Amazonian Turtles Research Articles

Riverscape features determining the genetic structure of the Yellow‐Spotted Amazon River Turtle (Podocnemis unifilis) in Brazilian Amazonia

AbstractLandscape characteristics can influence gene flow depending on the species ability to disperse. This imposes different levels of resistance to movement, determining the genetic structure and diversity of populations. Waterfalls and rapids in the Amazon basin have been suggested as contributing factors to the diversification and genetic structure of freshwater species, including turtles. Thus, along some main rivers of the Brazilian Amazon: Juruá, Madeira, Amazonas, Trombetas, Tapajós, Xingu, Tocantins, and Araguaia, we evaluated the spatial distribution of genetic diversity and characterized the population structure of Podocnemis unifilis, a widely distributed and endangered Amazonian turtle, using the mitochondrial DNA control region. We tested for isolation by geographic distance and by resistance models through an integrative approach using genetic, geographic, and ecological data, comparing these matrices with genetic distance. We found heterogeneous levels of genetic diversity and no spatial patterns. Results supported the isolation by resistance hypothesis, where the movement of individuals was influenced by freshwater, vegetational, climatological, and geomorphological variables, explaining the genetic distance of P. unifilis. Rapids and waterfalls impose greater resistance although they are barriers with different levels of permeability to the P. unifilis gene flow. Thus, the idiosyncrasies of each sub‐basin must be considered in the interpretation of the patterns found in assessing phylogeographic history.Abstract in Portuguese is available with online material.

Priority areas and integrated actions for the conservation of Amazonian turtle populations historically over-exploited by humans

The definition of priority areas for conservation and integrated management actions are essential for the effective maintenance and recovery of natural populations, especially for species overexploited by humans. Amazonian chelonians are a food resource historically used by people, resulting in the decline of species populations and worsening the risk of local extinctions. In this paper, we establish priority areas and define integrated conservation actions for populations of three Amazonian chelonians most threatened by human consumption in Brazil (Podocnemis expansa, P. unifilis and P. sextuberculata). To do so, we used 15 prioritization criteria (ecological, logistical and socioeconomic) estimated with 30 years monitoring data in 15 areas by the Amazon Chelonian Program (in portugues Projeto Quelonios da Amazonia, PQA). Each criterion presented four levels of priority with scores increasing according to the relevance for conservation of chelonian populations. The sum of the scores obtained in each area of the PQA allowed a ranking and four categories of importance for conservation to be defined. We also analyzed the similarity of scores among areas of the PQA and among the prioritization criteria to evaluate the application of integrated conservation action strategies. The areas of PQA were classified as Extremely Important for Conservation (Rebio Trombetas River, Middle Xingu River, Middle Araguaia River, Upper Guaporé River), Very Highly Important for Conservation (Middle Purus River, Middle Juruá River, Crixás-Açu River Mouth, Sub-middle Tapajós River); Highly Important for Conservation (Sub-Middle Araguaia River, Amazonas River Mouth, Middle Mortes River); and Important for Conservation (Middle Guaporé River, Lower Branco River, Flechal River, Afuá River). The prioritization and similarity analyses can support the development of a national integrated plan of conservation actions to reduce the overexploitation of Amazon chelonian populations, according to the ecological, logistical and socioeconomic needs of each PQA area.

The exposure in ovo of embryos belonging to Amazonian turtle species Podocnemis expansa (Testudines) to commercial glyphosate and fipronil formulations impairs their growth and changes their skeletal development

Pesticides are widely used in agricultural production; moreover, they can have direct and indirect effect on both flora and fauna. Aquatic organisms, among other animals, including reptiles, are mainly susceptible to contamination effects. Accordingly, the aim of the present study is to test the hypothesis that the incubation of Podocnemis expansa eggs in substrate added with glyphosate and fipronil formulations changes their viability, interferes with their growth and induces bone alterations. Eggs collected in natural environment were artificially incubated in sand moistened with water added with glyphosate Atar 48, at concentrations of 65 or 6500 μg/L (groups G1 and G2, respectively), and with fipronil Regent 800 WG at 4 or 400 μg/L (groups F1 and F2, respectively) or, yet, with the combination of 65 μg/L glyphosate and 4 μg/L fipronil, or with 6500 μg/L glyphosate and 400 μg/L fipronil (groups GF1 and GF2, respectively). The level of exposure to the herein assessed pesticides was quantified at the end of the incubation period; it was done by dosing its concentration in eggshells. Eggs exposed to the tested pesticides did not have their viability affected by it; however, all embryos exposed to the tested pesticides showed lowered body mass at hatch, as well as impaired development. In addition, bone malformation in the scleral ossicular ring was observed in individuals in groups F1, F2 and GF1. Pesticides accumulated in eggshells at concentrations related to exposure level. Thus, the recorded results have evidenced some remarkably relevant, and previously unknown, impacts associated with the exposure of a species listed as lower risk/conservation dependent, which spends most of its life in the water, to two widely used pesticides, at a very sensitive stage of its life, namely: egg incubation on land.

Exposure in Ovo to Commercial Glyphosate and Fipronil Formulations Impairs the Growth and Changes the Bone Development of Amazonian Turtle (Podocnemis Expansa, Testudines) Embryos

Exposure in Ovo to Commercial Glyphosate and Fipronil Formulations Impairs the Growth and Changes the Bone Development of Amazonian Turtle (Podocnemis Expansa, Testudines) Embryos

Neonatal biometry and characterization of Amazonian Turtle nests (Podocnemis expansa)

The present study aimed to study the reproduction of the Amazon turtle (Podocnemis expansa) through the evaluation of the reproductive parameters of adult females. This study was carried out in the Crixás-Açu River, municipality of Mundo Novo, state of Goiás, Brazil. In September, the biometrics of 20 females were evaluated during the spawning period. Their nests were marked for subsequent evaluation of hatchlings, measuring the distances of each nest to the river and vegetation. The second stage consisted of the evaluation of hatchlings and characterization of nests after egg hatching. The data were tested using the Pearson Correlation to measure the degree of linear correlation between the variables analyzed, such as the parameters of females, hatchlings, nests, and eggs. Nest depth was positively correlated with the number of eggshells found. We also found a correlation between the number of eggsshells and the distance of nests to the vegetation. Although moderate, this result indicates that as the distance to the vegetation increases, the number of eggshells found in nests decreases. The spawning site for Amazon turtle breeding is crucial to determine a higher number of eggs hatching and better development of hatchlings. However, the literature is still very scarce regarding the choice of spawning grounds and the influence that vegetation may have on the development of freshwater turtle hatchlings in Brazil.

Hematologycal and blood biochemistry parameters of captive big-headed amazon river turtles, Peltocephalus dumerilianus (Testudines: Podocnemididae)

The determination of hematological values is used to obtain knowledge about the health conditions of animal species. The big-headed Amazon River turtles, (Peltocephalus dumerilianus)are considered one of the least known testudine species concerning their biology and health status. Herein, we determined the hematological and plasma biochemical parameters of 17 (eight males and nine females) adult P. dumerilianusto provide reference interval values for clinically healthy individuals. We collected the blood samples by puncturing the femoral vein using long heparinized hypodermic syringes. Sexual dimorphism for individuals was determined by external observation of the shape of the plastron. The average values obtained for the ten hematological and biochemical parameters analyzed were red blood cell count = 0.32 million µL-1; hematocrit = 20.6 %; hemoglobin = 8.5 g dL-1; mean corpuscular volume = 681.6 fL; mean corpuscular hemoglobin = 267.8 pg; mean corpuscular hemoglobin concentration = 41.9 g dL-1; glucose = 80.6 mg dL-1, total protein = 4.1 g dL-1, triglycerides = 388.9 mg dL-1, and total cholesterol = 79.3 mg dL-1. Despite the sexual dimorphism evidenced for the species, there was no significant statistical difference between males and females for both hematological and biochemical parameters analyzed herein. Based on these results, the population is considered healthy, with parameter values coinciding with previously reported reference ranges for testudines species in the region. The results obtained in this study can be used for assessing the health status of other Amazonian turtle populations, especially in actions aimed at cultivation strategies, management, and species conservation.

Transplantation of nest of amazonian turtle Podocnemis expansa (Schweigger, 1812)

The main objective of this study is to analyze the effectiveness of the Podocnemis expansa nest transplantation technique used to aid in the conservation of the species, aiming to increase the number of individuals in nature. The Amazonian turtle is famous for its large size and commercial attractiveness, being the target of rampant hunting, mainly by populations that depend on the species economically. In September 2018, natural nests of P. expansa that were in areas of flood risk were excavated and transplanted into new nests constructed by the team. At the same time, the breeding females had their dimensions verified, as well as their respective eggs. In the second stage of the experiment, which occurred in November of the same year, the nests previously transplanted were counted, including the amount of eggshell, indicating how many eggs hatched, and measuring the size of the newborns, besides the presence of deformities. The sand collected from the bottom and surface of the natural and transplanted nests were analyzed by sieving. Through Pearson's correlation, the data were tested and related. No significant relationships were found between the birth rate and the grain size of the nests, which shows that grain size did not influence the success of hatching in the present study. It was found a strong relation (r = 0.80) between the number of eggs and the percentage of deformities of each transplanted nest, showing that the presence of deformed individuals in turtle nests is natural.

Mutagenic, genotoxic and morphotoxic potential of different pesticides in the erythrocytes of Podocnemis expansa neonates

Despite the damaging effects of pesticides glyphosate (Gly), atrazine (Atra) and fipronil (Fip) on different organisms, the mutagenic, genotoxic and morphotoxic potential of testudine erythrocytes in freshwater remains unknown. Thus, the aim of the present study is to assess the toxicological potential of these compounds in Podocnemis expansa (Amazonian turtles) neonates from eggs artificially incubated in substrate at different concentrations of herbicides Gly and Atra and insecticide Fip. Micronucleus test and other nuclear abnormalities, as well as comet assay and morphometric measurements taken of models' circulating erythrocytes were used as toxicity biomarkers. Pups exposed to Gly (groups Gly-65 ppb and Gly-6500 ppb) were the ones recording the largest amount of nuclear abnormalities; erythrocytes with multilobulated, notched and displaced nucleus were mostly frequent in groups Atra-2 ppb and Gly -65 ppb. All treatments (Gly-6500 ppb, Atra-2 ppb, Atra-200 ppb, Fip-4 ppb and Fip-400 ppb), except for group Gly-65 ppb, led to decreased erythrocyte area, increased “nuclear area: erythrocyte area” ratio, as well as to decreased erythrocyte and erythrocyte nuclei circularity, which highlights the clear effect on the size and shape of these cells. On the other hand, the comet assay did not evidence any genotoxic effect caused by the assessed pesticides. This is a pioneer study on the mutagenic and morphotoxic potential of pesticides in P. expansa eclodides exposed in ovo to Gly, Atra and Fip; therefore, it is an insight on how these compounds can affect the health of these animals.

Evolutionary insights in Amazonian turtles (Testudines, Podocnemididae): co-location of 5S rDNA and U2 snRNA and wide distribution of Tc1/Mariner.

ABSTRACTEukaryotic genomes exhibit substantial accumulation of repetitive DNA sequences. These sequences can participate in chromosomal reorganization events and undergo molecular cooption to interfere with the function and evolution of genomes. In turtles, repetitive DNA sequences appear to be accumulated at probable break points and may participate in events such as non-homologous recombination and chromosomal rearrangements. In this study, repeated sequences of 5S rDNA, U2 snRNA and Tc1/Mariner transposons were amplified from the genomes of the turtles, Podocnemis expansa and Podocnemis unifilis, and mapped by fluorescence in situ hybridization. Our data confirm the 2n=28 chromosomes for these species (the second lowest 2n in the order Testudines). We observe high conservation of the co-located 5S rDNA and U2 snRNA genes on a small chromosome pair (pair 13), and surmise that this represents the ancestral condition. Our analysis reveals a wide distribution of the Tc1/Mariner transposons and we discuss how the mobility of these transposons can act on karyotypic reorganization events (contributing to the 2n decrease of those species). Our data add new information for the order Testudines and provide important insights into the dynamics and organization of these sequences in the chelonian genomes.

Opinion 2431 (Case 3587) – Podocnemis unifilis Troschel, 1848 (Reptilia, Testudines): precedence given over Emys cayennensis Schweigger, 1812

The International Commission on Zoological Nomenclature has conserved the usage of the specific name of Podocnemis unifilis Troschel, 1848 for a widely distributed species of Amazonian turtle, by giving it precedence over its rarely used senior subjective synonym Emys cayennensis Schweigger, 1812 (currently Podocnemis cayennensis).

Model-based riverscape genetics: disentangling the roles of local and connectivity factors in shaping spatial genetic patterns of two Amazonian turtles with different dispersal abilities

Genetic patterns are shaped by the interaction of different factors such as distance, barriers, landscape resistance and local environment. The relative importance of these processes may vary for species with different ecological traits. Here we compared two related Amazonian riverine turtle species (Podocnemis erythrocephala and Podocnemis sextuberculata) with distinct dispersal abilities to assess how differently local and connectivity variables influence their genetic patterns. We used a total of 609 genetic samples to estimate mitochondrial (mtDNA) genetic diversity and differentiation for each locality. We applied model selection on models associating genetic diversity to local variables representing hypotheses of climate and primary productivity, water level variation, hunting pressure and downstream increase in genetic diversity. We modeled the relationship of genetic differentiation with connectivity variables representing hypotheses of isolation by distance (IBD), isolation by resistance (IBR) and isolation by barrier (IBB). Model selection for genetic diversity was only important (excluded the null model) for the high-dispersal species (P. sextuberculata), with best models including hypotheses of productivity and hunting pressure. Genetic diversity was higher in more productive sites and in sites with higher concentration of villages (opposed to expected). Although a variable importance testing showed low importance for connectivity models, IBB (Amazon River) and IBR (resistance by current and past climatic suitability and river color) models explained more genetic differentiation turnover than IBD (riverway distance). Models explained a higher percentage of genetic differentiation for the low-dispersal species (P. erythrocephala), with Amazon River as main predictor. We show that, although local variables are often overlooked in riverscape genetics studies, they can influence intrapopulacional genetic diversity of aquatic species, even those with high dispersal ability. By applying a resistance-model framework and by using riverscape genetics factors relevant in basin-wide context, we provide a novel approach to investigate genetic patterns of other aquatic vertebrates in fluvial systems.

Nesting and neonates of the yellow-spotted river turtle (Podocnemis unifilis, Podocnemididae) in the Araguari River basin, eastern Amazon, Brazil

Predation and alteration of microhabitats may represent high risk for nesting of Amazonian turtles. This study aimed at investigating the nesting and body parameters of neonates of Podocnemis unifilis in the Araguari River basin, State of Amapá, Brazil. The spawning sites of this turtle were monitored along the Falsino River (a region with two reserves) and in the urban area of the Porto Grande city along the Araguari River, from August to December 2011. A total of 180 nests were found and the nesting occurred from September to November, with prevalence in October. Eggs hatching occurred in December. The mean incubation period was 63.5 ± 5.2 days and the eggs hatching success was 25%. However, approximately 80% of the nests had suffered predation mainly by humans, which occurred in both the protected areas of the reserves and the urban area. The pattern of nesting site choice was discussed. Egg size was larger than that previously described for the same turtle species in the other regions. The body condition index of neonates indicated a good use of vitelline reserves. The results indicate the urgent need for strategic actions to conserve and maintain the natural stocks of this relatively vulnerable turtle in the region.

Case 3587 Podocnemis unifilis Troschel, 1848 (Reptilia,Testudines): proposed precedence over Emys cayennensis Schweigger, 1812

The purpose of this application, under Article 23.9.3 of the Code, is to conserve the specific name Podocnemis unifilis Troschel, 1848, for a widely distributed species of Amazonian turtle (family podocnemididae) of both economic and conservation importance, by giving it precedence over its infrequently used senior synonym Podocnemis cayennensis (Schweigger, 1812). This species, the Yellow-spotted River Turtle, has long been referred to as P. unifilis by the IUCN Red List and CITES, as well as in at least 200 scientific publications over more than a century, whereas the name P. cayennensis has only been applied to this species in very few recent publications. Prior to 1974, the name cayennensis had usually been used incorrectly for another species, the Red-headed River Turtle, Podocnemis erythrocephala (Spix, 1824), as noted and corrected by Mittermeier & Wilson (1974) and Pritchard & Trebbau (1984). The conservation of the binomen P. unifilis will stabilize the use of a name that has been in general use for this species in the vast majority of the scientific publications, government documents, endangered species lists, and the general literature for over 100 years. Giving precedence to the older name (cayennensis) would be counter to usage, and would create much confusion in the literature.

Tursiocola podocnemicola sp. nov., a new epizoic freshwater diatom species from the Rio Negro in the Brazilian Amazon Basin

Tursiocola podocnemicola sp. nov. is described from the Amazonian Rio Negro Basin in Brazil where it was found living epizoically on the carapaces of the freshwater turtle Podocnemis erythrocephala Spix. The detailed morphology of this epizoic diatom is examined using both light and scanning electron microscopy and compared with similar species of the genera Tursiocola Holmes, Nagasawa & Takano and Epiphalaina Holmes, Nagasawa & Takano. Specimens of this epizoic diatom belong to the genus Tursiocola, characterized by the presence of extensive pseudosepta, covering part of the apices and continuing along the mantle margin to merge with the stauros, uniseriate striae and two knob-like structures between the internal central raphe endings. However, the new species has a different external raphe structure when compared with all other species described from the mentioned genera, with unilaterally, strongly deflected, proximal raphe endings. The ecology and possible origin of the species on the Amazonian turtle's carapace is briefly discussed.

Pharmacological restraint of captivity giant Amazonian turtle Podocnemis expansa (Testudines, Podocnemididae) with xylazine and propofol

Identify a technique to induce brief sedation and hypnosis in Podocnemis expansa. Twenty commercially bred P. expansa, weighing on average 1.2 +/- 0.24 kg, were subjected to two protocols: G1 was given 1.5 mg/kg IM of xylazine and 5 mg/kg IV of propofol, while G2 received 1.5 mg/kg IM of xylazine and 10 mg/kg IV of propofol. The drugs were applied, respectively, in the left thoracic member and in the cervical vertebral sinus. Assessments were made of the anesthetic parameters of locomotion, muscle relaxation, response to pain stimuli in the right thoracic members, pelvic members and tail, easy handling and heartbeat, as well as ambient temperature and glycemic level. A consistent hypnotic effect was recorded 49.6 +/- 22.1 seconds in G2 and after 58.2 +/- 55.1 in G1. All the animals of G2 recovered in 198 minutes, and those of G1 in 156 minutes. The hypnosis achieved with these associations was satisfactory, and G1 was as efficient as G2, allowing for the pharmacological restraint for the collection of biological samples, physical examinations and minor surgeries on these species.

Crescimento ponderal de filhotes de tartaruga gigante da Amazônia (Podocnemis expansa) submetidos a tratamento com rações isocalóricas contendo diferentes níveis de proteína bruta

A criação de Podocnemis expansa, a tartaruga-da-amazônia, com finalidade comercial foi implantada no Brasil em 1992. Contudo, muitas questões acerca do manejo, da nutrição, da sanidade e, principalmente, da reprodução ainda são obscuras. Visando contribuir para o desenvolvimento de uma metodologia alimentar da espécie, objetivou-se testar diferentes níveis de proteína da dieta. Uma amostra de 480 animais neonatos de, aproximadamente, um mês de vida foram trazidos de uma área de proteção localizada no rio Araguaia no Estado Goiás para o Núcleo de Pscicultura Experimental/UFG. Os animais foram divididos em seis grupos de 80 animais e colocados em caixas de água de 500 litros. Cinco grupos receberam rações formuladas com diferentes teores de proteína bruta (PB) vegetal: PB 18% (PB18), PB 21% (PB21), PB 24% (PB24), PB 27% (PB27) e PB 30% (PB30), enquanto o outro grupo (PBA30) recebeu ração comercial para peixes contendo proteína de origem animal (30% de PB). Bimestralmente, foram realizadas biometrias para determinação das medidas de comprimento (CC) e largura da carapaça (LC), comprimento da carapaça (CP) e largura do plastrão (LP) e do peso corporal (PC). O experimento demonstrou superioridade do tratamento PBA30 em todas as medidas estudadas, seguidos seqüencialmente pelos tratamentos PB30, PB27, sem diferenças significativas entre estes grupos. Os piores resultados foram para os grupos PB24, PB21 e PB18, que não diferiam entre si. Filhotes de P. expansa nos dez primeiros meses de vida alimentados com dietas contendo elevados percentuais de proteína bruta (acima de 27%) respondem melhor em termos de crescimento e ganho de peso que aqueles alimentados com dietas com percentuais mais baixos. A dieta contendo proteína bruta de origem animal apresentou melhores resultados que as de origem vegetal.

Conservation and management strategies for commonly exploited amazonian turtles

In the Amazon, turtle hunting is more than simply a method of obtaining meat, it is a way of life and part of local culture. To reduce the illegal catch of Amazonian freshwater turtles knowledge about the ecology of the species is needed to establish conservation and management strategies. The exploited species have a high reproductive potential but a large percentage of the hatchlings are consumed by predators (mainly fishers) if left without proper management. It is suggested that a proportion of the hatchlings should be collected on the nesting beaches and subsequently raised in semi-natural conditions for later releases into lakes. This should be done at regular intervals to produce a commercial harvest after 8 years. Such a strategy would provide an economic incentive to protect and maintain wild populations as sources of hatchlings.