Justification
We assess Rhinoclemmys punctularia as Near Threatened (NT) based on past (three generations, ca 40 years) and ongoing habitat loss and actual or potential levels of exploitation (criteria A2cd+4cd). The species uses a wide variety of water bodies in forested habitats (tropical rainforest, tropical moist forest), as well as more open habitats in the cerrado, savanna-forest ecotone, coastal restinga in Brazil, and it is also known from areas of non-saline coastal marsh. Despite this wide array of habitats, R. punctularia has been facing significant habitat loss and degradation. Although our models indicated only a 13% loss or alteration of habitat for its global distribution, the populations in northeastern and southeastern Brazil are located in the Atlantic Forest, an area where habitat loss is over 40%. Taking the documented habitat losses into account and the continuing and projected losses to Amazonian forests, as well as the taxonomic uncertainty associated with apparently isolated subpopulations in several areas subjected to varying threats, we assess R. punctularia as NT at this time. It was previously assessed as Least Concern by the TFTSG (Behler 1996), and therefore was not published on the Red List at that time.
Geographic Range Information
The distribution of Rhinoclemmys punctularia is in northeastern South America, where it is widely distributed from eastern Venezuela and Trinidad and Tobago through Guyana, Suriname, French Guiana, and into Brazil in the eastern Amazon Basin, with additional disjunct subpopulations in the Atlantic Forest along the Brazilian east coast (Pritchard and Trebbau 1984, Ernst and Barbour 1989, Rueda-Almonacid et al. 2007, Ouboter et al. 2007, Ferrara et al. 2017, TTWG 2021). There is also a disjunct subpopulation in southwestern Venezuela considered a separate subspecies, R. p. flammigera (see Figure S1 in the Supplementary Information). In Brazil, besides occurring in the northern and eastern portions of the Amazon Basin, it also occurs in the hydrographic basins of the Tocantins-Araguaia, western northeast Atlantic, Parnaíba, eastern northeast Atlantic, eastern Atlantic, and southeast Atlantic. Some of these records refer to populations in the northeastern region (Valle et al. 2016) and southeastern region of Brazil (Siciliano et al. 2014, Oliveira et al. 2018). These subpopulations are apparently disjunct (Valle et al. 2016) and possibly a separate species (Oliveira et al. 2018). The states within Brazil that are considered part of the natural distribution of R. punctularia include Amapá, Amazonas, Bahia, Espírito Santo, Maranhão, Pará, Piauí, Roraima, and Tocantins.
Ferrara et al. (2017) calculated the total distribution range of R. punctularia in the Amazon Basin to be 3,267,963.86 sq. km. In Brazil, the country with the highest distribution percentage (71%), its range was estimated at 1,681,987 sq. km (Vogt et al. 2023). However, using a tighter estimated distribution shell around known localities, TTWG (2021) calculated the estimated historical indigenous range (area of occupancy, AOO) as approximately 2,163,814 sq. km, and the estimated historical indigenous extent of occurrence (EOO), calculated as a minimum convex polygon according to IUCN protocol, as approximately 5,992,970 sq. km (TTWG in press). The current AOO is significantly smaller than the historical indigenous range. The species has been recorded at elevations from 2 to 310 m asl (Freitas et al. 2017, Garcia-Passos et al. 2018).
Population Information
In Brazil, a large population of Rhinoclemmys punctularia was studied by Wariss et al. (2012) on Algodoal-Maiandeua Island, Maracanã, Pará. Of 169 individuals recorded (45.3% females, 43.2% males, and 11.5% juveniles), 14 individuals were recaptured, and the sex ratio was not different from 1:1. The occurrence of the species was higher in coastal plain lakes (0.017 individuals captured per hour) compared to the “igapós” (name for flooded forest in the Amazon; 0.0025 individuals per hour; Wariss et al. 2012). The capture rate was negatively affected by salinity, with no individuals recorded in locations with salinity higher than zero. This result was attributed to the lack of specializations for osmoregulation and also to the scarcity of food in the tidal channels. However, the study indicated that R. punctularia may inhabit aquatic habitats with widely varying pH values within its geographic distribution. There are also records of individuals moving up to 600 m between lakes of the coastal plain and temporary pools formed around the lakes during the rainy season (Wariss et al. 2012). Small populations were also investigated in Pará, one in a small stream in the Tocantins basin (14 individuals), and another in several small water bodies in the Tapajós basin (29 individuals; Brito et al. 2022). Among the individuals captured in the two populations, 89% were adults and the sex ratio did not differ from 1:1 in both populations. The carapace length distribution did not vary between the two areas and tended to be normal in the Tapajós basin, where most captured individuals had carapace lengths between 16.0 and 19.9 cm (Brito et al. 2022). The capture effort per individual varied between populations; in the Tocantins population, one individual was captured per 286 trap-hours, while in the Tapajós, a much higher effort of 2,681 trap-hours was required to capture a single individual. Despite sampling in various water bodies, 100% of the turtles captured in the Tocantins occurred in a first-order stream. In contrast, in the Tapajós, turtles were found in seven water bodies, with 44% of captures occurring in first-order streams, 31.5% in third-order streams (both dammed and not dammed), and 20% in second-order streams. There was no difference in captures among the various water body categories in the Tapajós, suggesting that the species does not have a preference among the investigated stream categories (first-order, second-order, third-order small streams, sixth-order, and lentic streams; Brito et al. 2022). Rhinoclemmys punctularia occurred in syntopy with other turtle species (Chelidae and Kinosternidae); however, it was always the most abundant species in the locations where it occurred (Brito et al. 2022). Despite the dry season showing higher capture rates of R. punctularia, neither Wariss et al. (2012) nor Brito et al. (2022) observed a significant difference in captures between the seasons of the year (dry and rainy).
In Venezuela, there have been no studies concerning this species' natural history; it is necessary to conduct studies, especially regarding its reproduction, population structure, and habitat use (Trebbau and Pritchard 2016). There is a disjunct population (often considered as the separate subspecies R. p. flammigera) along the Ventuari River, a tributary of the Orinoco River in Amazonas State, where an inferred area of occupancy (AOO) is less than 5,000 sq. km (Hernández and Rojas 2015); the estimated historical indigenous range or original AOO of the population was calculated at 25,125 sq. km by TTWG (in press), suggesting a major recent decline in AOO. Paolillo O. (1985) mentioned that this population in Amazonas state is very uncommon in the region. Therefore, due to its restricted distribution and low abundance, this population may be at increased risk of extinction (Rojas-Runjaic et al. 2011).
In French Guiana, there have been no population studies on R. punctularia, but the species seems quite common both in coastal areas and in deep forest (M. Dewynter pers. comm.). In Guyana, there have been no population studies either, but indigenous communities have suggested that populations of the species have been in decline for the past 20+ years (N. Millar pers. comm.). In Trinidad and Tobago, there have also been no population studies, but it has previously been considered to be a common turtle found in almost all types of habitats, except in areas dedicated to sugar cane (Pritchard and Trebbau 1984). No population estimates are available for Suriname.
Habitat and Ecology Information
Rhinoclemmys punctularia inhabits various types of water bodies such as rivers, lakes and interdunal lakes, coastal plains lakes, coastal swamps, flooded savannas and polders, temporary ponds and pools, tidal channels, cultivated lands, weedy ditches (in downtown Cayenne), and first, second, and third-order streams known in the Brazilian Amazon as “igarapés” (Pritchard and Trebbau 1984, Ernst and Barbour 1989, Rueda-Almonacid et al. 2007, Wariss et al. 2012, Pereira et al. 2013, Valle et al. 2016, Cunha et al. 2019, Brito et al. 2022). These water bodies are typically found within Tropical Rain Forest, but also gallery forest within savanna (llanos in Venezuela, cerrado in Brazil), and restinga in coastal areas (Pritchard and Trebbau 1984, Rojas-Runjaic et al. 2011, Wariss et al. 2012, Pereira et al. 2013, Silva et al. 2016, Brito et al. 2022). In the first-order streams where R. punctularia is found, there is the presence of monodominant palm-tree stands of Mauritia flexuosa L.f. and Euterpe oleracea Mart. (locally known as "buritizais" and "açaizais," respectively), commonly found in the headwater areas of the Amazon region (Brito et al. 2022). These environments have also been reported for populations in Venezuela (Pritchard and Trebbau 1984). Apparently, the water quality of the water body is of little importance; they are found in both clear and muddy, acidic and neutral water (Pritchard and Trebbau 1984). However, this turtle seems to avoid environments with saline water (Wariss et al. 2012), despite being common in coastal lentic habitats along parts of the northern Brazilian coast (Siciliano et al. 2014).
Rhinoclemmys punctularia is an omnivorous species that feeds more frequently on plants, including palm fruits from the Arecaceae family, such as Mauritia flexuosa, and Annonaceae (Rueda-Almonacid et al. 2007, Vogt 2008, Ferrara et al. 2017). It can feed both on land and in water (Ferrara et al. 2017). In a study conducted with faecal content analysis (Brito et al. 2022), it was shown that individuals frequently consume items of plant origin, mainly seeds of Myrtaceae (91.0%) and Inga sp. (82.0%), in addition to Lecythidaceae flowers (36.0%). However, when observing stomach contents, fish scales were also detected (Brito et al. 2022). In a population studied in a coastal region, seeds of Annona sp. (Annonaceae) and Chrysobalanus sp. (Chrysobalanaceae) were found in the faeces of turtles. Local residents also indicated the consumption of Nymphaea sp. (Nymphaeaceae) (Wariss et al. 2012).
The reproductive period of R. punctularia can vary. There are records of gravid females between September and December (Cunha et al. 2019) and nests between March and April (Vogt 2008) and July (Soares et al. 2017). Females typically lay 1–2 eggs, but it can vary up to four eggs (Vogt 2008, Soares et al. 2017, Ferrara et al. 2017, Cunha et al. 2019). It has been reported that R. punctularia does not dig a nest, but rather deposits the eggs on the forest floor; according to Vogt (2008) and Pritchard and Trebbau (1984), the eggs are laid in the leaf litter at the base of tree trunks and around roots, being covered by leaves, and incubated for about five months. However, in captivity, a female R. punctularia was observed digging a nest where a single egg was deposited at a depth of 10 cm (Soares et al. 2017). The eggs are elongated, very large and with a thick, brittle shell to prevent desiccation (Pritchard and Trebbau 1984, Vogt 2008, Ferrara et al. 2017). The size of the eggs can vary between 65 x 28 mm (Cunha and Vogt 2018), 65 x 35 mm (Vogt 2008), 67 x 38 mm (Ferrara et al. 2017), and 71 × 31 mm (Soares et al. 2017). The mass of the eggs can vary from 38 to 54 g (Vogt 2008, Cunha and Vogt 2018). On the basis of temperature-dependent sex determination (TSD) being present in R. areolata and R. pulcherrima (Ewert and Nelson 1991), it is reasonable to hypothesize that sex is also determined by incubation temperature in R. punctularia (Vogt 2008). Generation length is estimated at 10–17 years based on congeners and Iverson (2024).
Females can reach a straight-line carapace length (SCL) of 24.8 cm, while males can reach 20.1 cm (Pritchard and Trebbau 1984, Wariss et al. 2012, TTWG 2021). In a study of the largest population studied to date (169 individuals on Algodoal-Maiandeua Island, Maracanã, Pará, Brazil), the average SCL of females was 195.42 ± 18 mm (range 143–226 mm), and for males was 167 ± 12.7 mm (range 133–197 mm; Wariss et al. 2012). Size of hatchlings from Juruti, Pará, averaged 53.7 mm SCL and 26.6 g in mass (n = 3; Cunha et al. 2019); incubation time is about five months in the wild (Vogt 2008) or as short as 72–86 days in captivity (Cunha et al. 2019); there is a record of double-clutching in captivity with 45 days between nesting events (Cunha and Vogt 2018).
Threats Information
Global warming and climate change: A prolonged drought caused by climate change can negatively affect populations of Rhinoclemmys punctularia, leading to high mortality rates, as the water bodies used by the species dry up in some of their distribution areas (Oliveira et al. 2018). In addition to the lack of water or drastic reduction of water bodies caused by droughts, this turtle frequently moves on land (Brito et al. 2022), increasing the risk of death due to desiccation. Oliveira et al. (2018) recorded that of 21 dead turtles found, 71% were near dried or nearly dried water bodies. In addition, extreme drought can lead to natural or human-set fires, which, consequently, can result in the death or injury of turtles (Oliveira et al. 2018), in addition to causing the loss and alteration of habitats (Stanford et al. 2020). Chelonians are particularly affected by global warming due to temperature-dependent sex determination (TSD; Butler 2019), which may be found in this species. Changes in egg incubation temperature can lead to distortions in the sex ratio, as higher temperatures predominantly produce females, thereby reducing effective population size and genetic diversity in the population (Stanford et al. 2020).
Habitat loss: wildfires, degradation, and mining: Deforestation and habitat loss, especially in areas bordering the Amazon biome, can significantly impact R. punctularia populations, especially those residing in small water bodies within the forest. According to Fagundes et al. (2018), R. punctularia is among the Amazonian species most vulnerable to total area loss, accounting for 31.2% of Brazil. Considering the polygon generated from data collected by the authors and following the methodology of TTWG (2021), habitat loss up to the year 2021 was calculated based on land-use changes within the estimated distribution area of R. punctularia. Data from the MapBiomas Brazil and MapBiomas Amazônia (mapbiomas.org) were used for this analysis. We found that the situation of land-use change within the estimated occupancy area of R. punctularia poses little concern. In Brazil, 16.7% of the area has been altered, in French Guiana 1.5%, in Suriname 1.4%, in Guyana 1.7%, and in Venezuela 7.0% . In Brazil, if we consider only the Atlantic Forest, where there are records of populations in the southeast and northeast, the total land-use changes amounted to 40.6%, which is higher than that presented for all the countries mentioned above and for the global distribution of the species, which is 13.2%. Thus, while the overall land-use change in the global distribution area of the species is small, it is relatively high for the populations in the Atlantic Forest.
Another major threat is illegally set fires used for land clearing, as well as natural wildfires, with documented cases in some distribution areas of the species, such as in Pará, Bahia (Vogt et al. 2023), and Espírito Santo (Oliveira et al. 2018), Brazil. Oliveira et al. (2018) documented 12 individuals (48%) out of 25 discovered dead in an area that had been ravaged by deliberate fires or arson in southeastern Espírito Santo, Brazil. In Venezuela, since 2016, the national government has been promoting gold mining (Decree number 2.248 published in Official Gazette 40.855, February 2016, National Strategic Development Zone Orinoco Mining Arc) across a vast expanse that covers a significant portion of the species' distribution area. This activity is carried out without any environmental impact mitigation measures and involves the use of mercury, contaminating the waters of many rivers and leading to extensive deforestation. Additionally, this mining has significantly increased the human population, creating strong pressure on wildlife for the consumption of their meat, including turtles. In Brazil, mining disturbances are common in the Amazon Basin, but the actual impact in terms of contamination and habitat loss for R. punctularia is not well understood.
Dams: Hydroelectric plants severely affect water flow, converting lotic into lentic environments, and degrading water quality (Regolin et al. 2023). Hydroelectric power plants act in the same way of altering and causing the loss of habitats for R. punctularia populations, as they typically inhabit small bodies of water in the forest. The forests and areas surrounding dams are affected due to deforestation and reservoir filling, which flood the habitats used by this turtle, transforming açaizais, buritizais, lakes, and small streams into permanently flooded forests or large reservoirs.
Use and Trade Information
The consumption of Rhinoclemmys punctularia occurs among indigenous communities and traditional riverine populations in Brazil and Venezuela (Pritchard and Trebbau 1984, Señaris 2004, Rueda-Almonacid et al. 2007, Ferrara et al. 2017). There also appears to be illegal trade of this turtle species in Pará, Brazil (Vogt et al. 2023), but not in much of the rest of its distribution.
Conservation Actions Information
The listing of all species of Rhinoclemmys in CITES Appendix II went into effect 23 February 2023 (CITES 2023). Currently, there is no record of any monitoring programme in any of the countries where the species occurs. However, recently the creation of a Turtle Management Plan in Guyana has been facilitated for 26 indigenous communities found in Region 9, with the main objective of monitoring Podocnemis unifilis and P. expansa, but it states that further research is needed for R. punctularia (N. Millar pers. comm.). In Brazil, a large portion of the distribution of R. punctularia is located in the Amazon Rainforest (legal Amazon) where 22% of the territory is covered by Conservation Units that are an effective strategy for nature conservation; however, the areas surrounding this biome, especially those located in the “Amazonian Arc of Deforestation,” can threaten the maintenance of R. punctularia populations, as occurs with other aquatic and terrestrial animal species (Ilha et al. 2018, Miranda et al. 2021). Additionally, there are records of the occurrence of R. punctularia in at least 14 Conservation Units (Vogt et al. 2023), which are: Floresta Nacional (FLONA) Carajás, FLONA Crepori, Reserva Extrativista (RESEX) Baixo Juruá, RESEX Mãe Grande de Curuçá, RESEX Médio Juruá, RESEX Tapajós-Arapiuns, RESEX Verde para Sempre, Área De Proteção Ambiental (APA) Baía de Todos os Santos, APA da Baixada Maranhense, APA da Região Metrolpolitana de Belém, APA das Reentrâncias Maranhenses, APA Algodoal-Maiandeua, APA do Arquipélago Do Marajó, and Floresta Estadual do Amapá.
Rhinoclemmys punctularia was previously assessed as Least Concern by the IUCN Tortoise and Freshwater Turtle Specialist Group (TFTSG) in 1996, and was therefore not included on the Red List at that time (Behler 1996, TTWG 2021). Subsequently, it was again provisionally assessed as Least Concern by the TFTSG in 2011 (Rhodin et al. 2018, TTWG 2021).
Habitat loss and degradation are among the greatest threats to R. punctularia. This fact is exacerbated by the fact that many records of the species are located outside Conservation Units. Special attention should be given to populations in the southeastern and northeastern regions of Brazil that are situated within one of the world's most threatened biomes, the Atlantic Forest (Marques et al. 2021), but have limited data regarding their population status. Furthermore, for many countries where the species occurs, we lack knowledge about natural populations and their conservation status. This is the case in Venezuela, where populations have been suffering due to the advancement of mining, including petroleum exploration, which is causing habitat loss in vast forested areas, including the distribution area of R. punctularia (O. Hernández pers. obs.). In Venezuela, due to the increase in poverty, it is necessary to provide rural inhabitants with alternative means of subsistence in order to reduce hunting as the main source of meat for these families.
Research Needed:
It is necessary to confirm the taxonomic status of populations in southeastern and northeastern Brazil and whether they represent a new species or merely disjunct, possibly translocated, populations of R. punctularia (Valle et al. 2016). A comprehensive, integrated taxonomic investigation of apparently isolated populations of R. punctularia in Venezuela (Paolillo O. 1985, Rojas-Runjaic et al. 2011) and Brazil should be undertaken within the context of sampling within all six range countries. Both genetic and morphological data will be necessary to resolve the taxonomy. If different species are involved, it is important for the new species to be validated. Assessing two or more species as a single one can lead to errors in decision-making regarding conservation and threat criteria, which do not correspond to reality, putting populations and species at risk.
It is also necessary to understand the population trend of the species, especially in countries where there are no studies (Venezuela, Trinidad and Tobago, Guyana, Suriname, and French Guiana). In Brazil, it is essential to determine if the populations in the southeast and northeast are declining due to the impacts reported by Oliveira et al. (2018), who also reported many individuals with injuries and deaths caused by fire, indicating that this might be a recurring issue (J.C. F. Oliveira pers. obs.). The impact on populations situated within the "Amazonian Arc of Deforestation" in the Amazon Rainforest should also be investigated.
Ecological and conservation studies are of utmost importance for species conservation. Vogt (2008) reported that R. punctularia was one of the least known species in Brazil. Since 2008, little has changed regarding this statement, as there are still aspects related to its natural history and ecology that remain unknown across its distribution range. Population trends are urgently needed to monitor populations in critical areas for the species and its habitat trends; although the species appears to be a generalist, studies may indicate if there are preferred habitats that need conservation.