Demography of Acanthochelys spixii (Testudines, Chelidae) in the Brazilian

Cerrado
Author(s): Habib J. Fraxe Neto, Marcela Ayub Brasil, Gabriel de Freitas Horta, Thiago Oliveira Barros,
Guth Berger Falcon, and Guarino R. Colli
Source: Chelonian Conservation and Biology, 10(1):82-90. 2011.
Published By: Chelonian Research Foundation
DOI: http://dx.doi.org/10.2744/CCB-0876.1
URL: http://www.bioone.org/doi/full/10.2744/CCB-0876.1

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Chelonian Conservation and Biology, 2011, 10(1): 8290

g 2011 Chelonian Research Foundation

Demography of Acanthochelys spixii (Testudines, Chelidae) in the Brazilian Cerrado

HABIB J. FRAXE NETO1, MARCELA AYUB BRASIL1, GABRIEL DE FREITAS HORTA1,
THIAGO OLIVEIRA BARROS2, GUTH BERGER FALCON2, AND GUARINO R. COLLI2
1

Programa de Pos-Graduacao em Biologia Animal, Universidade de Braslia, 70910-900 Braslia, DF Brazil

[hfraxe@senado.gov.br; chela_bio@yahoo.com.br; gfhorta@gmail.com];
2
Departamento de Zoologia, Universidade de Braslia, 70910-900 Braslia, DF Brazil [thiagoobarros@gmail.com; grcolli@unb.br]

ABSTRACT. We estimated demographic parameters for Acanthochelys spixii in Parque Nacional de

Braslia, Distrito Federal, Brazil, based on 4 years of data collection, and also analyzed the effects
of sex, temporal variation, and climatic factors on population dynamics. The adult sex ratio did
not vary significantly from 1:1. By using the Akaikes information criterion, selection of candidate
models constrained for climatic variables indicated that the interaction between total rainfall and
average air temperature from the previous month as well as recapture probability (p) on a
monthly basis explained most variation in demographic parameters, with a constant annual
apparent survival (W) value of 0.82. Recapture rates during the study period varied from 0.01 to
0.23 and, during the dry season, from 0.01 to 0.04. The monthly average population size was 30
adult turtles, with values between 10 and 35 adults over 4 years. The annual population growth
rates were 1.37 for 20052006 and 0.59 for 20062007. The small population size of Acanthochelys
spixii seems characteristic of chelids in the area, and maintaining it depends on preserving natural
ecosystems inside Parque Nacional de Braslia.
KEY WORDS. Reptilia; Testudines; Chelidae; Acanthochelys spixii; freshwater turtle;
demography; markrecapture; survivorship; Brazil; Cerrado
Demographic parameters are crucial aspects of
animal ecology and life histories, and one of the main
tools for biodiversity conservation (Vitt and Caldwell
2009). Robust data on turtle demography are critical for
effective management and conservation, especially if
impacts on population survival, such as anthropogenic
factors, are considered (Gibbons et al. 2001). For
management success, the complexity of turtle population
characteristics demands focus on selected demographic
data and also great care in analyzing estimated parameters. Indeed, population models now available demand
greater responsibility among researchers to perform the
necessary assessments so that the most appropriate
models are selected (Amstrup et al. 2005; Cooch and
White 2008). At the same time, to predict population
abundance or viability with high precision is a difficult
task, especially given the insufficient information on
species life histories (Huston 2002).
About 17% of the 328 known turtle species occur in
South America, including 8 families. The Chelidae has
the largest geographical distribution and is the most
species-rich family (19 of 22 described South American
species occur in Brazil) (Souza 2005). Knowledge of the
status of non-Amazonian turtles in Brazil is sparse,
especially for the Cerrado biome, which is one of the 34
world biodiversity hotspots (Myers et al. 2005). Six
species of chelids occur in the Cerrado (Colli et al. 2002):
Acanthochelys spixii, Chelus fimbriatus, Mesoclemmys
gibba, Mesoclemmys vanderhaegei, Phrynops geoffroanus, and Platemys platycephala. When considering the

incipient knowledge about non-Amazonian chelids

(Souza and Molina 2007), life history studies conducted
under natural conditions are important to inform conservation and management programs (Souza 2004). A
demographic analysis of Mesoclemmys hogei, the most
threatened Brazilian freshwater turtle (Tortoise and
Freshwater Turtle Specialist Group 1996b), highlighted
the importance of habitat preservation and concluded that
low survival rates are related to predation at initial
development stages (Moreira 2002). A long-term study on
Hydromedusa maximiliani estimated an annual population
growth of 1.012, which indicates a healthy population
because of the level of protection of the study site (Souza
1995; Souza and Abe 1997; Souza and Martins 2006;
Martins and Souza 2009).
Although there are no demographic studies on
Cerrado turtles, amphibian and lizard populations show
a tight association between demography and climate, a
consequence of cyclic reproduction (e.g., Wiederhecker et
al. 2003; Vasconcellos and Colli 2009). Demographic
studies of Cerrado species are warranted because 1) at
least 80% of the biome has been modified by human
activities (Dias 1994); 2) until 2008, the Cerrado had lost
about 48% of its native landscape, and only 2.89% of its
territory is adequately protected (Ministerio do Meio
Ambiente 2009); and 3) degradation of aquatic ecosystems in the Cerrado is ongoing (de Sa et al. 2003;
Nogueira et al. 2010).
Acanthochelys spixii (black spiny-necked swamp
turtle) (Fig. 1A, B), popularly known in Brazil as

FRAXE NETO ET AL. Demography of Acanthochelys spixii

83

Figure 1. Acanthochelys spixii in (A, EGabriel Horta) terrestrial and (B, EThiago Barros) aquatic habitats. Study site, Lagoa do
Henrique, during (C) the rainy season and (D) dry season (EGabriel Horta). (E) Parque Nacional de Braslia, completely surrounded by
the heavily urbanized matrix of the city of Braslia. White pin depicts Lagoa do Henrique (Google Earth).

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cagado-preto, is a small (maximum carapace length

around 170 mm) semi-aquatic turtle that inhabits
freshwater and terrestrial habitats associated with temporary swamps, slow moving waters, heavily vegetated
aquatic bodies, and small rivers (Damato and Morato
1991; Tortoise and Freshwater Turtle Specialist Group
1996a). In captivity, these animals display little activity
during the cold season, which suggests hibernation in the
wild (Molina and Rocha 1990). Acanthochelys spixii has a
broad distribution in South America, and occurs from
Uruguay and Argentina through the Brazilian states of
Rio Grande do Sul, Parana, Sao Paulo, Minas Gerais, and
Distrito Federal (its northernmost limit) (Rhodin et al.
1984; Brandao et al. 2002). In Brazil, A. spixii inhabits
areas with severe winters in the southern states to areas
with a mean annual temperature of approximately 22uC.
Suitable habitats for the species include contact zones
between open (e.g., Cerrado) and closed (Atlantic rainforest) formations (Souza 2005). The species was
considered vulnerable in Uruguay, because of its nearthreatened International Union for the Conservation of
Nature (IUCN) status, low abundance, and vulnerability
to environmental changes (Carreira et al. 2007). In 1998,
the Brazilian state of Sao Paulo listed A. spixii as
vulnerable (State Decree 42.838/98). Herein, we estimate
demographic parameters and model the effects of sex and
climatic variation in a population of A. spixii from the
Cerrado biome of central Brazil, based on 4 years of
markrecapture research. We hypothesize a significant
association of demographic and climatic parameters,
given previous studies with other herpetological fauna
in the region.
METHODS
Study Site. Parque Nacional de Braslia (PNB) is
the largest fully protected area of Distrito Federal, Brazil,
with 42.389 ha. It integrates the Man and Biosphere
Program of the United Nations Educational, Scientific, and
Cultural Organization (UNESCO-MAB) Biosphere Reserve core area of the Brazilian Cerrado (UNESCO 2001)
and protects different vegetation types, such as cerrado
sensu stricto, campo sujo, campo limpo, and gallery
forest (Eiten 1972). We studied a population of A. spixii
that inhabited a pond, Lagoa do Henrique (lat 15u41.2799S,
long 47u56.4559W). During the rainy season, this rich
lentic system, given its diversity and abundance of algae,
macrophytes, odonates, and anurans, reaches an area of
approximately 4 ha (Fig. 1C, D). Fifty years after its
creation, PNB is under strong anthropogenic pressures
associated with a growing urbanization process since the
Brazilian capital moved from Rio de Janeiro to Braslia:
from 1954 to 1998, 73% of the original cover of Cerrado in
Distrito Federal was lost (UNESCO 2001). Today, PNB is
completely surrounded by urban and rural areas in Braslia
(Fig. 1E). Climate in the region is highly seasonal: a wet
season from October to April concentrates almost all of the

15002000 mm annual precipitation; the dry season occurs

from May to September, with some months receiving
literally no rain; the average air temperature is relatively
constant throughout the year, approximately 20u22uC; the
climate is semihumid and hot (Nimer 1989).
Field Methods. The turtles were captured by
aquatic funnel traps baited with sardines. For each
captured turtle, we recorded the following: body mass
with a 5 g Pesola spring scale; midline carapace length,
maximum carapace width, midline plastron length,
maximum plastron width, and maximum shell height,
with 0.01-mm digital Mitutoyo calipers; sex; predation
scars; and presence of leeches. Each captured animal was
marked by marginal scute notching (Cagle 1939) and
released at the place of capture. Sex was determined
based on plastron and cloacal characteristics (Molina and
Rocha 1990; Metrailler 2005); all captured animals but
one, which was excluded from demographic analyses,
were adult. Water-level variations were measured (with a
1.0-cm ruler, positioned at the center of the pond) to
investigate their association with total rainfall in the
previous month. Throughout the study period, the
sampling effort was the same: the traps were checked at
least twice per week, and bait was renewed every 15 days.
The study was conducted from the first day of 2005 to the
last day of 2008 (48 months), a total capture effort of
427 days.
Demographic Analyses. Before the capture
recapture study, 3 turtles of this population were found
dead, with signs of bird predation. One of the turtles,
preyed upon by a common caracara (Caracara plancus),
was a gravid female and its remains consisted solely of
the shell with 4 eggs. During the capturerecapture
period, 2 marked females and 1 marked male also were
found dead along the pond margins, seemingly eaten by
caracaras. Furthermore, 1 marked female drowned inside
a trap and 1 nonmarked female was found dead at the
pond margins, with egg remains inside its shell. The shells
of the dead turtles as well as the drowned female were
deposited in the Colecao Herpetologica da Universidade
de Braslia.
Markrecapture data, based on individual monthly
encounter histories of adult turtles, were used to estimate
basic demographic parameters by using MARK v. 5.1
software, which allows for covariate (such as climatic
factors) and group (e.g., sex) influences on parameter
estimates (White and Burnham 1999). MARK also
provides model selection based on the Akaike information
criterion (AIC), an information theory tool for achieving
an optimal balance of model fit, indicated by the model
likelihood, and precision, indicated by the number of
parameters (Cooch and White 2008). Apparent survival
(W) and recapture probability (p) were estimated under the
standard Cormack-Jolly-Seber (CJS) model for open
populations, in which changes such as gains (in situ
reproduction and immigration) and losses (death and
emigration) are expected to occur. The CJS model is

FRAXE NETO ET AL. Demography of Acanthochelys spixii

85

Table 1. Body measurements of adult Acanthochelys spixii in Parque Nacional de Braslia, Brazil, according to sex, with analysis of
variance results. Data are mean SD.
Measurement
Body mass (g)
Shell height (mm)
Carapace length (mm)
Carapace width (mm)
Plastron length (mm)
Plastron width (mm)

Females (n 5 23)
330.87
49.54
139.78
93.96
118.76
62.72

50.67
2.93
5.55
3.76
5.38
2.92

based on recaptures of previously marked animals and on

4 assumptions: 1) equal catchability; 2) survival homogeneity; 3) marks are correctly recorded and are neither
lost nor missed; and 4) sampling periods are instantaneous, and individuals are released immediately after
sampling (Amstrup et al. 2005). Assumptions 3 and 4
were not violated by virtue of our sampling regime. We
tested assumptions 1 and 2 through goodness-of-fit (GOF)
tests by using software U-CARE v. 2.3 (Choquet et al.
2002). The most parameterized (global) model, in which
apparent survival (W) and recapture probability (p) varied
with both sex (s) and time (t), was used as a general global
model (W (s*t) p (s*t)) in the GOF tests. After confirming
assumptions 1 and 2 of the CJS model via GOF tests, we
progressively fit simpler models (Lebreton et al. 1992) to
achieve the best survival and recapture estimates by using
the fewest parameters (Cooch and White 2008). Model
selection was based on AIC corrected for small sample
sizes (AICc), where the best model is the one with the
lowest AICc and the largest AICc weight (WAICc).
Differences in AICc between the best model and the
model being evaluated (DAICc) also were used in model
selection: when DAICc , 2, we assumed that there is
substantial support for the model under consideration; if
4 , DAICc , 7, we assumed that there was considerably
less support; and if DAICc . 10, then there essentially
was no support (Burnham and Anderson 2002). To assess
the importance of parameters, we built several candidate
models by testing the effects of sex and time in apparent
survival and recapture probabilities, and also the effects of
climatic factors (rainfall and average temperature), both
in the current and previous month. Climatic data were
obtained from Estacao Meteorologica do IBGE, 30 km
away from the study site. To constrain models, monthly
rainfall and temperature were added as linear functions of
recapture probability (Burnham and Anderson 2002).
Moreover, to estimate data overdispersion, we calculated
the variance inflation factor (c ) of the global model,
which, if . 1, required some adjustments in AICc values.
Monthly variation of population size (N) was
estimated by the Jolly-Seber (JS) model for open
populations, implemented in module POPAN of software
MARK (White and Burnham 1999). The JS model
enables calculation of abundance parameters derived
from estimates of the marked to the noncaptured animals
by using a maximum likelihood approach. All of the
estimators rely on marked population size estimation:

Males (n 5 33)

50.65
57.96
44.47
42.57
89.26
125.47

247.73
43.91
128.79
86.32
105.97
54.14

36.83
2.56
6.40
4.66
4.70
2.75

p
,
,
,
,
,
,

0.001
0.001
0.001
0.001
0.001
0.001

survival estimators are calculated from the ratio of

marked animals present at time j + 1 to those present at
time j. For survival estimation, if there is no distinction
between losses as an effect of either death or permanent
emigration, we named this estimator apparent survival
for both CJS and JS models. Beyond the 4 assumptions of
the CJS models, JS models also require that all emigration
is permanent and that the study area remains constant
(Amstrup et al. 2005).
To estimate population growth rate (l), we used the
Pradel model implemented by software MARK, in which
apparent survival (W) and recapture probability (p) are
calculated in addition to l. The Pradel model is an
extension of the JS model that considers the capturehistory data in reverse time order to infer the recruitment
process and its proportional reflection in l. In this case, it
is crucial to keep in mind that l is not necessarily
equivalent to the growth rate of the entire population; it is
only the realized growth of the sample from which the
encounter histories were generated. This consideration is
important because uncertainty in results demands caution
when implementing conservation strategies (Cooch and
White 2008). Model selection was based on AICc, as
described for the CJS model estimators. In addition, l for
the first and last intervals are inestimable, a factor that
poses limits on conclusions about population stability in a
relatively short study period such as ours (Williams et al.
2002; Cooch and White 2008).
RESULTS
During the 48 months of the study, 56 adult turtles
(23 females and 33 males) were individually marked and
captured 174 times, with 43 individuals being recaptured
at least once. The sex ratio among marked animals was
slightly male biased, at 1.43:1, which did not differ
significantly from 1:1 (x2[1] 5 1.79; p 5 0.18). Adult
females were significantly heavier and larger than males
(Table 1). Among 174 capture events, leeches (Batracobdella sp.) were observed on turtles on 102 occasions; 1
male turtle was captured with 38 leeches attached to its
body. The water level varied up to 116 cm and was
positively associated with total rainfall in the previous
month (rS 5 0.66, p , 0.001).
The overall goodness-of-fit test detected no general
significant deviation from fit of the global model (Ws*t, ps*t)
to the CJS model (x2[79] 5 29.91; p . 0.99), so the CJS

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Table 2. Five best candidate models of Cormack-Jolly-Seber (CJS) model for monthly apparent survival (W) and monthly recapture
probabilities (p) in Acanthochelys spixii. AICc 5 Akaikes information criterion for small samples (lower values meaning better model
fit); DAICc 5 difference between the AICc of the current and the best model (model 1); WAICc 5 weight of fit for each model; K 5
number of estimated parameters. Subscripts: s, sex variation (males, females); t, time variation (i.e., 48 months); s*t, variation in both;
rain and temp, variation in rainfall and average temperature of the current month; rain-1 and temp-1, variation in rainfall and average
temperature of the previous month; month, monthly variation (i.e., equal survival or recapture probabilities for each month of the
year); and (.), the parameter is held constant.
Model
1.
2.
3.
4.
5.

W., p[(rain-1)*(temp-1)](t)
W., p[(rain-1)*(temp-1)](month)
Ws, pmonth
W., p(temp-1)(month)
W., pmonth

AICc

DAICc

WAICc

Deviance

728.15
730.78
731.13
743.57
778.71

0.00
2.63
2.98
15.42
50.56

0.6690
0.1798
0.1509
0.0003
0.0000

5
5
14
3
13

595.50
601.13
580.61
618.19
580.68

model could be used with our data. The specific tests for
the CJS model assumption of equal catchability provided
no evidence of a trap dependence effect for males (test
2.Ct, x2[13] 5 13.64, p 5 0.40) or females (test 2.Ct,
x2[9] 5 2.46, p 5 0.98). Likewise, the specific tests for the
assumption of homogeneous survival provided no evidence
for the presence of transients among males (test 3.Sr,
x2[10] 5 3.40, p 5 0.97) or females (test 3.Sr, x2[3] 5 0,
p . 0.99). The assumption of homogeneous survival was
not violated either for males (test 3.Sm, x2[6] 5 1.64,
p 5 0.95) or females (test 3.Sm, x2[4] 5 0.63, p 5 0.96).
Because the overdispersal value c, calculated as the x2 of
the overall model divided by its degree of freedom, was
0.38, we set the c value as 1.00, not adjusting the AICc, and
ran the models (White and Burnham 1999).
CJS model analysis indicated that the 3 best models
had a similar power in explaining the encounter history
data, because DAICc , 3 for each model (Burnham and
Anderson 2002). The 3 models accounted for almost
100% of the Akaike weight (Table 2). Given the amongyear variation in Cerrado environmental factors (Fig. 2A),
models with capture probability that depended on the
interaction of prior monthly rainfall and temperature,
incorporated as constraints, represented 85% of the
Akaike weight (Table 2, models 1 and 2). In addition,
constraining the time variation of recapture probability to
a monthly basis, i.e., when considering equal recapture
probabilities for each month of the year, also contributed
to model fit (Table 2, models 2 and 3). This indicates a
recurrent pattern of recapture probabilities associated with
the same month in different years.
To incorporate model uncertainty in the parameter
estimation, we calculated W and p under a modelaveraging approach, which consisted of averaging parameters of candidate models weighted by their normalized
AICc. Model averaging for monthly apparent survival (W)
was 0.984, a constant value for both males and females
(95% CI, 0.9690.992; SE 5 0.005). Annual survival
probability, calculated as the monthly survival estimate
raised to the 12th power, was 0.823. Recapture probability
(p) values were low and varied from 0.005 to 0.232, with
similar patterns over the years. From May to September of
every year, a time period that coincides with the dry

season, we rarely captured a turtle, and p varied from

0.005 to 0.044 (Fig. 2B).
Population-size estimates under the JS model in
module POPAN of program MARK, which assumes only

Figure 2. (A) Monthly rainfall (dashed line) and average air

temperature (continuous line) in Distrito Federal, Brazil,
between January 2005 and December 2008. The gray shading
indicates dry periods (Source: Estacao Meteorologica do IBGE).
(B) Monthly recapture and (C) population size estimates with
standard errors of Acanthochelys spixii, from January 2005 to
December 2008.

FRAXE NETO ET AL. Demography of Acanthochelys spixii

Table 3. Five best candidate models for population growth rate

estimation (l) based on Pradel model analysis for Acanthochelys
spixii. (See Table 2 for definition of abbreviations.)
Model
1.
2.
3.
4.
5.

Ws*t, pt, lt
Wt, ps*t, lt
Ws, pt, lt
W., p., lt
Ws*t, p., lt

AICc

DAICc

WAICc

195.86
198.47
200.55
204.74
205.21

0.00
2.61
4.69
8.88
9.35

0.70
0.19
0.07
0.01
0.01

13
14
9
5
10

1 cohort, resulted in the best data fit by the model with

constant survival and time-dependent recapture probability: W., pt, pentt. Because constraints in the probability of
entrance of new individuals (pent) via both immigration
and recruitment (birth) make no biological sense, this
parameter of the JS model was assumed to vary freely
over time. Average monthly population size was 30.4,
with values that varied from 10 to 35 adult individuals
(Fig. 2C).
Annual population growth rates estimated under the
model-averaged AICc-ranked Pradel models resulted in 2
values: 1.37 0.19 SE (95% CI, 1.011.74) for the
20052006 interval and 0.59 0.08 SE (95% CI, 0.43
0.73) for the 20062007 interval. The top-ranked model
incorporated survival varying with time and sex, and both
recapture probability and population growth rate with
time variation Ws*t, pt, lt with 70% of the Akaike weight
(Table 3).
DISCUSSION
Adult sex ratio represents a fundamental demographic parameter because the proportion of sexes may affect
population dynamics (Lovich 1996). Unbalanced ratios
are known for many wild turtle populations, as well as
biased sampling associated with season of capture and
trapping techniques (Gibbons 1990). Although temperature-dependent sex determination may also influence
turtle sex ratios (Schwanz et al. 2010), all chelids
probably have genotypic sex determination (Janzen and
Paukstis 1991). Moreover, interpreting causes of adult
turtle sex ratios depends on sufficient population records,
but demographic data exist for few turtle species
(Gibbons 1990). In natural populations of Emydura
macquarii, adult sex ratios were strongly male biased in
9 of 11 populations examined and even an analysis
adjustment with matched cohorts was insufficient to
explain the strong male bias (1.22.9) in 5 of the 9
populations (Georges et al. 2006). In the longest
demographic research conducted in Brazil for a chelid,
a 1:2 female-biased ratio was reported for Hydromedusa
maximiliani in the Atlantic Forest, apparently driven by
differential mortality and/or unknown natural factors
(Martins and Souza 2009). As in our study, the sex ratio
of Mesoclemmys hogei did not differ significantly from
1:1 (Moreira 2002). In reptile populations with genotypic

87

sex determination, a 1:1 sex ratio is expected to occur

(Janzen and Paukstis 1991). We believe that no sampling
bias associated with season or trap methods affected our
results, because our study was conducted continuously
across seasons, and GOF testing for trap dependence was
not significant for either sex. Because sex ratios may
differ among years (Gibbons 1990), it is important to
continue efforts to monitor changes in this population,
especially when considering its small size.
CJS constrained models 1 and 2, which accounted for
85% of the Akaike weight, that assume that recapture
probabilities depends on the interaction of previous
monthly total rainfall and average air temperature.
Moreover, among the 3 best models, 2 considered
recapture probability estimates that vary on a monthly
basis. This recurrent pattern of monthly recapture
probability, as well as the power of constrained models
based on climatic data, seems related to the very regular
weather patterns of the biome. Indeed, the Cerrado has the
most predictable climate among Brazilian biomes (Nimer
1989). Turtle activity patterns are often associated with
climate, with rainfall and air temperature being the most
influential parameters in many species (Souza 2004). The
higher capture rates during the rainy season were
probably associated with rising water levels. Rainfall in
the previous month and water levels were significantly
correlated and, as the pond continually rises during
raining periods, odonate abundance and richness proportionally increase (Habib J. Fraxe Neto, pers. obs.).
Odonates are the most important prey for A. spixii at the
study site (Brasil et al. 2011 [this issue of CCB]).
Low values of capture probability, as in our
estimates, could result from emigration, hibernation,
idiosyncrasies of Cerrado turtle populations, or an
interaction of these factors. The study site is limited to
a lentic portion of about 4 ha. However, population spatial
boundaries are generally vague and hard to define
(Williams et al. 2002), and it is possible that individuals
use habitats beyond the pond or migrate to other aquatic
habitats nearby (see Souza 2004; Horta 2008). Observations that corroborate this hypothesis include 1) the
population inhabits a temporary pond that was completely
dry just before the 2003 rainy season; 2) after measurements, turtles released at the pond margins often sought
refuge in terrestrial vegetation instead of going directly to
the water, where they were initially captured; 3)
occasionally, we found animals at least 500 m away
from the pond. Another hypothesis is hibernation during
colder months (Cerrado dry season), as recorded in other
studies (Molina and Rocha 1990). Radiotelemetry and/or
studies of gene flow may be useful to test these
hypotheses (Harless et al. 2009). Another explanation
for low recapture probabilities is idiosyncrasies of
chelonian populations in the Cerrado. Relatively high
numbers and ease of capture characterize turtle populations in other Brazilian biomes, such as Atlantic rainforest
(Martins and Souza 2009) and Amazonia (Fachn-Teran et

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al. 2003). However, populations with sufficient numbers

to provide robust demographic estimates are often hard to
locate in the Cerrado (F.L. Souza, pers. comm.). Moreover, most A. spixii in the Cerrado are small or medium
sized, with no economic importance for humans, and,
because of that, it is even harder to obtain information
about populations.
The 2 best CJS models assumed constant apparent
survival (W), and model averaging for the annual parameter
estimate was 0.823, with no between-sex variation during
the study period. Despite the strong wetdry seasonality of
the Cerrado, there was no evidence for the influence of
climate on survival, as recorded elsewhere (Converse et al.
2005). High levels of adult survival are particularly
desirable in management plans of species with life histories
that make them prone to overexploitation because of
increased adult mortality and its resulting low probability
of reproductive success (Congdon et al. 1993; Heppell
1998). In Terrapene ornata, high adult survival is necessary
to attain 30+ years of longevity (Converse et al. 2005).
However, some researchers argue that differences in
exploitation vulnerability should be evaluated on a species
by species basis, so that species with fast life histories
may provide some level of adult harvest (Fordham et al.
2009) and that turtles may respond to changes in
demographic processes in ways not predicted by common
demographic models (Spencer and Janzen 2010). Chelodina rugosa, a fast-growing, early-maturing, and highly
fecund species, subject to indigenous harvesting and pig
predation, may compensate for low adult survival rates
with elevated hatchling survival, smaller female size at
maturity, and increased female postmaturity growth
(Fordham et al. 2009).
The 2 values for annual population growth (l), 1.37
for 20052006 and 0.59 for 20062007, must be
interpreted with caution because of the short period of
estimable time intervals. However, when considering the
small population size, these estimates suggest that the
population is either persisting at low abundance or
declining in numbers. Therefore, continued estimation of
population growth and size is warranted. The monthly
population size curve (Fig. 2C) stabilized after August
2005 and remained at approximately 30 individuals. This
figure is relatively small compared with 2 studies with
chelids endemic to the Brazilian Atlantic rainforest. In
Sao Paulo, the estimated abundance of Hydromedusa
maximiliani was 235 (95% CI, 921016) from 1993
1994 and 318 (95% CI, 1011842) from 20032006
(Martins and Souza 2009). In Minas Gerais, the
population size of Mesoclemmys hogei at the Carangola
River varied between 6 and 132 turtles from April 2001
to March 2002 (Moreira 2002). In contrast, Amazonian
turtles are much more abundant: Fachn-Teran et al.
(2003) reported 2458 captures of adult Podocnemis
sextuberculata from September 1996 to August 1998 at
Reserva de Desenvolvimento Sustentavel Mamiraua.
These numbers highlight the importance of finding and

studying populations of chelids in Cerrado, given their

relatively low abundance.
Predicting demographic estimates must account for
habitats, because size and environmental and ecological
aspects of habitat patches may influence demographic
values (Huston 2002). An urban matrix isolates PNB, and
anthropogenic pressures on this protected area include a
large waste dump (Lixao da Estrutural), which attracts
feral dogs, rats, and birds of prey that probably are
responsible for depredation of at least 7 turtles at this
study site since 2004. In C. rugosa and E. macquarii,
which have predation by feral pigs and foxes, long-term
population declines were not compensated even by higher
adult survival rates (Fordham et al. 2006). Knowledge
about habitat and its biota should be used to manage
natural populations in a sustainable way (Huston 2002).
As myriad fragments now distributed along vast portions
of the original Cerrado landscape, the result of accelerated
conversion into agricultural and urban areas, PNB is an
island of biodiversity, and its reptile fauna may well
resemble the original communities that lived therein
(Rodrigues 2005). Our results indicate that the population
of A. spixii inside PNB is relatively stable, within the
limits of our sampling, therefore, this conservation unit is
fulfilling its goals. The preservation of natural ecosystems
inside PNB is pivotal for the maintenance of A. spixii in
the Distrito Federal region.
ACKNOWLEDGMENTS
We thank Mariana Mira Vasconcellos for her
valuable assistance with Program MARK. PNBs Administration was of immense help in all moments and we
especially thank Elmo Monteiro da Silva, Darlan Padua,
and Maria Helena Reinhardt (former directors), Maria
Helena Reinhardt (director), Diana Tollstadius, Raquel
Milano, Christiane Horowitz, and Marivaldo Santos
Santana. We gratefully acknowledge the field work
assistance of Rafael Carvalho, Isabela Ornellas, and
Mariana Naves. We also thank Anders Rhodin, Fred
Janzen, and an anonymous reviewer for insightful
suggestions on the manuscript. The study was conducted
under licenses IBAMA 146/2004, 328/2006, 086/2007,
and authorization for activities with scientific purposes
SISBIO 14286-1. This research was supported by Turtle
Conservation Fund, Conselho Nacional do Desenvolvimento Cientfico e Tecnologico CNPq, Fundacao de
Apoio a` Pesquisa do Distrito Federal FAPDF,
Coordenacao de Aperfeicoamento de Pessoal de Nvel
Superior CAPES, and Fundacao de Empreendimentos
Cientficos e Tecnologicos - FINATEC.
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Received: 18 July 2010
Revised and Accepted: 3 March 2011