NORTH-WESTERN JOURNAL OF 10 (1): 143-148 ©NwjZ, Oradea, Romania, 2014 Article No.: 131521 http://biozoojournals.ro/nwjz/index.html

How tuberosus (Testudines: ) reproduce in the Brazilian Caatinga?

João Fabrício Mota RODRIGUES1,3,* and José Roberto Feitosa SILVA2,3

1. Núcleo Regional de Ofiologia da Universidade Federal do Ceará (NUROF-UFC), Avenida Humberto Monte S/N – CEP 60455-760, Campus do Pici, Fortaleza, CE, . 2. Laboratório de Histologia – Universidade Federal do Ceará, Centro de Ciências, Avenida Humberto Monte S/N – CEP 60451-970, Campus do Pici, Fortaleza, CE, Brazil. 3. Programa de Pós-Graduação em Ecologia e Recursos Naturais – Universidade Federal do Ceará, Centro de Ciências, Avenida Humberto Monte S/N – CEP 60455-760, Campus do Pici, Fortaleza, CE, Brazil. *Corresponding author, JF.M. Rodrigues, Tel: (85)33669801, E-mail: [email protected]

Received: 26. August 2013 / Accepted: 1. November 2013 / Available online: 28. December 2013 / Printed: June 2014

Abstract. Caatinga has a semiarid climate with strong seasonality and long periods of drought, which should require adaptations in the in the region. Hence, we studied how the freshwater species , a very water dependent animal, deals with these adversities. The present study aimed to evaluate the influence of seasonality on nesting sites, hatching period and to report and discuss the use of secretive habitat by hatchlings for the freshwater turtle species P. tuberosus, from central hinterland of the state of Ceará. Data collection occurred in the Cedro water reservoir, located in Quixadá-CE, Brazil, between October 2011 and September 2012. We measured nests (n = 30) and hatchlings (n = 24) of the studied species. Nests were always found in shaded areas. Hatchlings were more abundant in the rainy season and showed cryptic behaviour. We observed that the life history traits of these were related to the rainy season in the region.

Keywords: Life History, habitat use, freshwater , adaptations, reproductive traits, seasonality.

Introduction Ferreira Júnior & Castro 2010, Rasmussen & Litzgus 2010, Turkozan et al. 2011, Zare et al. 2012, Caatinga is a physiognomy found in Brazilian Pignati et al. 2013). Hence, nest site selection is North-east, a semiarid region, and it is character- part of the habitat use in chelonians. ised by high temperatures and strong climatic sea- Vegetation cover and distance to water bodies sonality, because the rainy season is unpredictable are factors influencing the nesting sites (Bujes and short compared to the long dry season (Prado 1998, Molina 1998, Silva & Vilela 2008, Pignati et 2003). Since the production of viable offspring for al. 2013). Rainfall is another important factor that future generations is mandatory to improve or- is usually synchronic with the nesting and hatch- ganisms’ fitness (Stearns & Roff 2003), species liv- ing periods in turtles (Souza 2004). According to ing in Caatinga needs adaptations to overcome the this author, nests are built at the end of the dry adversities provided and, then, reproduce. Hence, season, and hatchings coincide with the beginning aquatic species, as freshwater turtles, can repre- of the rainy season, when the amount of resources sent good models to study these adaptations. Life in the environment is greater. Souza (2005) em- history traits of these animals, as nesting sites and phasises the importance of precipitation for the hatching time, should be influenced by these envi- distribution of freshwater turtle species in Brazil ronment characteristics. and shows that there is greater richness of these Parental care of the clutch is rare in Testudines animals in areas with higher rainfall. (Molina 1992) being known for flaves- Even with favourable environmental re- cens (Iverson 1990) and for polyphemus sources, having eggs hatch still does not guarantee (Grosse et al. 2012). Nevertheless, the selection of success since the mortality in this phase is very sites for nesting represents an important parental high in these animals. Hatch predation by fish investment in their young, because it increases the (Gyuris 1994, Blamires & Spencer 2013), ants odds of hatching and development of offspring, (Parris et al. 2002), birds (Janzen et al. 2000) and decreases the incubation time of the eggs, dimin- snakes (Perez-Heydrich et al. 2012) contribute to ishes nest predation and influences the sex ratio of the very high hatchling mortality of turtles the clutch (Packard et al. 1987, Wilson 1998, (Ferreira Júnior 2009, Perez-Heydrich et al. 2012). Hughes & Brooks 2006, Ferreira Júnior 2009, Adult turtles use more open and exposed portions 144 JF.M. Rodrigues & J.R.F. Silva of the habitat than the hatchlings which are more from the shore as water transparency allowed us to see secretive than adults in to avoid predators the bottom of the reservoir (approximately 50 cm depth (Jennings 2007). and 15 m away from the margin). These searches for young were conducted every month in the same area, Phrynops tuberosus (Peters, 1870) is a freshwa- where most of the nests were found. ter chelid turtle that inhabits the north and north- Individuals were measured (Carapace Length) with eastern regions of Brazil, also occurring in Caat- 300 mm analogue calliper, photographed, marked accord- inga areas (McCord et al. 2001, Rueda-Almonacid ing to Cagle (1939), sexed (following Rueda-Almonacid et et al. 2007). According to these authors, the unique al. 2007) and finally returned to their capture site. We re- source of information regarding P. tuberosus ecol- corded for each nesting site: presence / absence of vegeta- ogy, besides some natural history notes (Rodri- tion; occurrence of shading, provided by stones or / and plants; nest opening diameter, nest depth and distance to gues & Silva 2013), the species reproduction in the nearest water body. Since nest predation could have Amazonian rivers occurs during the dry season, influenced the diameter measures, we carefully removed and females are bigger than males in these popula- sediments of the nest surroundings until we observed a tions. On the contrary, we hypothesised that P. tu- regular opening, which was measured. Temperatures at berosus inhabiting semiarid regions of north- soil level in shaded and exposed sites were measured eastern Brazil reproduces in synchrony with the with a thermohygrometer in the afternoon (13 – 17 PM) short rain periods of this region. on June, July and August, in order to give us approxima- tions about the temperatures of these sites. Measurements Our study aims to provide information re- were taken in 20 minute intervals. Precipitation data were garding Phrynops tuberosus reproduction. Specific provided by Fundação Cearense de Meteorologia e Re- objectives are threefold: 1) to investigate basic nest cursos Hídricos (FUNCEME). ecology of Phrynops tuberosus 2) understand the in- The Chi-square test was used to assess whether the fluence of rainfall and temperature on the period number of hatchlings varied significantly throughout the of hatching and nesting site choice respectively of year. That test was also chosen to assess the selection of this species in the Caatinga region 3) report and the characteristics of spawning sites. There was no visual difference among the shade opportunities available. discuss secretive habitat use of P. tuberosus hatch- Therefore, it was expected that the number of nests found lings. in each types of shading were the same. We compared temperature in shaded and open sites with paired Stu- dent t test, because the variables had normal distribution Materials and Methods according to Shapiro-Wilk test. Variables were analysed at a significance level of p < 0.05. Analyses were per- The study was conducted at the Cedro water reservoir formed using the free software R ver. 2.13.0 (R Develop- (4°58'44''S and 39°04'09''W) which is located in the mu- ment Core Team 2011). nicipality of Quixadá (4°58'17''S and 39°00'55''W), in the centre of the state of Ceará (IPECE 2010). The water res- ervoir is an artificial pond that is connected to the Sitiá Results River. Cedro has a capacity of 125,694,200 cubic meters, a maximum depth of 16 meters and watershed of 210 km ². The area where the animals were more easily captured We measured 30 predated nests. Intact nests were has a local human population that enjoys the food re- not found. It was not possible to measure the sources provided by the water body, including fish and depth and diameter of all nests that were found shrimp. partially destroyed due to their conditions . We The climate is tropical and semi-arid, with an aver- could not measure the size or number of eggs due age temperature of 26 ° to 28 ° C and average annual rain- to the state of the eggshell fragments. Mean nest- fall of 838.1 mm. The rainy season usually occurs from ing opening diameter was 9.28 cm (1SD: 1.24, n = February to April, and the dry and rainy seasons are very well marked (IPECE 2010). The soil is shallow and rocky, 12), mean depth = 11.01 cm (1SD: 1.38, n = 8), dis- in general. The vegetation is characterised as a dense tance from the water = 6.73 m (1SD: 4.64, n = 30). thorny savannah (IPECE 2010). The surrounds of the Regarding the characterisation of spawning Cedro is covered by native vegetation. sites, all were found in shaded or partially shaded We conducted twelve field expeditions between Oc- areas, provided by rocks (74% of cases - n = 20) or tober 2011 and September 2012. These field trips occurred vegetation (22% of cases - n = 6). In only two sites, once every month, and they were formed by a group of the nests were found shaded by rocks and plants three people working continuously from 12 to 19 PM of one day. Nests were searched on land on the shore near simultaneously. Three spawning sites were found the spillway and near the restaurants (Rueda-Almonacid in the shade of a bridge. The vegetation found et al. 2007, Tortato 2007, Bujes & Verrastro 2008). We around the nests consisted mainly of grasses and looked for hatchlings in the aquatic environment as far sedges (Poaceae and Cyperaceae) and Myrtaceae, Phrynops tuberosus reproduction 145 which were abundant around the margins. There 2008, Schneider et al. 2011). Souza (2004), review- was no significant difference between the choice of ing the reproductive patterns of Brazilian freshwa- points of shading (χ2 = 2.98, P = 0.08). Mean tem- ter turtles, affirmed that the Brazilian turtles prefer perature in exposed sites was 42.4 ºC (1SD: 3.66, n to nest away from the water, despite that a defini- = 26, range: 35.8 – 47.2 ºC) and it was higher than tion of “far” has not been provided. The popula- in shaded ones (mean 35.16 ºC, 1SD: 1.59, n = 26, tion of from Reserva Biológica do range: 32.9 – 38.1 ºC) (t = 9.66, df = 25, p < 0.0001) Lami, Rio Grande do Sul, for example, follows this We captured 24 hatchlings of Phrynops tubero- trend and builds nests about 80 m away from wa- sus (mean 3.78 cm, 1SD: 0.24) throughout the year ter (Bujes 1998). Data found for P. tuberosus in (Fig. 01). The hatchlings were most commonly Quixadá, for P. geoffroanus and for H. tectifera found in the months of February and March, (Fagundes & Bager 2007; Silva & Vilela 2008, which corresponds to the rainy season in the re- Schneider et al. 2011) do not seem to support the gion. The distribution was found to be significant generalisation proposed by Souza (2004). (χ2 = 77; df = 11, p < 0.001) with an increasing con- According to Zare et al. (2012), the elevation of centration of P. tuberosus hatchlings during the nests, a direct measure of distance from water and rainy season. From the small size of the hatchlings margin slope, represents a trade-off between the found and the presence of umbilical scar, it can be risks of having the nest inundated and the risk of deduced that the period of hatching of these ani- hatchling’s predation and disorientation. Popula- mals was recent and within about one month. tions of Phrynops tuberosus from the Caatinga Thus, the period of hatching of the studied species should probably add other variables to this trade- occurs mainly between the months of January to off: higher insolation and risk of dehydratation of March, corresponding to the onset of the rainy disorientated hatchlings than in other regions. The season. high soil temperature in open areas and high tem- The hatchlings used several strategies to be- peratures found in Caatinga are probably more come less evident. They were always found in the dangerous to these young than in other less ex- water and hid near the edge of the weir (never far- treme environments. Hence, being closer to the ther than one meter), under floating macrophytes, water increases the chance of rapidly reaching the under rocks, under pieces of algae and even under aquatic environment and avoiding this primary trash such as plastic bags and pieces of discarded cause of death. clothing. The offspring of P. tuberosus also chose to The association between nests and grasses is remain immobile between stones (Fig. 2). common in species of the complex, which had been observed in the species P. hilarii and P. geoffroanus (Bujes 1998, Molina Discussion 1998, Silva & Vilela 2008). According to Turkozan et al. (2011), nesting close to vegetation may re- Mean nesting opening diameter of Phrynops tube- duce risk of predation. However, in our study, rosus found in Cedro were similar to the P. geof- nesting sites close to grasses seemed to be mainly froanus nests found in São Paulo Zoo (mean 9.6 related to shadow opportunity. Search for perma- cm) (Molina 1998) and in Guaporé river (mean 9.6 nently shaded areas is not common in the Phryn- cm) (Schneider et al. 2011). Nest depth was also ops geoffroanus complex. Phrynops hilarii, for exam- similar to this congeneric in the Paraná River ple, usually avoids nesting in sites with this fea- (mean 13.94 cm) (Silva & Vilela 2008) and in the ture, and P. geoffroanus prefers sites with partial Guaporé River (mean 12.6 cm) (Schneider et al. shading (Bujes 1998, Molina 1998, Silva & Vilela 2011). These similarities in nest characteristics are 2008). probably due to the similarities in size between A large proportion of shaded nests compared these two species. to studies in other regions can be attributed to the Distance between the nests of Phrynops tubero- high temperatures found in the exposed sites of sus and the water body was similar to that found the region. Ferreira Júnior et al. (2011) monitored for the species P. geoffroanus from Jupiá dam (eggs nest temperatures of Phrynops geoffroanus in the laid 8.2 m away from the water) and from the natural environment and found temperatures Guaporé River (5.3 m away), and to the Hydrome- range from 19 - 39 ºC in the hottest nesting site. dusa tectifera from Reserva Biológica do Lami (8.4 Temperature measurements from the banks of the m away) (Fagundes & Bager 2007, Silva & Vilela Cedro water reservoir found temperatures at soil

146 JF.M. Rodrigues & J.R.F. Silva

Figure 1. Numbers of hatchlings of Phrynops tuberosus captured between October 2011 and September 2012 (bars). The rainfall for the region was es- timated using the rainfall data from 1974 to 2012 (points).

Figure 2. Microhabitats used by hatchlings of Phrynops tuberosus. A: Piece of cloth under which a hatchling was found. B: Stones and gravel where a hatchling hid. C: Small P. tuberosus partially buried in sand and gravel. D: Hatchling hiding under macrophyte bank.

level of 40° C occurring daily between the hours of from which the predator sucks the egg contents.

1 p.m. to 3 p.m in open sites (mean 42.4 ºC). Shad- Salvator merianae is common in the semiarid region ing can assure the most suitable nest temperature. of Ceará (Vanzolini et al. 1980) and it was seen on Thus, higher temperatures seem to promote the the field trips. These lizards are known predators emergence of adaptations in the choice of nesting of turtle eggs (Bujes 1998, Goncalves et al. 2007, sites in order to overcome existing adversities. Tortato 2007). Locals also indicated the raccoon Predated nests presumably have been at- (Procyon sp.) as a possible predator of these eggs, tacked by the Argentine Black and White Tegu but it was not sighted during the field trips. (Salvator merianae; Teiidae). Eggs predated by this The relationship between the period in which species have a round cross-section in the eggshell the hatchlings were found and rainfall supports Phrynops tuberosus reproduction 147 the prediction of temporal synchrony between of microhabitat heat as a factor in determining hatching period and rainfall (Souza 2004) and em- habitat use by juveniles and adult turtles in re- phasises the importance of environmental charac- gions with a subtropical climate. Hiding under teristics on life history traits of freshwater turtles. macrophytes also would help to avoid predation According to Souza (2004, 2005), the distribution by birds, which are known hatchling predators of freshwater turtles and reproductive characteris- (Janzen et al. 2000). tics of these animals are closely related to rainfall. We concluded the distribution of rainfall in The increased amount of resources in the rainy the region influences hatching period, and high season is a major cause of the existence of this syn- temperatures, nest site selection of Phrynops tube- chronisation (Souza 2004). The need for appropri- rosus. In other regions with rainfall concentrated in ate values of soil moisture for the development of a few months and high temperatures, it is ex- eggs in the environment also reinforces the impor- pected that the freshwater turtles have responses tance of the rainy season (Packard et al. 1987, similar to those found in this study in relation to Ferreira Júnior 2009). the nest site selection and reproductive period. Rueda-Almonacid (2007) points out that the period of hatching of these animals in the Amazo- nian region roughly corresponds to the months of April to July, which did not correspond to that Acknowledgements. We thank IBAMA/SISBIO for the found in Quixadá. Hatching time in Amazonian license (32548-1), FUNCEME for providing weather data, turtles is highly influenced by the variation in CNPq for the fellowship given to J. F. M. Rodrigues, three anonymous reviewers that have helped us to improve the level of the Xingu River (Ferreira Júnior & Castro manuscript and all the friends that helped in the field 2010, Ferreira Júnior et al. 2011). Differences in survey. frequency of rainfall (less concentrated in the Amazon) could also be responsible for this differ- ence. In the marginal portion of the reservoir where References the hatchlings were found, no large fish or aquatic Blamires, S.J., Spencer, R.J. (2013): Influence of habitat and invertebrates, which could act as predators, were predation on population dynamics of the freshwater turtle found. However, large schools were seen in the georgesi. Herpetologica 69(1): 46-57. deep where adults were observed. These fish were Bujes, C.S. 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