Reproductive Allometry of Podocnemis expansa (Testudines: Podocnemididae) in

Southern Brazilian Amazon

Author(s): Thiago C. G. Portelinha , Adriana Malvasio , Carlos I. Piña , and Jaime Bertoluci
Source: Journal of Herpetology, 47(2):232-236. 2013.
Published By: The Society for the Study of Amphibians and Reptiles
DOI: http://dx.doi.org/10.1670/11-288
URL: http://www.bioone.org/doi/full/10.1670/11-288

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Journal of Herpetology, Vol. 47, No. 2, 232–236, 2013
Copyright 2013 Society for the Study of Amphibians and Reptiles

Reproductive Allometry of Podocnemis expansa (Testudines: Podocnemididae) in

Southern Brazilian Amazon

THIAGO C. G. PORTELINHA,1,2,3 ADRIANA MALVASIO,4 CARLOS I. PIÑA,1,3,5,6 AND JAIME BERTOLUCI7,8

1
CICyTTP –CONICET, CP 3105, Diamante, Entre Rı́os, Argentina.
2
Universidad Autónoma de Entre Rı́os (UADER)— Facultad de Ciencia y Tecnologı́a, CP 3100, Paraná, Entre Rı́os, Argentina
3
Proyecto Yacaré, Laboratorio de Zoologı́a Aplicada: Anexo Vertebrados (FHUC-UNL/MASP y MA), CP 3000, Santa Fe, Santa Fe, Argentina
4
Universidade Federal do Tocantins, Laboratório de Ecologia e Zoologia, Grupo de Pesquisas em Crocodilianos e Quelônios, 77001-090, Palmas, Tocantins, Brazil
5
Universidad Autónoma de Entre Rı́os (UADER)–Facultad de Ciencia y Tecnologı́a, CP 3105, Diamante, Entre Rı́os, Argentina
6
Universidad Nacional de Entre Rı́os (UNER)–Facultad de Ciencias de la Alimentación, CP 3200, Concordia, Entre Rı́os, Argentina
7
Departamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900, Piracicaba, São Paulo, Brazil

ABSTRACT.—Podocnemis expansa is the largest freshwater turtle in South America and exhibits a complex reproductive behavior. Females lay
eggs in sandy banks formed during the dry season. Nesting habitat can influence hatching success and sex determination. In some turtle species,
female body size is crucial to determine reproductive parameters such as clutch size and shape. In this study, we investigate allometric
relationships between female body size and their tracks, and clutch characteristics and nest shape in sandy beaches along the Javaés River,
southern Brazilian Amazon. Our results indicate that female body size can be estimated based on tracks. Larger females leave larger foot tracks
in the sand and have larger clutch sizes with larger clutch mass than smaller females. Female carapace width and body mass can be considered
reliable variables to estimate clutch size and total clutch mass for the species. Larger females should be protected because they can be
responsible for most annual clutch production.

RESUMO.—Podocnemis expansa é o maior quelônio de água doce da América do Sul, apresentando um comportamento reprodutivo complexo.
Essa espécie nidifica em bancos arenosos formados durante as vazantes dos rios da Amazônia. As caracterı́sticas do ambiente de nidificação
podem influenciar o sucesso reprodutivo e o sexo dos filhotes. Alguns trabalhos já demonstraram que o tamanho corporal da fêmea é
determinante para as condições da ninhada (quantidade e tamanho dos ovos) e nas dimensões dos ninhos (profundidade e diâmetro) em
algumas espécies de quelônios. O presente estudo investigou as relações alométricas entre o tamanho corpóreo da fêmea, seus rastros, as
variáveis da ninhada e a forma dos ninhos em ambiente natural em uma praia do rio Javaés, na Amazônia Brasileira. Foi observado que o
tamanho corpóreo da fêmea de P. expansa pode ser estimado em função do seu rastro. Fêmeas maiores deixam rastros maiores na areia, além de
produzirem mais ovos (tamanho da ninhada) e com maior massa (massa da ninhada) do que fêmeas menores. A largura da carapaça e a massa da
fêmea podem ser consideradas variáveis confiáveis para estimar o tamanho e a massa da ninhada dessa espécie. A proteção de fêmeas de maior
tamanho deveria ser priorizada, já que podem ser responsáveis por grande parte da produção anual de ovos.

Studies of biodiversity are increasingly important because but has never been assessed (Valenzuela, 2001; Bonach et al.,
every conservation or sustainable management project requires 2006). In the present study, we investigate the allometric
knowledge of the ecology of the targeted organisms, popula- relationships among female body size and track measurements,
tions, and ecosystems (Begon et al., 2006). Chelonians are nest shape, and clutch characteristics of P. expansa under natural
exploited widely throughout the world, and the genus conditions, providing information for conservation and man-
Podocnemis is the most highly used group in the Amazon and agement practices.
Orinoco basins (Dupre et al., 2007). As a result, these turtles play
an important role in regional economies (Klemens and
Thorbjarnarson, 1995). Therefore, information on population MATERIALS AND METHODS
and reproductive ecology of this turtle is relevant not only to
Study Area.—Fieldwork was carried out between September
elucidate its ecology but also for its conservation.
and December 2008 on a beach of the Javaés River (09858 0 S,
Podocnemis expansa (Schweigger, 1812), Giant Amazon River
50805 0 W), Tocantins state, southern Brazilian Amazon. The local
Turtle, is the largest freshwater turtle in South America
ecosystem is well preserved, and the area is a complex ecotone
(Pritchard, 1979). The species has a complex reproductive
that includes elements from Cerrado, Amazon Rainforest, and
behavior that involves nesting on sand banks formed by the
Pantanal (SEPLAN, 2001). The site is located between two
reduction of the water level of Amazonian rivers during the dry
season. Females store energy for the production of clutches that important protected areas of the Brazilian Amazon: Parque
are oviposited in sand holes (Valenzuela, 2001). We expect that Nacional do Araguaia and Área de Proteção Ambiental Ilha do
larger females will produce larger clutches in deeper nests. Bananal. The climate is tropical wet and dry (Peel et al., 2007),
In most vertebrate species, larger females invest more energy with two well-defined seasons: wet period from November to
in a clutch than smaller individuals (Reiss, 1991). The tracks that April (rainy season) and dry period from May to October (dry
female P. expansa leave in the sand after nesting are quite season). Annual rainfall is approximately 1750 mm and mean
evident and easily measured without disturbing other nesting annual temperature is approximately 248C, remaining almost
females (Bonach et al., 2006). constant throughout the year.
Podocnemis expansa foot tracks have been studied, and the Field Procedures.—Females were captured during three nights
relationship between foot track and female size was suggested at the beginning of the reproductive season (September 2008).
During the night (between 0000 and 0600 h), females were
8
Corresponding Author. E-mail: jaime.bertoluci@usp.br located with a spotlight. Researchers waited for females to finish
DOI: 10.1670/11-288 the nesting process to begin morphometric measurements and
 REPRODUCTIVE ALLOMETRY OF THE GIANT AMAZON RIVER TURTLE 233

TABLE 1. Relationship between foot tracks, clutch, eggs, and female body size in Giant Amazon River Turtle, Podocnemis expansa (least-square
regression: y = a + bx). BM, body mass; CL, carapace length; CW, carapace width; PW, plastron width; and track 1, foot track on the sand.

Excluded
y x a b df F P r2 (adj.) clutches

Track variables
Track 1 (cm) PW (cm) 8.20 1.20 29 16.15 0.0004 0.34 0
Track 1 (cm) BM (kg) 39.74 0.62 29 23.41 <0.0001 0.44 0
Clutch variables
Clutch size (n) CL (cm) -101.98 2.90 29 13.13 0.0011 0.29 0
Clutch size (n) CW (cm) -56.09 2.63 28 12.29 0.0016 0.29 1
Clutch size (n) BM (kg) 36.62 2.39 29 14.92 0.0006 0.32 0
Clutch size (n) Track 1 (cm) -15.04 2.07 28 7.07 0.0130 0.18 1
Clutch mass (kg) CL (cm) -10.16 0.19 28 39.13 <0.0001 0.58 1
Clutch mass (kg) CW (cm) -7.95 0.19 29 46.87 <0.0001 0.61 0
Clutch mass (kg) BM (kg) 0.06 0.13 29 28.14 <0.0001 0.48 0
Clutch mass (kg) Track 1 (cm) -3.07 0.12 28 13.81 0.0009 0.31 1
Egg variables
Egg mass (g) CL (cm) 2.02 0.48 29 7.65 0.0099 0.19 0
Egg mass (g) CW (cm) -5.93 0.68 28 15.17 0.0006 0.34 1

marking. For each female, we measured carapace length (CL), hatchling (CL, CW, PW, and BM) variables. Regressions also
carapace width (CW), and plastron width (PW) with a metric were established using nest characteristics (width, depth 1, depth
tape (to the nearest 1 mm) and body mass (BM) with a scale (to 2, and depth 3) as predictors in relation to the clutch variables
the nearest 100 g) according to Malvasio et al. (2005). Turtles were (clutch size, clutch mass, and hatching success). All variables
individually marked by drilling and fixing plastic tags to the were tested by linear regression. For regressions between tracks
marginal scutes of carapace (Portelinha, 2010). We measured the (track 1 and track 2) and female morphometric variables, we used
tracks left by each female with a metric tape in two ways: 1) foot the PW and female BM because these variables are the most
tracks (track 1) and 2) width of the mark left by the plastron on representative variables to deduce female body size from a track
the sand (track 2) (Bonach et al., 2006). The track measurements (Valenzuela, 2001).
were taken on flatter areas of the beach near the nest where the We used a Bonferroni correction (Norman and Streiner, 2008)
track was straight, and they were clear and firm in the sand. For for all predictor variables, considering significant results with P
each track, we took five measurements along the trackway < 0.025 for PW; P < 0.003 for CL, CW, and BM; and P < 0.008
portion and considered the mean value. for track 1 and track 2. Observations with leverage coefficient
Eggs were removed from nests and marked with a pencil to
greater than 4/N and highly standardized residuals were
avoid rotation and to ensure return to their original position in
excluded and the data reanalyzed (Sokal and Rohlf, 1995). All
the nest (Ewert, 1979; Larriera, 1991). Nonviable eggs (damaged
data were analyzed in the software InfoStat for Windows
or yolkless) were discarded. Egg length and width measure-
(INFOSTAT, 2008). Means are reported 6 SD.
ments were taken with calipers (to the nearest 0.01 mm), and
egg mass was measured with a digital scale (to the nearest 0.1
g). Clutch size (total number of eggs in the nest) was recorded, RESULTS
and clutch mass (sum of the mass of each egg) was calculated. Thirty Podocnemis expansa females were captured during three
These procedures occurred during the period of lower solar sample nights in approximately 18 h. We observed that larger
intensity (between 0600 and 0900 h or after 1700 h) to avoid (PW) and heavier (BM) females left larger foot tracks in the sand
death or damage to the embryos because of high temperatures.
(Table 1). However, no relationship was observed (P > 0.05)
We measured the following physical characteristics of nests
between track 2 and female morphometric variables (PW and
(Bonach et al., 2006): egg-chamber width (width), egg-chamber
BM).
depth (depth 1), nest height (depth 2), and depth until the first
Nest dimensions (depth and width) were not influenced by
egg on egg chamber (depth 3).
female size (P > 0.05). However, clutch size and clutch mass
During the incubation period, nests were monitored daily
until eggs hatched. Only after hatching were the nests opened were correlated positively to female size (CL, CW, and BM) and
again, when the number of unhatched eggs and live and dead track 1. Thus, larger females lay more eggs and produce heavier
hatchlings were counted. We calculated incubation time, clutches. We found no relationship between relative clutch mass
hatching success [(number of live hatchlings/clutch size) · and female size (P > 0.05). Hatching success also was not
100] and relative clutch mass [(clutch mass/female body mass) related to female size (P > 0.05). Nest physical characteristics
· 100]. Measurements of hatchling CL, CW, PW, and BM also (depth 1, depth 2, or depth 3 and width) were not correlated to
were collected. clutch size, clutch mass, or hatching success (P > 0.05).
Statistical Analysis.—We established allometric relationships Egg mass was related to female carapace length and width
between female morphometric variables (CL, CW, PW, and BM) (Table 1). However, we observed that egg size (length and
and tracks (track 1 and track 2) as predictors (independent width) does not depend on female size (P > 0.05). Although
variables) of nest (width, depth 1, depth 2, and depth 3), clutch bigger females lay more and heavier eggs, there was no
(clutch size, clutch mass, relative clutch mass, and hatching relationship between hatchling body size and female morpho-
success), egg (egg length, egg width, and egg mass), and metric variables (CL, CW, and BM; P > 0.05).
234 T. C. G. PORTELINHA ET AL.

DISCUSSION as it has been hypothesized for this species (Valenzuela, 2001;

In turtles, sexual maturity is related to female minimum body Bonach et al., 2006). However, because the type of sediment
size and age (Cagle, 1950; Legler, 1960); for this reason, body could affect these relationships, extrapolation to other sites
length has been used in many studies of reproductive allometry should be taken with caution.
as a basis for relationships (Peters, 1983; Souza et al., 2006). In Furthermore, we found a strong relationship between clutch
this study, we used both body size and body mass to establish size and clutch mass and all female morphometric variables,
relationships between nest and clutch variables, tracks, eggs, including foot tracks (Table 1). This relationship demonstrates
and hatchlings. The use of other variables, as proposed by this that larger females tend to produce larger clutches with heavier
work, may clarify relationships that have not been tested, such eggs, as it has been observed for the Amazonian species
as the width of the foot tracks and female body size. Podocnemis sextuberculata (Haller and Rodrigues, 2006) and some
According to Alho and Pádua (1982), Podocnemis expansa species of crocodilians (Thorbjarnarson, 1996; Verdade, 2001;
females reach sexual maturity at a CL of 50 cm. In the present Larriera et al., 2004). However, although the generated model
study, female CL = 71.9 6 4.6 cm (range, 62.0–79.0; n = 30). explained more than 60% of variation for some relationships
Lower values for adult females of the same species were (Table 1), other factors, such as population density, nutritional
presented by Cantarelli (2006), with CL = 64.0 6 3.9 cm (52.5– status, age, and climate variables, should be considered in
69.1; n = 34). In addition, we observed a mean BM = 29.1 6 5.8 studies with reptiles because they may influence clutch size and
kg (19.0–41.0; n = 30). These values were also greater than those clutch mass (James and Whitford, 1994).
presented by Cantarelli (2006) (24.9 6 3.1 kg, 17.0–30.0; n = 34) Podocnemis expansa produces large clutches. Soares (1996) and
for the turtles of the Araguaia River (Goiás state, central Brazil). Bonach et al. (2006) found similar clutch sizes for this species in
Although the area studied by Cantarelli (2006) is close to our different locations in the Brazilian Amazon (105.0 and 103.0 6
study site, differences were observed for both CL and BM and 18.2 eggs, respectively). Hildebrand et al. (1988) observed a
could reflect variation between two distinct populations. mean clutch size of 105.0 eggs for the P. expansa population of
Generalizations between reproductive status and body size the Caquetá River (Colombia), and a similar value was reported
must be made with caution, because there also may be variation by Valenzuela (2001) (103.0 6 23.7 eggs). Iverson et al. (1993)
due to external factors, such as climate change (Frazer et al., suggested that variation in clutch size of a particular species
1993) and hunting pressure (Velasco and Ayarzaguena, 1995), may be associated with latitudinal differences, as observed in
both of which can affect body size at maturity. Clemmys guttata (Litzgus and Mousseau, 2006) and crocodilians
We found nest height (depth 2) = 78.9 6 14.1 cm (46.0–101.0; (Wilkinson, 1983; Simoncini et al., 2009). The mean clutch size
n = 30); however, lower amplitude values were described by found in this study (106.0 6 23.6 eggs, 36.0–141.0; n = 30) is
Alho et al. (1979) (75.0–80.0 cm), Bonach et al. (2006) (37.5–83.0 similar to values reported for different populations of this
cm), and Ferreira Júnior et al. (2007) (53.7–64.8 cm). Variation species in different regions of the Amazon, regardless of
found by these studies may be related to differences in beach latitudinal variation (0–138S; 098S in our study). Although
characteristics (such as height and grain size), characteristics clutch size is similar in these areas, female size seems to be
that can influence nest digging (Ferreira Júnior and Castro, different (e.g., CL = 74.1 6 4.2 cm [Soares, 1996]; CL = 64.0 6
2006). No relationship was found between nest depth and 3.9 [Cantarelli, 2006]; and CL = 71.9 6 4.6 cm [this study]). This
hatching success (P > 0.05), as described by Bonach et al. (2006). observation should not be expected if the relationship between
This finding may be related to chelonian embryonic develop- female size and clutch size found in this study is the same in all
ment being more influenced by other nest variables, such as these areas. Future studies should investigate this question.
temperature, humidity, and sediment grain size (Morris et al., Our results suggest that, as adult P. expansa females increase
1983; Packard et al., 1999; Ferreira Júnior et al., 2007). their size, they also store more energy (in absolute terms) for
Egg-chamber width observed in this study (17.0–52.0 cm; n = reproduction, as suggested by the increase in clutch mass with
30) was higher than values reported by Alho et al. (1979) (20.0– the female body size (Table 1). Moreover, our data indicate that
25.0 cm) and Bonach et al. (2006) (16.0–37.5 cm; n = 10). The larger females invest in the production of not only more eggs
same was observed for depth until the first egg on egg chamber but also heavier eggs, as described by Valenzuela (2001).
(depth 3) (31.8 6 5.6 cm, 23.0–46.0; n = 30) compared with the Nevertheless, we found no relationships between body size
studies mentioned above (13.0–18.0 and 10.0–40.0 cm, respec- and relative clutch mass. This finding indicates that there is no
tively). Some studies suggested that nest dimensions are related difference in the relative energetic investment among females
to female body size, because smallest females should have from different size classes (or ages), contrary to what was
limitations to dig wider and deeper nests (Ehrhart, 1995; observed by Cantarelli (2006) for P. expansa and in some
Valenzuela, 2001; Morjan, 2003; Bonach et al., 2006). However, crocodilians species (Thorbjarnarson and Hernández, 1993;
no relationships (P > 0.05) were found between nest dimensions Verdade, 2001; Larriera et al., 2004).
(depth 1, depth 2, or depth 3 and width) and female body size Egg dimensions (length, width, and mass) found in this study
(CL, CW, and BM) or foot track (track 1), suggesting larger and (41.3 6 1.5 mm, 38.8 6 1.6 mm, and 36.4 6 4.7 g, respectively)
smaller females may dig similar nests in some areas. were smaller than those observed by Ojasti (1971) (46.0 mm,
Foot tracks varied from 47.0 to 67.0 cm (57.7 6 5.8 cm; n = 40.0 mm, and 40.0 g) in the Orinoco River (Venezuela).
30), and the mark of female plastron in the sand varied from Although latitudinal variation did not affect clutch size (as
15.0 to 26.0 cm (20.4 6 5.3 cm; n = 30). Similar values for tracks described herein), we may not discard the possibility that egg
have been presented by Valenzuela (2001) (54.8 6 4.3 cm, 44.0– size could be influenced by this factor, as proposed by Vanzolini
66.0 cm for foot tracks; n = 88) and Bonach et al. (2006) (50.4 6 (1997).
3.6 cm, 43.0–55.5 cm for foot tracks and 21.9 6 2.5 cm, 18.5–26.5 The possibility of establishing relationships between foot
cm for Ttrack 2; n = 14). We found a positive relationship tracks, size and number of eggs and hatchlings, and physical
between foot tracks, female body size, and clutch size, nest characteristics and nesting female will contribute positively
suggesting that trackways are useful to relate these variables to management techniques of P. expansa conservation programs
 REPRODUCTIVE ALLOMETRY OF THE GIANT AMAZON RIVER TURTLE 235

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