Open-access Deeper nests enhance embryo survivorship of the Yellow-Spotted River Turtle in the southern Amazon Region

Ninhos mais profundos aumentam a taxa de sobrevivência de embriões de tracajá no sul da região Amazônica

Abstract

The reproductive ecology of a species is a key focus of conservation planning efforts as it offers insights into how the species persists and adapts to its environment. The Yellow-Spotted River Turtle, Podocnemis unifilis (Troschel,1848), has a wide distribution within the Amazon region and is generalist in its nesting site choice. Monitoring the nesting habits of this turtle is essential to understand the resilience of its populations and to evaluate the impact of environmental disruptions. This study aimed to assess how environmental factors affect the hatching rate, nest loss, and sex ratio of P. unifilis in the Iriri River, Pará. In 2012 and 2013, we monitored 121 nests over approximately 200km of the river within the Terra do Meio Protected Area. Nests with deeper egg chambers located at high elevated areas of the beaches had a higher mean hatching rate. Moreover, deeper nests had fewer rotten eggs and were less infected by Sarcophagidae fly larvae. Animals predated only two nests, and humans collected five nests. Nests that were manipulated presented lower hatching rates compared to unmanipulated nests. Furthermore, the sex ratio 100% biased towards females may indicate the limit of the behavioral and physiological plasticity of the species. Compared to other areas, P. unifilis nests had deeper egg chambers in the Iriri River, likely due to climate and nesting site granulometric profile. Our findings suggest that females of P. unifilis adjust nest characteristics to maximize the survival of their offspring in this coarse sediment environment. The plasticity in nesting site selection and nest depth highlights the species’ ability to adapt, enabling it to occupy a wide geographic area and successfully reproduce in various environments. However, climate change may gradually alter this situation, emphasizing the need to gather reproductive data from different sites to monitor the species’ capacity to adapt to habitat alterations.

Keywords Hatching rate; Xingu basin; Amazon freshwater turtle; Podocnemis unifilis

Resumo

A ecologia reprodutiva de uma espécie é um ponto chave nos esforços para a elaboração de planos conservacionistas, uma vez que oferece informações sobre como a espécie persiste e se adapta ao ambiente. O Tracajá, Podocnemis unifilis (Troschel,1848), possui ampla distribuição na região Amazônica e é generalista na escolha do sítio de desova. O monitoramento dos hábitos de nidificação da espécie é essencial para compreender a resiliência das diferentes populações e avaliar o impacto de perturbações ambientais. Este estudo teve como objetivo avaliar como os fatores ambientais afetam a taxa de eclosão, a perda de ninhos e a razão sexual de P. unifilis no rio Iriri, Pará. Em 2012 e 2013, monitoramos 121 ninhos ao longo de aproximadamente 200 km do rio dentro da Área Protegida da Terra do Meio. Os ninhos com câmaras de ovos mais profundas, localizados em zonas elevadas das praias, registaram uma taxa média de eclosão mais alta. Ainda, os ninhos mais profundos tinham menos ovos podres e estavam menos infectados por larvas de moscas Sarcophagidae. Os animais predaram apenas dois ninhos e os humanos coletaram cinco ninhos. Os ninhos que foram manipulados apresentaram taxas de eclosão mais baixas do que os ninhos não manipulados. Além disso, a razão sexual 100% tendenciosa para as fêmeas pode indicar o limite da plasticidade comportamental e fisiológica da espécie. Em comparação com outras áreas, os ninhos de P. unifilis apresentaram câmaras de ovos mais profundas no rio Iriri, provavelmente devido ao clima e ao perfil granulométrico do local de nidificação. Os nossos resultados sugerem que as fêmeas de P. unifilis ajustam as características dos ninhos para maximizar a sobrevivência da prole nesse sítio de desova com sedimentos mais grossos. A plasticidade na seleção do local de desova e na profundidade dos ninhos destaca a capacidade de adaptação da espécie, permitindo que ela ocupe uma ampla área geográfica e se reproduza com sucesso em vários ambientes. No entanto, as alterações climáticas podem alterar gradualmente esta situação, enfatizando a necessidade de reunir dados reprodutivos de diferentes locais para o monitoramento do potencial de adaptação da espécie às alterações do habitat.

Palavras-chave Taxa de eclosão; Bacia do rio Xingu; tartarugas de água doce da Amazônia; Podocnemis unifilis

Introduction

The choice of the nesting site environment plays a crucial role in the reproductive success of oviparous species. The temperature and humidity that the eggs experience during the incubation period directly influence the development and growth of embryos of ectothermic animals (Angilletta et al., 2004). In the case of freshwater turtles, the effect of temperature on physiological processes can be seen in the duration of hatchling incubation, growth rate, and swimming performance (Du et al., 2007; Lefebvre et al., 2011; Micheli-Campbell et al., 2011). These traits are likely determined by the nesting site selected by females, aiming to increase the fitness of the offspring (Mitchell et al., 2013; Warner, 2014). Thus, most suitable nesting sites may differ in their optimal environmental features depending on the species and the geographic location (Bowen et al., 2005; Litzgus & Mousseau, 2006; Valenzuela et al., 2019). Since the interaction of the nest microclimate and regional climate determines the temperature changes during the incubation period, there are behavioral and physiological differences in nest site selection among populations with wide distribution (Hughes & Brooks, 2006; Warner, 2014; Weisrock & Janzen, 1999; Wilson, 1998).

The selection of nesting sites can affect the sex of turtle embryos. For species with Temperature-Dependent Sex Determination (TSD), sex differentiation occurs in a thermosensitive period during incubation (Bull & Vogt, 1979). In most freshwater turtle species, higher temperatures result in more female-biased clutches, while lower temperatures produce more male-biased clutches (Ferreira Júnior, 2009; Valenzuela et al., 2019). However, the ratio of each sex may vary depending on the latitude, as different populations have varied levels of sensitivity to temperature (Fuentes et al., 2017; Hoekstra et al., 2018; Lovich et al., 2010). Separated populations may vary their physiological response to temperature oscillation and show distinct thresholds for sex differentiation in embryos (Valenzuela et al., 2019). Additionally, some turtle species were recorded varying the type of nesting site substrate, which drove different sex proportions in the clutches (Erickson et al., 2020). Previous studies have shown that changing the nest substrate can lead to a more balanced overall sex ratio in certain turtle populations (Erickson et al., 2020; Mitchell & Janzen, 2019; Rasmussen & Litzgus, 2010). Therefore, nesting site selection is a complex behavior that accounts for multiple local and regional factors and may play a crucial role in the persistence of turtle populations.

By nest site selection, females may compensate for external environmental conditions, balancing nest microclimate, and maximizing survivorship and fitness (Bull et al., 1982; Litzgus & Mousseau, 2006; Morjan, 2003). In some species, females from different populations change the nesting site from open to shadier areas depending on the latitude (Ewert et al., 2005; Micheli-Campbell et al., 2013). Additionally, the nest substrate plays a crucial role in determining offspring survivorship through managing temperature: fine-grain substrates retain more moisture and present lower temperature oscillation than coarse-grain ones, which may buffer temperature peaking during the incubation period, avoiding extreme conditions (Mitchell & Janzen, 2019; Topping & Valenzuela, 2021). Besides the nest location, females may change nest features according to climate variations. In response to a drier climate, females can dig deeper nests that increase embryo survivorship (Czaja et al., 2020; Morjan, 2003; Refsnider et al., 2022). Despite that, the limitation of this strategy is the individual size, and for small species, this cannot be enough to compensate for climatic conditions (Refsnider et al., 2013). Thus, knowing nest environmental features is essential to understanding how populations are experiencing regional gradients and assessing their vulnerability to habitat disturbances. Moreover, the combination of habitat features likely influences the probability of embryo mortality by external threats.

The most recorded causes threatening freshwater turtle nests are animal predation, flooding, and collection by humans (Moll & Moll 2004). Predation by animals is the most frequent, usually related to environmental characteristics that may favor predator adaptations. Some predators can quickly locate turtle nests around their habitat range using olfactory and visual cues (Dawson et al., 2016; Riley & Litzgus, 2014; Zappalorti et al., 2017). Nests of populations inhabiting rainforests, which contain a high abundance and diversity of species, often comprise the diet of mammals, reptiles, and even insects (Erickson & Baccaro, 2016; Salera Junior et al., 2009; Schneider et al., 2011). Besides that, flooding is one of the main causes of nest embryo mortality, especially in regions around large rivers. In Australia (Micheli-Campbell et al., 2013) and the Amazon Region (Arraes et al., 2016; Bock et al., 2021; Erickson et al., 2020; Pezzuti & Vogt, 1999), freshwater turtle nests are commonly impacted by sudden rises in river levels, decreasing the number of successful nests. Moreover, the survival rate of freshwater turtle embryos is influenced by the social and economic profile of the area, since human populations often collect turtle eggs for consumption and pet trade (Moll & Moll, 2004). In regions having a high density of riverine populations, such as the Amazon, freshwater turtle eggs and meat have been consumed since colonial times, playing an important cultural and economic role (Chaves et al., 2020; Michalski et al., 2020; Mittermeier, 1978). Therefore, estimating reproductive success for a species distributed widely across different regions becomes complex and depends on several biological, physical, and social factors.

In the Amazon region, the Podocnemis unifilis (Troschel,1848) is a medium-sized turtle that can be found in white, clear, and blackwater rivers (Rueda-Almonacid et al., 2007). It is considered a generalist in terms of nest site selection since its nests are usually found during the dry season in sandbanks, clay banks, rocky grounds, and near vegetation (Erickson et al., 2020; Ferreira Júnior & Castro, 2010; Michalski et al., 2020; Pignati et al., 2013). The high diversity of nesting sites drives annual and spatial variation of the overall nest hatching rate across populations, as well as the overall nest sex ratio (Arraes et al., 2016; Erickson et al., 2020; Pignati et al., 2013a; Pignati et al., 2013b). Like most freshwater turtles, P. unifilis is a TSD species that produces female-biased clutches at high temperatures and male-biased clutches at lower ones (Souza & Vogt, 1994). Therefore, the nest site selection can be a determining factor in preventing external threats for this species. The eggs of P. unifilis are a valuable food source for monkeys, birds, insects, and lizards during the dry season, and predation rates may increase if nests are close to vegetation (Erickson & Baccaro, 2016; Salera Junior et al., 2009). The collection of nests by humans may occur more frequently when nests are laid on fine sand (Michalski et al., 2020), and it is recorded across the Amazon region since it has been an important food source for traditional communities for generations (Chaves et al., 2020; Mittermeier, 1978; Pantoja-Lima et al., 2014). Furthermore, nests that are closer to the river or nested in shallow areas of the nesting sites are usually vulnerable to flooding, as the sudden rise of river water (locally known as repiquete) may occur in all phases of the incubation time (Erickson et al., 2020; Pezzuti & Vogt, 1999; Pignati et al., 2013a). Therefore, the species’ wide distribution makes it crucial to monitor nest site selection as evidence of how females interact with the environmental gradient, aiming to understand local variations and vulnerabilities, which can be essential for conservation management.

The Amazon landscape is very diverse and understanding the variations in species reproductive aspects is important due to the environmental threats to the region. Factors like deforestation, river damming, and climate change can significantly impact natural cycles, affecting the feeding and nesting habitats of the species adapted to them (Alho, 2011; Eisemberg et al., 2016; Fearnside, 2015; Resende et al., 2019). Therefore, it is crucial to conduct local studies to understand variations in reproductive patterns at the population level and to predict the consequences of environmental disturbances on the ecosystem (Proença et al., 2017). By monitoring reproduction events, we can develop better management plans considering habitat features and reproductive characteristics of each nesting region. Our study evaluated how local nest characteristics, such as nest height, distance from the shore and vegetation, egg chamber depth, and canopy coverage, influenced the hatching rate, egg loss, and sex ratio of Podocnemis unifilis nests in Iriri River, Pará.

Material and Methods

1.

Study site

We conducted a study in the Iriri River, which is the major left-bank tributary of the Xingu River, located in the State of Pará, Southeast Amazon, Brazil. The Iriri River is a clear water system that originates from the Central Brazilian shields with its headwater in Serra do Cachimbo (Junk et al., 2011). The vegetation in the area consists of submontane and alluvial rainforest, and the climate is tropical monsoon with a high annual mean temperature (> 26º) (Alvares et al., 2013). The high-water season occurs between February and May, and the low-water season between August and October (ICMBIO, 2015). In 2012, the mean daily temperature was 24.71 ± 0.58, and the annual rainfall of 1310 mm. In 2013, the mean daily temperature was 23.91 ± 0.41, and the annual rainfall was 1350 mm (Figure 1).

Figure 1
Mean river level (light blue line), max rainfall (dark blue line), and mean daily temperature (dashed red line) by month in the Iriri River, southern Amazon region.

The river segment was located within the Terra do Meio Protected Area (TMPA) (from 54°18’30.7” W 5°36’09.7” S to 54°14’00.9” W 5°43’27.7” S). The TMPA is categorized as an Ecological Station that aims to conserve biodiversity (ICMBIO, 2015). During the high-water season, the landscape of TMPA is characterized by waterfalls, rapids, and flooded forests, providing food sources for aquatic fauna. In the dry season, rocky rapids and sandbanks emerge, making refuge and nesting environments available for reptiles and birds (Campos-Silva et al., 2018; Junk et al., 1989; Silva & Rodrigues, 2010).

2.

Sampling design

Fieldwork was conducted during the nesting season in August and the hatching season in October of 2012 and 2013, covering approximately 200 km of the river. During the nesting campaigns, we searched for nests in the early morning, using female turtle tracks as indicators. Each nest was marked with a stake and georeferenced. Most nests were opened to count the number of eggs and measure various environmental variables, including the distance to the river, nest height, slope, egg-chamber depth, depth to the first egg, and canopy cover. Additionally, we collected substrate samples for granulometric analysis.

To determine the incubation period, we observed female tracks, examined egg characteristics, and assessed egg pigmentation to establish the oviposition date (Pezzuti & Vogt, 1999). The distance from the nests to the riverbank was measured with a 50 m tape measure. Nest height was determined using water-filled hoses and a measuring tape, following the method outlined by Pantoja-Lima et al. (2009). We employed a Starrett inclinometer to measure the slope at the nest site. The depths of the egg chamber (the distance from the nest surface to the bottom of the chamber) and the first egg were measured using a millimeter rule, as described by Pignati et al. (2013a). Canopy coverage was estimated with a spherical densitometer model C (Lemmon, 1956). For sediment analysis, approximately 200 g of surface material was collected from 43 nests and classified by particle size using a sieve system (Folk, 1974) at the Geology Laboratory of the Federal University of Pará (UFPA). Canopy coverage estimation and granulometric analysis were only performed for nests from 2012. We classified 30 nests (24.74%) as “unmanipulated” because we did not open them for internal measurements, and we compared their hatching rates with those of the manipulated nests.

Throughout both seasons, we observed complete and partial nest losses. To determine the causes of mortality, we examined egg characteristics and the external conditions surrounding the nests, such as predator tracks, the distribution of eggshells, and the overall appearance of the nest surface. During the hatching season, we counted hatched and unhatched eggs to calculate the hatching rate. For sex ratio analysis, we humanely euthanized five hatchlings from each of the 43 nests. These hatchlings were preserved in 10% formalin and stored in 70% alcohol at the Laboratory of Aquatic Ecology and Fisheries at UFPA. The sex of the hatchlings was determined by examining the size and appearance of their gonads, following the methodology described by Malvasio et al. (2012).

3.

Data analysis

Before selecting the appropriate tests, we assessed the data for normality using the Shapiro-Wilk test. We applied a Permutational Analysis of Variance (PERMANOVA) utilizing Euclidian distance to analyze the variation of local and climatic environment variables between the years (Anderson, 2014). The hatching rate was calculated as the proportion of hatched neonates relative to the total number of eggs in the clutch. This rate was represented as a vector containing the number of successes (fully developed hatched hatchlings) and failures (dead embryos or unhatched hatchlings) for the analysis (Crawley, 2007).

We evaluated the relationship between this vector and explanatory variables—such as height, depth, distance to the river, canopy coverage, and granulometric fractions—using a Generalized Linear Model (GLM) with a quasibinomial distribution to adjust for overdispersion (Carranco et al., 2022; Knoerr et al., 2021). Before modeling, we conducted a Pearson correlation analysis and removed highly correlated variables (correlation coefficient > 0.70). The years 2012 and 2013 were included in the models to account for annual variation, while canopy coverage was only considered for nests from 2012. Granulometric fractions were classified as gravel, very coarse sand, coarse sand, medium sand, fine sand, very fine sand, and mud. To avoid collinearity among these fractions, we performed a Principal Component Analysis (PCA), using the first axis score as an explanatory variable (Pignati et al., 2013a). This first axis accounted for 42.20% of the variance, with higher axis values associated with middle-sized particles and lower values linked to coarse sand.

To compare hatching rates between manipulated and unmanipulated nests, we employed a Kruskal-Wallis test to rank values and analyze data distribution between groups, given that the hatching rate data did not follow a normal distribution (Shapiro-Wilk normality test: w = 0.73, p = 0.003) (Ostertagová et al. 2014). The sex ratio was determined based on the proportion of female hatchlings to the total number of hatchlings within each clutch.

We categorized egg losses as rotten, undeveloped, predated, or collected by humans. For each category, the proportion of lost eggs was represented by a vector, indicating the number of successes (living hatchlings) and failures (lost eggs by category) (Crawley, 2007). Given the high presence of Sarcophagidae fly larvae in dead hatchlings, we included this as a loss category to assess potential environmental influences. One nest was excluded from the GLM analysis involving fly larvae, as it exceeded Cook’s Distance (0.5), suggesting it was unduly influencing the trend line and the analysis results (Crawley, 2007). Finally, we evaluated the relationships between the proportion of lost eggs and environmental variables using a GLM with a quasibinomial distribution (Carranco et al., 2022). Analyses were conducted only when at least ten nests fell within specific mortality categories.

Results

We monitored 64 nests in 2012 and 57 nests in 2013. In 2013, native shrub vegetation partially shaded 31.57% of nests during the morning or afternoon. Plant species comprises the locally called sarão (Augusta longifolia), bananinha-do-mato (Bromelia antiacanta), ginja (Prunus cerasus), caferana (Bunchosia armeniaca), goiaba (Psidum guajava), and vassourinha (Scoparia dulcis). The local environment variables of the nests did not vary between 2012 and 2013 (Pseudo-F = 0.13, p = 0.82, Table 1), as well as the climatic ones (Pseudo-F = 0.34, p = 0.52). In 2012, the granulometric profile of the nests was composed of an average of 21.18% gravel, 28.87% very coarse sand, 20.07% coarse sand, 24.13% medium sand, 04.19% fine sand, 01.24% very fine sand, and 0.28% mud (Figure 2). A descriptive analysis of the granulometric fractions is available in Table S1.

Table 1
Podocnemis unifilis nest environmental characteristics described as mean ± standard deviation (min-max).
Figure 2
Average proportion of granulometric fractions for each nest in the Iriri River, Pará.

In 2012, the mean clutch size was 16.70 ± 4.16 (8 – 27) eggs; in 2013, it was 17.10 ± 3.15 (10 – 26). The mean hatching rate in 2012 was 0.76 ± 0.26 (0 – 1), and the nests presenting higher hatching success had deeper egg chambers (β = 0.59, p = 0.004, Figure 3) and were at higher heights (β = 0.70, p = 0.003, Figure 4). In 2013, the hatching rate had no relationship with abiotic variables, with a mean success of 0.75 ± 0.37 (0 – 1). The unmanipulated nests monitored in 2013 presented a 0.92 ± 0.11 (0.61 – 1) mean hatching rate, which was higher than all manipulated nests (0.75 ± 0.32, 0 – 1) (Kruskal-Wallis chi-squared = 3.84, df = 1, p-value = 0.04, Figure 5). The sex ratio analysis showed that 100.00% of all the hatchlings were females.

Figure 3
Relation of the hatching rate and egg-chamber depth of P. unifilis nests in the Iriri River, Pará.
Figure 4
Relation of the hatching rate and height of P. unifilis nests in the Iriri River, Pará.
Figure 5
Hatching rate of manipulated and unmanipulated nests of P. unifilis in the Iriri River, Pará.

In 2012, lost nests represented 6% (N = 4) of the nests monitored, and partial egg losses occurred in 48 (75%). One entire nest was predated by the snail kite (Rostrhamus sociabilis) (1%) in 2012, three nests were collected by humans (4%), and there was at least one undeveloped egg inside 29 nests (45%). Rotten eggs were observed in 18 nests (28%) and were more frequent in shallower nests (β = 0.48, p = 0.02, Figure 6). Only two nests had one egg with fungus (3%). Sarcophagidae fly larvae were observed in the carcass of fully developed hatchlings in nine nests (14%), negatively associated with the final depths (β = 0.32, p = 0.03, Figure 7).

Figure 6
Relation of rotten eggs number with egg-chamber depth of P. unifilis nests in the Iriri River, Pará
Figure 7
Relation of Sarcophagidae fly larvae presence with egg-chamber depth of P. unifilis nests in the Iriri River, Pará.

In 2013, total lost nests represented 8% (N = 5), and partial egg losses occurred in 25 (43%). Only one nest was predated in 2013 (1%), two nests were collected (3%), and at least one undeveloped egg was present in 10 nests (17%). Two nests and their paddocks were no longer in the area in hatching monitoring, and there was at least one rotten egg in 12 nests (21%). We observed Sarcophagidae fly larvae in two nests (3%). The egg mortality was not related to environmental variables.

Discussion

Understanding the reproductive aspects of nesting turtles is essential for local conservation efforts. Ensuring the effectiveness of conservation strategies becomes puzzling when the species is widely distributed (Boyd et al., 2008). Since freshwater turtles present interpopulation variation in response to local environmental factors, monitoring the nesting habitat across their range is essential to assess their adaptative plasticity and resilience to habitat alterations (Refsnider & Janzen, 2012). In the present study, P. unifilis nested in open sandy areas and partially vegetated sites, with few nests collected or predated along the Iriri River. Our results showed higher hatching success in nests located in elevated areas with deeper egg chambers. Shallower nests had more rotten eggs and Sarcophagidae fly larvae than deeper ones. All nests produced female offspring. The present study showed a potential adaptation of the species to high temperatures at nesting sites, improving survivorship but failing to balance the sex ratio.

During summer, which corresponds to river turtle reproductive season, the Iriri River features rocky grounds and coarse sand habitats with shrubs, with less frequent clay banks. Due to logistic constraints and local guides’ indication, the sampled area comprised homogeneous environments, which may explain the lack of effect from granulometric fractions on the biological variables. However, we shall consider in the interpretation of the results that the granulometric variation from middle-size to coarse sand leads to high thermal conductivity and lower water retention in the incubation substrate, resulting in high-temperature fluctuations in the egg chambers (Souza & Vogt 1994, Mitchell & Janzen 2019, Erickson et al. 2020). While regional temperatures in the Amazon are relatively stable, substrate characteristics typically influence female nesting behavior and likely determined nest locations in our study (Alvares et al., 2013; Micheli-Campbell et al., 2013; Morjan, 2003). Since the nesting environment did not vary widely between years, the low number of nests with a complete dataset in 2013 (N = 19) may explain the consistency in biological variables.

The nesting behavior associated with vegetation is expected for freshwater turtles, but mostly below canopy shade (Ewert et al., 2005; Micheli-Campbell et al., 2011; Refsnider et al., 2013; Zappalorti et al., 2015). However, our study showed that P. unifilis females nested in sites with lower to middle canopy coverage, sometimes near shrub vegetation in the sarobal habitat. Although embryo development relies on appropriate heat levels, extremely high and low temperatures can be detrimental (Camillo et al., 2022; Rafferty & Reina, 2014). Nest site selection behavior varies among climatic regions. Populations from temperate regions often choose warmer areas with sparse vegetation, as found for Emydoidea blandingii, Clemmys guttata, and Crysemys picta marginata in Canada (Markle et al., 2021), and Terrapene carolina carolina and Clemmys guttata in the north of United States (Refsnider et al., 2022). Other species encountered in warmer climates prefer nesting sites close to vegetation or with more canopy coverage, such as Trachemys callirostris callirostris in Colombia (Restrepo et al., 2006) and Chrysemys picta bellii in the southern United States (Refsnider et al., 2013). Thus, this behavior varies to find the most suitable nesting sites for embryo development, which may be crucial in regions with high-temperature oscillations, such as tropical countries.

In neotropics such as the Amazon basin, nesting near vegetation may enhance offspring survival by maintaining humidity levels in egg chambers during high-temperature fluctuations (Correa-H et al., 2010; Janzen, 1994; Restrepo et al., 2006). Podocnemis unifilis nests are commonly found near plant species across Amazon nesting sites (Conway-Gómez et al., 2014; Erickson et al., 2020; Pignati et al., 2013b). This adaptability characterizes the species as the most generalist within the Podocnemididae family regarding nesting site choice (Erickson et al., 2020; Haller et al., 2006; Batistella & Vogt, 2008; Rueda-Almonacid et al., 2007). As the species produces hard-shelled eggs (Winkler, 2006), clutches are tolerant to water loss and desiccation, enabling them to increase dispersion area and successfully nest in different environments (D’Alba et al., 2021; Packard et al., 1987; Tracy et al., 1978). However, extreme conditions can override those adaptations and increase egg mortality. This information also highlights the importance of native vegetation to the reproduction of freshwater turtles in the Xingu Basin, playing a role in the temperature control of the P. unifilis nests, and being a food resource for the aquatic fauna during the high-water season (Cunha & Ferreira, 2012).

Although the selection of the nesting sites depends on environmental cues, females may adjust nest characteristics based on external conditions (Souza & Vogt, 1994). For most freshwater turtle species, female size influences the egg-chamber depth (Iverson et al., 2019). However, some species modify this feature in response to climate conditions to enhance offspring survivorship (Morjan, 2003). For example, Chrysemis picta constructed deeper nests closer to the water in low latitudes and shallower nests in high latitudes (Refsnider et al., 2013). Another study proved that regional differences in nest depth are not a result of population genetic variation, but a species behavior plasticity since translocated C. picta individuals from colder weather areas changed this nest trait in response to warmer conditions (Refsnider & Janzen, 2012). Behavior plasticity may be advantageous in adapting to environmental changes that drive a directional selection, reducing genetic variability mainly in long-lived species (Hoffmann & Sgró, 2011). This aspect of the species’ life history is essential for supporting management strategies since it may evidence its adaptation capacity and how susceptible it is to environmental disturbance (Hoffmann & Sgró, 2011).

Although the mean temperature remains relatively stable across the Amazon region, local characteristics influence female nesting behavior. In the Iriri River, the nests of P. unifilis were found to be deeper than was previously recorded in the Amazon, while maintaining the average hatching rate observed in other populations. The mean hatching rate in our study is comparable to the hatching rate in the lower Amazon River, where hatching success was 67% in 2007 and 75% in 2009 (Pignati et al., 2013b) and 76% in Bolivian Amazon (Carvajal et al., 2011). Hatching rates of Podocnemididae turtles often fluctuate between years, primarily due to external factors (Arraes & Tavares-Dias, 2014; Fachín Terán & von Mülhen, 2003; Pantoja-Lima et al., 2009). Additionally, substrate type and nest depth may influence the probability of hatchling survival (Erickson et al., 2020; Ferreira Júnior & Castro, 2006). We hypothesize that the granulometric profile of our study area favored deeper nests, enhancing the hatching rate. In Javaés River, P. unifilis nests primarily consisted of medium-sized sand, with an average depth of 15.6 cm (Ferreira Júnior & Castro, 2003). In the Tucuruí hydroelectric reservoir, the mean nest depth was 13.9 cm (Félix-Silva, 2009), while it reached 18.2 cm in the Araguari River (Arraes & Tavares-Dias 2014). Given the species’ size, P. unifilis nests feature a shallow egg chamber that experiences greater temperature fluctuations compared to those of larger species (Ferreira Júnior & Castro, 2006). Therefore, deeper egg chambers can be gainful in warmer regions by decreasing the temperature variation inside the nests (Riley et al., 2014). Furthermore, the elevation of the nesting site also influences embryo survivorship.

Freshwater turtles often choose elevated nesting sites to avoid inundation from rising river water levels (López et al., 2013; Micheli-Campbell et al., 2013; Santoro et al., 2023). Flooding events can significantly impact turtle hatching success, and even resilient species may experience changes in eggshell shape and reduced hatchling mass due to variations in humidity during incubation (Delmas et al., 2008; Petrov et al., 2023; Fordham et al., 2006; Bock et al., 2021). In the Amazon region, the hatching rate of P. unifilis declined in the lower sections of beaches due to nest flooding in the Javaés River (Ferreira Júnior & Castro, 2010). Conversely, in the Iriri River, no nest loss from flooding was recorded in 2012 and 2013, as this area corresponds to the upstream portion of the Xingu basin, where tidal influences are minimal (ICMBIO, 2015). While these elevated areas can reduce the risk of nest flooding, they typically have lower moisture levels than shallow grounds, which can also affect embryo development, especially in coarse sand substrate (Packard et al., 1987). Although this behavior may seem contradictory regarding substrate type, nesting in elevated areas can enhance hatching success when river levels rise at the end of the nesting season, as observed for this species in Venezuela (Escalona et al., 2019). Despite the absence of nest mortality due to flooding, we noted other factors influencing embryo survivorship.

This study recorded undeveloped eggs in the P. unifilis nests. The presence of such eggs in freshwater turtle nests is typically associated with infertility, insufficient nest temperatures for complete development, and heat stress (Santoro et al., 2023; Zappalorti et al., 2017). For Glyptemys muhlenbergii, approximately 10% of the eggs failed to hatch due to these factors (Knoerr et al., 2021). Previous research has noted the occurrence of undeveloped eggs in other Amazonian oviposition sites in low frequencies (Carvajal et al., 2011; Pignati et al., 2013a). Unhatched eggs are not extensively studied in freshwater turtles, yet they may serve as important indicators of skewed adult sex ratios and declining population health (Pearse et al., 2010; Roques et al., 2006; Zhang et al., 2015). Additionally, rotten eggs were found in nests along the Iriri River, similar to observations in other freshwater turtles, where they often consist of broken eggshells that have remained in the egg chamber for extended periods (Walde et al., 2007). Shallow egg chambers experience greater temperature fluctuations, which can either lead to embryo mortality or accelerate decomposition (Micheli-Campbell et al. 2011). Furthermore, these conditions can attract predators, such as Sarcophagidae fly larvae, drawn by the olfactory cues from the nests (Holden et al., 2021; Riley & Litzgus, 2014).

Similar to our findings, Sarcophagidae fly larvae have been documented consuming the eggs and hatchlings of other freshwater turtles, such as Graptemys ouachitensis in the Wisconsin River (Geller, 2022), and Chysemys picta in the water bodies of Algonquin Provincial Park (Riley et al., 2014). These larvae can detect the chemical scents of carcasses and burrow into nests to reach the egg chamber (Bolton et al., 2008). While they prefer necrotic tissues, Sarcophagidae larvae may opportunistically prey on live embryos and hatchlings. Previous studies have shown that fly larvae inside freshwater turtle nests can lead to decreased hatching success (Saumure et al., 2006). Despite the presence of fly larvae, our study observed a low proportion of predated nests compared to other P. unifilis nesting sites in the Amazon basin. For instance, in the Nichare-Tawandu rivers, 14.1% of nests were predated by animals (Escalona & Fa, 1998), 10% of the nests were affected in Solimões River (Fachín Terán & von Mülhen 2003), and 2.7% in the Araguari River (Arraes & Tavares-Dias, 2014). Predators are adapted to use visual and olfactory cues to identify nests, such as the red fox (Vulpes vulpes) for nests of Chelodina colliei (Dawson et al., 2014). In the Amazon region, the most recorded predator of P. unifilis nests is the lizard genus Tupinambis, though hawks, vultures, ants, and monkeys also pose threats (Ferreira Júnior & Castro, 2003; Pantoja-Lima et al., 2009a; Salera Junior et al., 2009). Some predation incidents were linked to the nest’s proximity to vegetation, as certain predators are sensitive to high surface temperatures on sandbanks (Erickson & Baccaro, 2016). Although some nests in our study area were located near shrub vegetation, this may not have been sufficient to buffer the surface temperature, which prevented predation. Despite being a crucial food source for wildlife, freshwater turtles are also vital for human populations.

Amazon riverine populations have relied on freshwater turtle meat and eggs for subsistence across generations (Chaves et al., 2020; Mittermeier, 1978; Pezzuti et al., 2010; Stanford et al., 2020). In the Nichare-Tawandu rivers, 84.9% of the nests were harvested by humans (Escalona & Fa, 1998), and 75.5% were collected in the Araguari River (Arraes & Tavares-Dias, 2014). Although human collection remains the primary threat to this species throughout its distribution (Ferreira Júnior & Castro, 2010; Pantoja-Lima et al., 2014; Quintana et al., 2019), the low human population density and the distance from urban centers at our study site (ICMBIO, 2015) may account for the reduced number of collected nests in the area. Additionally, the coarse sand nesting sites in the Iriri River likely complicate the identification of nest locations, as female tracks are more easily observed in fine sand substrates (Michalski et al., 2020).

Environmental characteristics significantly influence the sex ratio of offspring. This study found an overall sex ratio of 100% biased toward females in the P. unifilis population. The sex determination of freshwater turtles is driven by the populational reaction norm, which involves the interaction between the pivotal temperature (the temperature that produces equal proportions of males and females) and the transitional range of temperatures (the range that yields both sexes in varying proportions) (Girondot, 1999). Freshwater turtles with a narrow transitional temperature range may be more susceptible to climate change, as extreme temperatures experienced by embryos within nests can exceed this range, resulting in single-sex clutches (Hulin et al., 2009; Valenzuela et al., 2019; Camillo et al., 2022). For P. unifilis, no studies have specifically identified the pivotal temperature or the transitional range, apart from Hulin et al. (2009), which reported high data variability and excluded species information from the overall model.

Although the present study did not assess temperature variation within nests, the environmental characteristics of the study area likely increased the internal egg chamber temperature, potentially exceeding the transitional range for P. unifilis and leading to female-only production. In artificially incubated Chrysemys picta nests, frequent exposure to excessively high temperatures resulted in embryo feminization or mortality (Valenzuela et al., 2019). Some researchers question whether the behavioral plasticity of female nest site selection can sufficiently compensate for the extreme conditions caused by temperature fluctuations inside nests (Refsnider & Janzen, 2012; Roberts et al., 2023). Although the habitat sampled in the Iriri River was relatively homogeneous, variations in nest microhabitats were observed. Some nests were located near shrub vegetation and rocks or were shaded by canopy cover, which tends to lower nest temperatures (Janzen, 1994). Despite this, no variation in the sex ratio was noted. The occurrence of single-sex clutches in nature is rarely recorded for freshwater turtles (Leivesley et al., 2022; Spencer & Janzen, 2014), suggesting that the Iriri River population may be experiencing extreme temperatures that override the effects of microhabitat gradients.

The sex ratio of P. unifilis varies between years and according to nest site conditions across the Amazon basin. For instance, in the Purus River, nests incubated in sandbanks exhibited a female-biased sex ratio, while those incubated in clay soils showed a male-biased ratio (Erickson et al., 2020). In the lower Amazon, the sex ratio was female-biased in 2007 but shifted to male-biased in 2009 (Pignati et al., 2013a). Although the sex ratio fluctuates annually in response to regional conditions, high-temperature fluctuations on coarse sand nesting sites likely contribute to increased internal temperatures during the incubation period, resulting in a female-biased sex ratio. (Refsnider et al., 2013; Erickson et al., 2020). For related species, Podocnemis sextuberculata has a pivotal temperature of approximately 33.73°C and a narrow transitional temperature range of 1.16°C, indicating potential vulnerability to climate change(Camillo et al., 2022). Studies predict that rising temperatures associated with climate change may drastically alter the population structure of TSD species (Gallego-García & Páez, 2016; Refsnider et al., 2013; Telemeco et al., 2013). A population exhibiting a biased sex ratio may face decreasing genetic variability, reduced recruitment of mature individuals, and declining fecundity (Topping & Valenzuela, 2021).

To interpret our results accurately, it is crucial to note that during fieldwork, residents identified only the most significant nesting sites for our survey as sandy beaches. At the end of our fieldwork, locals mentioned clay banks as occasionally used nesting grounds for females. If these nesting areas had been sampled, our findings might have aligned with those of Erickson et al. (2020), who reported a predominance of female-biased nests on sandy beaches and male-biased nests on clay areas, potentially balancing the overall sex ratio. This perspective is further supported by Miorando et al. (2015) study, which documented a male-biased adult sex ratio of P. unifilis in the Iriri River. Although our surveys were limited to sandy beach areas, this does not undermine the significance of our findings regarding the nesting behavior and adaptability of P. unifilis in such environments. In contrast to our results, Erickson et al. (2020) observed only one single-sex nest in sandy areas. This discrepancy underscores the importance of long-term monitoring of this population to understand the resilience and impacts of climate change and habitat alterations on reproductive parameters.

Our results indicate that the construction of deeper nests appears to be successful, as the mean hatching rate was comparable to that of other populations. However, the sex ratio was not balanced. A deeper egg chamber may reduce temperature variation and work as an adaptation to achieve a more favorable sex ratio, resulting in a higher proportion of male hatchlings (Doody et al., 2004; Erickson et al., 2020; Spencer & Janzen, 2014). Although females can adjust the size of the egg chamber, the extent of nest depth is limited by the individual’s size, highlighting the vulnerability of small species (Morjan, 2003). Therefore, while deeper nests may enhance survivorship by mitigating temperature fluctuations, this adaptation might not be enough to achieve a balanced sex ratio.

Understanding the limitations of species’ behavioral plasticity is crucial in the context of climate change. In the future, the southern Amazon is expected to be one of the most affected regions, with predictions of decreased rainfall and altered river flows (Brêda et al., 2020; Sorribas et al., 2016). These changes may significantly impact freshwater turtles by reducing the availability of nesting areas due to flooding, increasing temperatures, and lowering humidity—all of which can adversely affect embryo development and alter the sex ratio balance (Butler, 2019; Eisemberg et al., 2016). Previous research has characterized P. unifilis as a generalist in nesting site selection, suggesting some resilience to environmental fluctuations (Erickson et al., 2020; Escalona et al., 2019; Pignati et al., 2013b). However, our findings highlight the limits of this resilience, indicating that certain environmental pressures and adaptive strategies may not be sufficient to sustain natural reproductive patterns (Topping & Valenzuela, 2021). Therefore, further research into the life story of species, such as the assessment of population structure and reproductive aspects, may be useful for estimating the impact of climate change on species (Butler, 2019).

Given that freshwater turtles are culturally significant to riverine populations and play an important ecological role, species conservation is a priority for local communities in the Amazon (Pezzuti et al., 2018; Freitas et al., 2020). Nesting site management is the most common strategy for protecting freshwater turtle reproductive events throughout the Amazon region. Information regarding reproductive success and the species’ capacity to adapt to various nesting habitats, as well as changing environments, is essential for effective conservation planning (Lubchenco et al., 2019). Understanding how populations interact with their environment can inform efficient conservation actions and foster community engagement through co-management plans tailored to the specific needs of each nesting area (Lubchenco et al., 2019). Additionally, monitoring species across their distribution serves as an indicator of environmental impacts on populations, highlighting areas that require protection and conservation (Hoffmann & Sgró, 2011). Future studies should prioritize data collection over consecutive years and in different areas along the Iriri and Xingu rivers to elucidate patterns related to habitat gradients and the influence of climate change, deforestation, agriculture, and dams on the population ecology of freshwater turtles.

Supplementary Material

The following online material is available for this article:

Table S1 – Descriptive statistics of the granulometric fractions proportion of the monitored Podocnemis unifilis nests.

Figure S1 – Model assumptions of the Podocnemis unifilis nests hatching rate by the effect of egg chamber depth + nest height utilizing the quasibinomial distribution on GLM.

Figure S2 – Model assumptions of the proportion of rotting eggs in the P. unifilis nests by the effect of egg chamber depth utilizing quasibinomial distribution on GLM.

Figure S3 – Model assumptions of the proportion of eggs consumed by Sarcophagidae fly larvae in the Podocnemis unifilis nests by the effect of egg chamber depth utilizing the quasibinomial distribution on GLM.

Acknowledgments

We are grateful to the University of Pará and the Núcleo de Ecologia Aquática e Pesca da Amazônia (NEAP) for making available the laboratory for the analyses and ICMBio for logistic and financial support.

Data Availability

All data supporting the results in papers published in the journal must be archived in an appropriate public archive offering open access and guaranteed preservation (https://www.scielo.br/journal/bn/about/#data-availability).

The datasets generated during and/or analyzed during the current study are available at: https://doi.org/10.000001/example.dataset

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Edited by

  • Associate Editor
    Pedro Nunes

Publication Dates

  • Publication in this collection
    10 Jan 2025
  • Date of issue
    2024

History

  • Received
    08 May 2024
  • Accepted
    25 Oct 2024
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E-mail: contato@biotaneotropica.org.br
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