur- 158 (Fig. 2). The number of individuals captured tle. Total precipitation of each sampling month was ob- did not differ by month throughout the year (χ2 = Population structure of Phrynops tuberosus 129
Figure 2. Number of males, females, and juveniles of Phrynops tuberosus captured between December 2011 and November 2012 (recaptures in- cluded) in the Banabuiú River, Ba- nabuiú, Ceará, Brazil.
Figure 3. Size classes of individuals of Phrynops tuberosus captured in the Banabuiú River, Ceará, Brazil.
Figure 4. Number of captured indi- viduals of Phrynops tuberosus in the Banabuiú River, Ceará, Brazil, per hour during the day. Each time represents an interval of one hour (e.g. 08:00 = 08:00 – 08:59).
15.47, df = 11, p = 0.16). The sex ratio was 3.92:1 ranged from 29 to 42o C when turtles were cap- male: female, which represented a significant de- tured. There was neither a correlation between the parture from 1:1 (χ2 = 41.52, df = 1, p < 0.001). number of captured turtles and air temperature (r The 200-225 mm and 225-250 mm size classes = - 0.31, p = 0.35, n = 9) nor precipitation (r = - 0.32, were the most common (Fig. 3). Air temperatures p = 0.31, n = 12). Turtles were captured almost 130 J.F.M. Rodrigues & J.R.F. Silva equally throughout the day (Fig. 4). 2013). The turtle’s life history traits, such as low We recaptured 18 animals, three females, 11 mortality in adulthood, low recruitment of young, males, and four juveniles. Recapture intervals and a high investment in maintenance and growth ranged from one to nine months. The population’s could explain this pattern (Congdon & Gibbons size was estimated at 574.38 individuals (CI = 1990). Higher rates of predation on young indi- 345.68 – 1050.18). The population density based on viduals may also contribute to the observed distri- our observed (minimum) population size (134 in- bution (Verdon & Donnelly 2005). However, de- dividuals) was 327 ind / ha, and had a biomass of spite the low proportion of juveniles in the total 268.75 kg / ha. sample (approximately 12%), the high minimum density and population size estimates may indi- cate that the P. tuberosus population from Ba- Discussion nabuiú is healthy. Understanding if this status is consistent for other freshwater turtles in the Caat- We found a male-biased population of Phrynops inga would be a main goal of a conservation pro- tuberosus in the Banabuiú River in Caatinga. Such ject focusing on turtles in this biome, which natural history and ecological data are essential should include population structure studies as a for conservation projects and further empirical starting point. studies (Bury 2006). Deviations in the sex ratio There was no annual or daily variation in the may be the result of sampling flaws, behavioural activity pattern or capture rates for P. tuberosus differences between the sexes, and differences in and these were also independent of the climatic maturation time of males and females, among data evaluated (air temperature and precipitation). other factors (Gibbons 1990, Lovich and Gibbons Other studies, such as Souza & Abe (2001), Souza 1990). A biased sex ratio is common in turtles in (2004), Litzgus & Mousseau (2004), and Lescano et general (Gibbons 1990, Verdon & Donnelly 2005, al. (2008) showed differences in the activity of tur- Germano & Rathbun 2008, Bujes et al. 2011), but tles. The lack of influence of air temperature on the not in Brazilian chelids (Souza & Abe 2001, Brito et activity pattern is consistent with Lescano et al. al. 2009, Marques et al. 2013). Capturing turtles by (2008), but in contrast to Souza & Abe (2001). For diving generally shows no tendency toward de- P. tuberosus, water temperature could be a better viations in the proportion of males and females predictor of their activity, as for H. tectifera (Les- captured (Sterret et al. 2010). Hence the sampling cano et al. 2008). Future studies evaluating this re- method used herein was not responsible for the lationship could be important. The consistency in operational biased sex ratio we found. According water depth and flow rate at the study area to Gibbons (1990), this male-biased sex ratio could throughout the year may also explain the lack of also indicate that males are more active than fe- relationship between capture rates and environ- males, but this hypothesis would require using te- mental variables, because turtles tend to respond lemetry to understand home ranges and specific behaviourally to changes in habitat characteristics habitat uses. (Cash & Holberton 2005). Captures occurred al- Differences in mortality rate between sexes most equally through the day, and only the inter- may also cause deviations in the sex ratio of the val 08:00 – 08:59 presented a low capture rate (Fig. population. Female mortality on unpaved roads 4). This difference is probably due to a “burning next to the studied area could be a possible expla- in” phase of the capture method used, when the nation for the biased sex ratio found in the present collectors were still getting used to the water con- study, although it was not systematically esti- ditions, such as transparency, and forming a mated. Populations of freshwater turtles near search image of turtles. highways and roads tend to have a higher propor- Population density and biomass were rela- tion of males, because females are run over more tively high in comparison to other estimates for often when leaving the water to look for nesting populations of riverine South-American chelids, sites (Aresco 2004, Steen & Gibbs 2004, Gibbs & such as Hydromedusa tectifera (153 individuals / ha; Steen 2005, Steen et al. 2006). Lescano et al. 2008) and Phrynops geoffroanus (345 This population consisted mainly of adults, a kg / ha; Rueda-Almonacid et al. 2007). The popu- characteristic commonly found in turtle popula- lation size estimate from the capture-mark- tions (e.g. Souza & Abe 2001, Brito et al. 2009, Bu- recapture method also reinforced the high abun- jes et al. 2011, Famelli et al. 2011, Marques et al. dance of P. tuberosus in the Banabuiú River. The Population structure of Phrynops tuberosus 131 absence of other potentially competing turtle spe-
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