Freshwater turtle (Reptilia: Testudines) assemblage from an urban protected Atlantic Forest remnant: population density, movement and habitat preference

ABSTRACT

Urbanization may significantly impact wild population dynamics, even in protected green spaces. From 2016 to 2018, we accessed an assemblage of freshwater turtles isolated in an urban remnant of the Atlantic Forest, southern Brazil. We captured turtles by active search, hookless fishing, and funnel trap, and we marked them individually. Using a capture-mark-recapture method, we estimated population density, and movement, including home range size and habitat selection. Home ranges were estimated using the 100% minimum convex polygon method and habitat selections through eigenanalysis. We captured 41 specimens of Phrynops geoffroanus (Schweigger, 1812), 35 Trachemys dorbigni (Duméril & Bibron, 1835), and 20 Trachemys scripta elegans (Wied-Neuwied, 1839). The invasive T. dorbigni showed the highest density (1.72 individual/ha), followed by the native P. geoffroanus (1.36 individual/ha) and the invasive T. scripta elegans (0.87 individual/ha). Home range sizes for P. geoffroanus and T. dorbigni ranged between 0.04-0.48 ha, with the latter species covering the longest distance (525.8 m). All three species showed a preference for habitats influenced by human presence (walkways). Our findings highlight the anthropic influence on the movement of the freshwater turtle assemblage and underscore the need for enhanced protection of native species and control of invasive turtles. This study provides essential baseline data for future researches and management of urban areas.

KEYWORDS:
Anthropic pressure; chelonians; hotspot; habitat selection; home range; invasive alien species

INTRODUCTION

Aquatic systems are among the most productive ecosystems globally, yet they are also some of the most degraded due to human activities such as urbanization, agriculture, and grazing (Paul and Meyer 2001). Urbanization, in particular, can rapidly and extensively alter natural environments, posing a substantial threat to aquatic ecosystems through deforestation, degradation, and fragmentation of native and riparian vegetation (Paul and Meyer 2001, Marchand and Litvaitis 2004, Bujes et al. 2011, Guzy et al. 2013). Habitat loss and fragmentation isolate wildlife populations into patches, leading to reduced dispersal, diminished genetic variability, and potentially causing deleterious effects such as local extinctions (Guzy et al. 2013). Alterations in riparian vegetation can also affect water temperature, resulting in increased temperature fluctuation, decreased biodiversity, and altered spatial distribution of the species (Paul and Meyer 2001, Marchand and Litvaitis 2004). Additionally, urban water bodies are often structurally modified through channelization, damming, and siltation (Spinks et al. 2003, Guzy et al. 2013). Biotic pressures, such as the introduction of alien species, further exacerbate the challenges faced by remaining native species in urban green spaces (French et al. 2018), causing direct harm through competition, niche displacement and potential extinction (Lockwood et al. 2013).

In general, many species are heavily impacted by anthropic pressure. Some may not survive under these conditions, while others may persist, reproduce, and even thrive in such disturbed environments, including amphibians, reptiles, birds and mammals (Rees et al. 2009, Hunt et al. 2013, Villaseñor et al. 2017, Beaugeard et al. 2019, Santini et al. 2019). However, despite their ability to persist, human disturbance influences how these animals move, select and use their habitats (Slabbekoorn and Peet 2003, Ryan et al. 2008, Hill and Vodopich 2013). In addition, such disturbances may change demographics characteristics of populations, such as size and density (Souza and Abe 2000, Howel and Seigel 2019). Freshwater turtles, for instance, exhibit strong responses to local-scale urbanization (Hill and Vodopich 2013). Several environmental features that influence turtle movement are frequently modified in urban settings, including riparian vegetation, the availability of basking sites, refuges, and feeding resources (Huey 1991, Standing et al. 1999, Souza and Abe 2000, Compton et al. 2002, Cosentino et al. 2010, Quesnelle et al. 2013, Ghaffari et al. 2014, Latham et al. 2022). Furthermore, turtle movement patterns may vary based on species, sex, season, and interespecific interactions (Compton et al. 2002, Fachín-Terán et al. 2006, Segurado and Figueiredo 2007, Rees et al. 2009, Bower et al. 2012, Paterson et al. 2012, Ryan et al. 2014, Famelli et al. 2016, De Leão et al. 2019, Petrozzi et al. 2021).

In the past decade, there has been a notable increase in studies on Brazilian freshwater turtles, with most research focusing on populations from the central, northern regions (e.g., Brito et al. 2018, Fagundes et al. 2018, De Leão et al. 2019, Brito et al. 2020, Michalski et al. 2020). However, in urban environments, the ecological knowledge of native turtle populations (e.g., Müller et al. 2019) and their interactions with alien species remains limited. Phrynops geoffroanus (Schweigger, 1812), a well-studied species of Neotropical urban fauna, exhibits high biomass and density in polluted water bodies (Souza and Abe 2000, 2001, Souza et al. 2008, Martins et al. 2010). Nonetheless, native Chelidae turtles, including P. geoffroanus, are impacted by the introduction of alien species (Martins et al. 2014, Molina et al. 2016).

Trachemys dorbigni (Duméril & Bibron, 1835) and Trachemys scripta elegans (Wied-Neuwied, 1839) are among the most common alien turtles in Brazilian urban areas (e.g., Santos et al. 2009, Molina et al. 2016, Ciccheto et al. 2018, Santos et al. 2020). There is, however, a significant gap in the available information on alien species in Brazil (Ziller and Zalba 2007, Zenni et al. 2024), with even less known about invasive turtles and their interactions with native species. Understanding the persistence of these invasive species, their demographics, and their coexistence with native turtles is essential for elucidating the invasion dynamics of Trachemys species (Molina et al. 2016).

Considering the high diversity of freshwater chelonians in Brazil (32 species; Guedes et al. 2023) and the frequent introduction of invasive turtles into the wild, often due to pet release (Romagosa 2015), combined with the impact of urbanization on wild population dynamics, our goal was to estimate some demographic parameters, patterns of habitat use and preferences to propose better management and conservation strategies for freshwater turtles under continuous anthropogenic pressure. We herein investigated population density, home range and habitat preference within the park features for one native species (P. geoffroanus) and two invasive alien turtles (T. dorbigni and T. scripta elegans) coexisting in a small, closed area. Based on previous studies in urban environments, we were expecting high densities for all three species, with larger home ranges for Trachemys due to their invasive potential. Additionally, we predicted that urban features influence their movement, altering space utilization and habitat preferences due to human disturbances (Ryan et al. 2008, Cosentino et al. 2010, Hill and Vodopich 2013, Munscher et al. 2021).

MATERIAL AND METHODS

Study area and target species

The study area encompassed 47 ha remnant of the Atlantic Forest located centrally within Maringá city, state of Paraná, southern Brazil (23°25’S, 51°55’W; Fig. 1). This fragmented forest is a protected area designated as a Conservation Unit and serves as a public park called Parque do Ingá. It hosts several river sources of the Ivaí Basin, ultimately flowing into the Paraná River, along with a diverse array of native fauna and flora (SEMA 2010, 2020). The surveyed park comprises numerous interconnected lagoons linked to a central lake, with connectivity stablished through a canal leading downstream. However, this canal act as a barrier to aquatic fauna movement due to its significant elevation drop and shallow depth, compounded by anthropogenic factors such as waste accumulation and branches.

Figure 1
Location of the study area in Brazil. The red square represents the park studied (Parque do Ingá), located in the urban area of Maringá City, Paraná state, Brazil.

The area falls within a transition zone between tropical and subtropical climate types (Köppen 1978), characterized by well-distributed rainfall throughout the year, with a slight decrease during winter. The average annual temperature is 20.5 °C, and the mean annual rainfall reaches 1,550 mm. The rainy summer season spans December to March, with January being the hottest and most humid month, while the dry winter season extends from June to September, with July being the coldest and driest month (Deffune and Klosowski 1995, SEMA 2011).

Within the study area, the turtle assemblage comprises four species: two native and two invasive alien species. We focused on three of them (Fig. 2): Phrynops geoffroanus, Trachemys dorbigni, and T. scripta elegans. Due to the low number of individuals captured (n = 2), we could not access the population of the fourth species, Hydromedusa tectifera, Cope 1870. The sole native species among those studied is P. geoffroanus. While T. dorbigni is native to Brazil, its presence in this region is considered alien, as its distribution is restricted to the states of Rio Grande do Sul and Santa Catarina (Guedes et al. 2023). Trachemys scripta elegans is also an alien species, naturally occurring in the northern and central United States and northwest Mexico, and has been introduced to all countries except Antarctica (Painter and Christman 2000, Rueda-Almonacid et al. 2007). Both Trachemys species were likely introduced to this region through pet release and are classified as invasive in Brazil (Zenni et al. 2024). Trachemys dorbigni has been recognized for its invasive potential throughout the Americas (Fonseca et al. 2021), while T. scripta is listed as one of the top 100 worst invasive species of the world (GISD 2024).

Figure 2
Species of freshwater turtles studied in an urban area in southern Brazil: (A) Trachemys dorbigni; (B) Phrynops geoffroanus; (C) T. scripta elegans; (D) P. geoffroanus marked with an epoxy number.

Sampling procedures

We sampled 11 aquatic habitats randomly selected within the park, including the main lake and small lagoons, from July 2016 and August 2018. We conducted surveys every month, approximately three times per month, with the frequency ranging from one to seven times. However, sampling was not conducted in December 2016, January 2017, March 2017, June 2018, and July 2018. The total sampling effort accumulated to 61 days. We captured turtles using three different methods: i) Active search, with two researchers performing hand capture surveys, carefully walking among sample sites, with the aid of binoculars, looking for turtles basking on logs, rocks, and the water’s surface. The method was employed for five hours per day, totaling 610 h; ii) Hookless fishing with clip, a novel trap method similar to traditional fishing but without causing injury to the turtles (Rocha et al. 2024). The device, baited with chicken gizzard, consisted of a specific clip (fishing snaps) attached to a fishing line operated by one researcher, equipped with a hand dip net (2 cm mesh). We used four devices at locations spaced 10 m apart and operated by two researches, for five hours per day, resulting in a total of 1220 h of operation; iii) Funnel trap, with double-mouth baited with chicken gizzard. These traps, each measuring 100 cm long × 50 cm external diameter × 25 cm entrance diameter, with 2 cm mesh, were activated for 24 hours and checked by two researchers thereafter. Five devices spaced 10 m apart were utilized on six occasions, resulting in a total of 720 hours of operation. This method served as a complementary approach due to urban challenges, including accessibility of local people and the risk of device theft.

We marked individuals using unique numbers affixed to the carapace (Fig. 2D), with natural marks on the plastron (i.e., plastron scutes suture) also recorded as control marks. Subsequently, we measured the curvilinear carapace and plastron (length and width) and determined sex based on secondary sexual traits (e.g., tail length, cloaca position; Rueda-Almonacid et al. 2007). We considered juvenile individuals as those with a carapace length of < 10 cm for T. scripta elegans (Lewis et a. 2018), < 12 cm Trachemys dorbigni (Fagundes et al. 2010), and < 21 cm P. geoffroanus (Souza and Abe 2001). Following handling, individuals were released at their capture site. Permits for handling and tagging the three species of freshwater turtles were obtained from the Instituto Chico Mendes de Conservação da Biodiversidade (55637-3), with animal care permission was provided by the Ethics Committee of the Universidade Federal de Mato Grosso do Sul (CEUA/UFMS 811/2016).

Data analysis

Density

We carried out a capture-mark-recapture (CMR) procedure to estimate population density and movements. We applied a closed population model to estimate density for each species, considering the study area’s closed characteristics and the long life period of the animals (Plummer 1977). We used the Maximum-likelihood approach on program DENSITY (version 5.0, Efford et al. 2004) to estimate population density and home-range parameters based on the capturing data according to the Spatial Explicit Capture-Recapture model (SECR). We modeled capture probability based on the distance between the sampled location and the home-range center, assuming that the spatial position of home-range centers followed a Poisson distribution. We applied the simplest spatial-detection function available in DENSITY software (half-normal), a function with two parameters: the first (σ) corresponding to a measure of home range size (2.45σ = 95% home-range radius assuming a circular shape (Efford et al. 2005) and the second (g0) being the one-night probability of capture at the home-range center (Anderson et al. 2022). The default settings were used for all computations, except for ‘buffer width’, which was set to 100 m. This was checked retrospectively using the spatially explicit capture-recapture log-likelihood tool to ensure these settings were appropriate (i.e., density estimates did not change as buffer width was increased). Population-scale density and mean home-range parameter estimates were obtained for each species independently, by pooling the two years trapping data into full 11 sessions of data on the basis of ‘between-sessions’ models of variation in g0 and σ (e.g., Richardson et al. 2017).We used corrected Akaike’s information criterion (AICc) values to choose between a null model with g0 and σ constant - Model (null), and models in which both parameters varied according to: (1) Temporal variation (months) in detection parameters (g0 and σ): Model (time); (2) behavioral response to capture, either permanent: Model (permanent behavior) (lasting the entire capturing session), or temporary: Model (temporary behavior) (affecting only the next capture); and (3) considering sex differences in g0 and σ: Model (sex) (Borchers and Efford 2008). We selected the best model based on the minimum values of the ΔAICc (< 2; Lebreton et al. 1992).

Home range

We calculated home range using Minimum convex polygons (MPC 100%). This approach was employed due to the reduced capture-recapture data; 44% of turtles were captured only once, and in our analysis, we included only data from turtles captured at least five times over the 34-months period. In addition, only captures at more than two different sites were considered. Despite the limitations of this estimation method (i.e., Silva et al. 2020), we selected this analysis as recommended for amphibians and reptiles (i.e., Row and Blouin-Demers 2006). Finally, we used the adehabitat HR package of R statistical computing environment (R Core Team 2022).

We calculated the maximum individual movement range by measuring the straight-line distance between their two farthest recorded locations (Ryan et al. 2014). We used simple linear regression with ordinary least squares (Zar 1996) to analyze how body size (carapace length-CL) affects the maximum distance range (MDR) according to the species. MDR was treated as the dependent variable and CL as the independent variable.

Habitat preference

The analysis of habitat selection of the individuals was performed using the adehabitat HS package of R, according to the Design II approach, which identifies the animals measures their habitat-habitat availability defined at the population level, i.e., the same for all animals (Calenge and Dufour 2006). To determine available habitat, we first characterized the eleven sampling locations, established a concentric 5 m buffer around each, and calculated the percentages of vegetation cover, water, surface area suitable for sunbathing (basking sites), and walkways. This information was analyzed through the software QGIS (Quantum Geographic Information System, v. 3.26) and confirmed during field work. For the habitat used by a given individual, we considered the habitat around the sampled location where it was captured. Note that not all the animals were trapped in the all the sampling locations. We compared the habitat used and available according to the Manly selection ratios (Manly et al. 2002). If all individuals exhibited equal habitat preferences, the preference ratios were averaged. However, if different preferences were observed, a factorial investigation using eigenanalysis was conducted (Calenge and Dufour 2006). Eigenanalysis is an extension of principal component analysis, including a graphic expression of habitat preference. This analysis produces plots explained by two factors or axes (factorial axis 1 is the x-axis and factorial axis 2 is the y-axis). The first factorial axis relates to the most selected habitat types and represents a useful tool to investigate the variability in habitat preference between individuals and identify groups of individuals choosing the same habitat (Calenge and Dufour 2006).

RESULTS

In total, we captured 96 freshwater turtles during the entire study period. From P. geoffroanus, we trapped 41 individuals comprising 26 females, nine males, and six juveniles. Over half of these individuals (n = 24) were capture only once, while 17 individuals were recaptured. Among them, 11 were captured twice, four were captured three times, one individual was captured four times and one individual six times. The sex ratio was significantly skewed towards females, with a ratio of 2.8 females to 1 male. From T. dorbigni, 35 individuals were trapped consisting of 24 females, nine males, and two juveniles. In terms of captures, 13 turtles were captured once, and 22 turtles were recaptured. Among them, nine were captured twice, two were captured three times, one was captured four times, three were captured five times, while other three individuals were captured six times. The remaining individuals were captured on seven occasions (n = 1), ten (n = 2) and 13 occasions (n = 1). The sex ratio of this species also favored females (2.6:1). The less trapped species was T. scripta elegans, with 20 individuals (11 females, eight males, and one juvenile). Six individuals of this species were captured once, and 14 were recaptured. Among them, four were capture twice, and other four turtles were captured four times. Moreover, one individual was captured seven times, four were captured nine times, and one was captured 15 times. In contrast to the other species, the sex ratio of T. scripta elegans did not significantly deviate from 1:1.

Our results revealed fluctuations in capture per unit effort (CPUE) across months (Fig. 3). In 2016, the native P. geoffroanus was predominantly captured in July, followed by consecutive months where it was the sole species captured (August and September). The alien T. dorbigni was the only species captured in October, with both alien species capture exclusively in the following month. Throughout 2017, all three species were captured every month, except for P. geoffroanus in December. Trachemys dorbigni exhibited slightly higher captures, mainly between August and September, while P. geoffroanus showed increased captures in August. Notably, T. scripta elegans reached its peak capture in February. Similarly, in 2018, T. scripta elegans demonstrated heightened captures in February, as well as in April. Although the other species were recorded during this period, their captures were less frequent. Our findings suggest a variation in activity among these coexisting species within a confined area.

Figure 3
Monthly captures of freshwater turtle from July 2016 to August 2018 in an urban park of southern Brazil. The graphs denote the total numbers of individuals captured each month for Phynops geoffroanus (top), Trachemys dorbigni (middle), and T. scripta elegans (bottom). White bars symbolize juveniles, gray bars represent males, and black bars indicate females. Dotted orange lines delineate the capture per unit effort (CPUE) per month sampled.

The population density of Trachemys dorbigni was highest at 1.72 individual/ha, possibly due to the spatial aggre gation of individuals. Phrynops geoffroanus was 1.36 individual/ha, and T. scripta elegans had the lowest population density at 0.87 individual/ha (Table 1). Home range size was estimated for five T. dorbigni (four females and one male), ranging between 0.04 and 0.48 ha (mean ± SD = 0.31 ± 0.21). Additionally, one P. geoffroanus (female) had a home range size of 0.26 ha. The slider T. dorbigni exhibited the greatest distance range, covering 525.8 m (n = 22), and was the only species to show a positive relationship between this variable and body size (p = 0.03, F = 8.70, r² = 0.30). Phrynops geoffroanus reached a maximum distance of 322.4 m (n = 17), while T. scripta elegans covered less than half the maximum distance of its congeneric species (227.3 m, n = 14). Manly’s selection ratios revealed variations in habitat preferences among individuals (χ² = 289.6, DF = 63, p = 0.001). Eigenanalysis illustrated the habitat selections of individual turtles, indicating a strong preference for walkway habitats across all three species (Fig. 4).

Figure 4
Eigenanalysis of selection ratios illustrating habitat preferences of freshwater turtles in an urban park, southern Brazil. Each vector represents the preference of an individual, with each number corresponding to a specific individual. The direction of the vector indicates the most preferred habitat for that individual. The length of the arrow reflects the strength of the preference for a particular habitat type.

Table 1
Estimates of freshwater turtles’s density per hectare (± Standard Error) and parameters of a half-normal detection function g0 and σ. ΔAICc is the difference between the corrected AIC of the model studied and the best model (with the lowest AICc). The total number of captured species: 41 Phrynops geoffroanus, 35 Trachemys dorbigni, and 20 T. scripta elegans. Parameters varied according to temporal variation in months (time), permanent behavioral response to capture (permanent behavior), temporary behavioral response to capture (temporary behavior), and sex differences (sex); null model is represented by (null).

Model	Density (±SE)	g0	σ	AICc	ΔAICc
Prynops geoffroanus
Sex	1.36 (0.34)	0.02	99.48	491.03	0.00
Null	1.35 (0.34)	0.02	99.71	492.42	1.39
Time	1.84 (0.40)	0.02	93.37	495.00	3.97
Permanent behavior	1.59 (0.41)	0.01	169.68	496.04	5.01
Temporary behavior	1.36 (0.34)	0.02	93.12	497.49	6.46
Trachemys dorbigni
Temporary behavior	1.72 (0.36)	0.03	86.56	1019.02	0.00
Sex	1.67 (0.35)	0.03	97.66	1037.96	18.94
Time	1.58 (0.34)	0.03	92.72	1038.19	19.17
Permanent behavior	1.91 (0.45)	0.01	97.38	1038.35	19.33
Null	1.66 (0.35)	0.03	97.97	1040.39	21.37
Trachemys scripta elegans
Time	0.87 (0.25)	0.07	64.18	691.15	0.00
Temporary behavior	0.93 (0.26)	0.06	64.65	702.30	11.15
Sex	0.91 (0.25)	0.12	57.52	709.68	18.53
Null	0.91 (0.26)	0.10	59.62	711.18	20.03
Permanent behavior	0.98 (0.27)	0.09	60.81	740.78	49.63

DISCUSSION

We elucidated previously unexplored data concerning the coexistence of native freshwater turtles and invasive alien species in Brazil. In our study populations, the fluctuation in captures across years seems to reflect the species’ varying activity levels by month. Phrynops geoffroanus, for instance, usually presents higher activity between September and November (Souza and Abe 2000, 2001), but in the present study, we captured more individuals slightly earlier, in July (2016) and August (2017). We also observed changes in activity for T. dorbigni; this species exhibited higher activity in October (2016), August (2017) and September (2017), differing from previous records in its original distribution range: February and March (Fagundes et al. 2010) and November and December (Bager et al. 2007, Bujes et al. 2011). In contrast, T. scripta elegans followed a pattern already recorded in its natural distribution, closely related to the summer season (Morreale et al. 1984, Mali et al. 2016).

In the context of sharing a small isolated area (total lakes area = 5.9 ha), where the turtles are hindered from exiting (Rocha et al. 2022), exclusive competition may occur. When native and alien species coexist with similar trophic requirements, the native tends to be excluded (Hardin 1960, Gotelli 2001, Pérez-Santigosa et al. 2011). Conversely, changes in activity among the three species may arise in response to coexistence, particularly considering P. geoffroanus as a generalist species tolerant to anthropogenic pressure. From this perspective, the regulation of population parameters, alterations in movement patterns, habitat segregation and niche partitioning are expected to play essential roles (Vogt and Guzman 1988, Segurado and Figueiredo 2007, Luiselli 2008, Alcalde et al. 2010, Gavina et al. 2018, Petrozzi et al. 2021).

Skewed sex ratio in turtles can be associated with many factors such as trapping method, area sampled, season, and differential mortality of the sexes (Brito et al. 2018, Howell and Seigel 2019, Rocha et al. 2024). We employed the same sampling methods across the three turtle species and observed female-biased sex ratio deviations in two of them. Previous research in the same area indicated unbiased sex ratio in captures using the two main methods used by our team (Active search and Hookless fishing), unlike funnel traps, which favored male captures (Rocha et al. 2024). Therefore, we cannot attribute the differences in sex ratio observed in P. geoffroanus and T. dorbigni to the method used.

In contrast to prior investigations with P. geoffroanus, our study revealed a reduced population density (1.36 turtle/ha). In pristine habitats, this species can attain higher density (41.8 individuals/ha, Abrantes et al. 2021), while urban environments may harbor even denser populations (170-230 turtle/ha, Souza and Abe 2000). The elevated population density observed in urban areas is likely attributed to a combination of urban factors favoring turtles, such as abundance of food from sewage and organic waste of polluted rivers, the absence of predators, and increased availability of nesting sites (Souza and Abe 2000, Martins et al. 2010, Molina et al. 2016). Food supplementation, for instance, has been shown to reduce dispersal behavior and diminish home range size (Souza et al. 2008). Although estimated for a single P. geoffroanus, our findings indicate a larger home range (0.26 ha) compared to those reported by Souza et al. (2008) in a polluted urban river (0.04-0.12 ha). The inverse relationship between density and home range size aligns with patterns noted by some authors (Efford et al. 2015, Sanchez and Hudgens 2015), while is refuted by others (e.g., Honora et al. 2019). However, given that these estimates derive from distinct sampling methods and environmental conditions, caution is warranted when establishing a comparison (Forero-Medina et al. 2011).

Food supplementation in our study area is likely not as abundant as in the urban rivers where P. geoffroanus was previously studied. Despite the presence of an additional food source provided by visitors in our study park, discharges of human sewage occur indirectly from stormwater drains (SEMA 2020), potentially representing localized supplemental food inputs. While predators are also limited, disadvantages in competitive interactions with invasive species emerge as significant factors that could potentially constrain or displace its population in our study area, particularly through competition for basking areas and food (Rocha et al. pers. comm.). Given the global conservation status of P. geoffroanus complex remains unaccessed by the IUCN (2024), their occurrence in two Brazilian global biodiversity hotspots (lineage 1, Carvalho et al. 2017, 2022), and the potential impact of invasive alien species on its populations, we strongly recommend ongoing monitoring of this species in our study area and urban regions across Brazil. Moreover, further studies are needed to evaluate competitive interactions among these species in different environments contexts.

Regarding T. dorbigni, higher density values were recorded in previous studies in its natural distribution area (7.61 individual/ha, Bujes et al. 2011), compared to our findings (1.72 individual/ha). However, as records of T. dorbigni beyond its original distribution range have been noted in recent decades, there is currently no data available on population characteristics of this turtle as alien species for comparison. The estimated home range (0.04-0.48 ha) was similar to those observed for Emydidae species in small anthropized areas (i.e., 0.003-3.12 ha for Glyptemys muhlenbergii, Morrow et al. 2001). While landscape composition has a weak effect on the movement of some species of the same family (i.e., Emydoidea blandingii, Fortin et al. 2012), many others have shown positive relationship between habitat conservation and home range size (e.g., 5-16 ha for Clemmys guttata - Litzgus and Mousseau 2006, 28.3 ha for Clemmys insculpta - Arvisais et al. 2002, 61.2 ha for Emydoidea blandingii - Edge et al. 2010). In pristine riparian vegetation and large wetlands areas, movement may increase since habitat is likely not a limiting resource, and with greater availability of spatial resources, home ranges tend to expand (Edge et al. 2010, Jaeger and Cobb 2012, Pérez-Santigosa et al. 2013). Although accurately estimating habitat availability is challenging in lentic systems, the habitat characteristics should be considered in descriptions of the spatial ecology of chelonians (Jaeger and Cobb 2012). Among the three turtle species, T. dorbigni covered the longest distances in water, in addition to be the only species showing a significant positive relationship between this parameter and carapace length. Females turtles, being the largest individuals, are capable of traveling long distances also on land to nest (up to 250 m, as reported by Bager and Rosado 2010). These findings underscore the high mobility capacity of females, and newborns, in reaching and colonizing new areas, thereby facilitating potential future invasions. Furthermore, intentional releases serve as an additional mechanism for their dispersal as alien species in many regions of Brazil (Ciccheto et al. 2018), driven by both legal and illegal pet trade practices and a lack of awareness and responsibility among owners.

Surprisingly, T. scripta elegans presented the lowest estimated population density (0.87 individual/ha). Indeed, the density of its populations can reach much higher values, both within its original distribution range (41-61 individuals/ha, Congdon et al. 1986) and beyond (89-299 individuals/ha, Taniguchi et al. 2017). As human trade is the primary driver of its introduction (Thomson et al. 2010), and their trade has been banned in Brazil (IBAMA Ordinance n. 93, July 7, 1998), the decrease in new introductions may be closely related to our results. Although still trade illegally in the country, the popularity of T. dorbigni surpasses that of T. scripta elegans in the Brazilian pet market (Alves et al. 2019). However, caution in identifying congeneric species is necessary, as hybridization between them has been observed (Figueiredo 2014, Tortato et al. 2014, Santos et al. 2020). Previous studies have found individuals morphologically classified as hybrid, but genetically belonging to T. scripta elegans lineage (Figueiredo 2014). Despite the turtles’ lifespan, limited mobility and no deaths detected, which often align with closed population assumptions, our study period reveled minimal occurrences of new births. Therefore, the density estimates for the three turtle species may be underestimated.

Controlling T. scripta elegans is strongly recommended due to their threat to native chelonians residing in this park (i.e., P. geoffroanus and H. tectifera, Martins et al. 2014, Grou et al. 2024) and their detrimental impact on the population dynamics of various native turtles worldwide (Cadi and Joly 2003, Polo-Cavia et al. 2009, 2010, 2011, Pearson et al. 2015, Taniguchi et al. 2017, Lambert et al. 2019). Similarly, implementing effective management strategies, such as control, is necessary to prevent future ecosystem damage caused by T. dorbigni, given their frequent introduction to new regions and the species’ ability to travel long distances.

The preference for walkways as habitat is a response to anthropic pressure on this freshwater turtle assemblage. Although we did not measure it, we had previously observed people feeding wild animals inside the studied park, as on some walkways. Since food gathering and diet type are predictors of movement (Slavenko et al. 2016), human presence is shown to be a driver of habitat use and selection by turtles studied.

Over two years of monitoring, we estimated a lower density of the native turtle population (P. geoffroanus). Despite a potential underestimation, our value is even lower than estimated in preserved areas. The second native species (H. tectifera) may not even be accessed due to its scarce record, with only two individuals observed compared to five recorded in previous studies, all of them adults (Carlos E.V. Grou, personal observation). Considering the presence of two invasive species in the area, with established populations exerting further stress on native populations, and given that this is a system where animal movement is restricted, both native species may be affected, with H. tectifera likely tending towards local population extinction. Moreover, the preference of the native turtle population for anthropogenic habitats raises concerns. In our study, this preference may be attributed to feeding behavior, which not only influences their diet and health but also encourages turtles to become increasingly comfortable in the presence of humans. This proximity may lead to their capture by park visitors, as it is a cultural practice in the area. Therefore, it is essential for conservation efforts to address both targeted monitoring of remaining native populations and the enforcement of park regulations to prevent the introduction of alien species, capture of fauna and feeding practices. In addition, recognizing the native species are influenced by anthropogenic factors, even within a Conservation Unit, should prompt managers to implement the control of invasive alien species and the enhancement of connectivity among green spaces for wild species. We also recommend the placement of educational signage to heighten visitor awareness and the implementation of environmental education initiatives (i.e., turtle watching programs; Lindeman 2020), to actively engage residents in chelonian conservation efforts.

ACKNOWLEDGMENTS

We thank R.M. Takemoto and the Ichthioparasitology Laboratory from Universidade Estadual de Maringá, Brazil, for their logistic support. We are grateful to C. Felix and M. Neves for their help on an earlier manuscript draft and to collaborators of the Tamari Project for assistance in the field. SBR was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Universidad de Córdoba by the postdoctoral contract (Plan Propio de Investigación).

LITERATURE CITED

• Abrantes MMR, Pereira JA, Brasil AWL, Souza AR, Dantas DFA, Brito PHI, et al. (2021) Ecological aspects of a population of Phrynops geoffroanus (Schweigger, 1812) in a semi-arid area of Northeastern Brazil. Research, Society and Development 10(7): e9510715154. https://doi.org/10.33448/rsd-v10i7.15154
  » https://doi.org/10.33448/rsd-v10i7.15154
• Alcalde LM, Derocco NN, Rosset SD (2010) Feeding in syntopy: Diet of Hydromedusa tectifera and Phrynops hilarii (Chelidae). Chelonian Conservation and Biology 9: 33-44. https://doi.org/10.2744/CCB-0794.1
  » https://doi.org/10.2744/CCB-0794.1
• Alves RRN, Araújo BMC, Policarpo IA, Pereira HM, Borges AKM, Vieira WLS, Vasconsellos A (2019) Keeping reptiles as pets in Brazil: Ethnozoological and conservation aspects. Journal for Nature Conservation 49: 9-21. https://doi.org/10.1016/j.jnc.2019.02.002
  » https://doi.org/10.1016/j.jnc.2019.02.002
• Anderson DP, Rouco C, Latham CM, Warburton B (2022) Understanding spatially explicit capture-recapture parameters for informing invasive animal management. Ecosphere 13(11): e4269. https://doi.org/10.1002/ecs2.4269
  » https://doi.org/10.1002/ecs2.4269
• Arvisais M, Bourgeois J-C, Lévesque E, Daigle C, Masse D, Jutras J (2002) Home range and movements of a wood turtle (Clemmys insculpta) population at the northern limit of its range. Canadian Journal of Zoology 80: 402-408. https://doi.org/10.1139/z02-013
  » https://doi.org/10.1139/z02-013
• Bager A, Freitas TRO, Krause L (2007) Nesting ecology of a population of Trachemys dorbigni (Emydidae) in southern Brazil. Herpetologica 63: 56-65. https://doi.org/10.1655/0018-0831(2007)63[56:NEOAPO]2.0.CO;2
• Bager A, Rosado JLO (2010) Estimation of core terrestrial habitats for freshwater turtles in southern Brazil based on nesting áreas. Journal of Herpetology 44(4): 658-662. https://doi.org/10.1670/09-036.1
  » https://doi.org/10.1670/09-036.1
• Beaugeard E, Brischoux F, Henry PY, Parenteau C, Trouvé C, Angelier F (2019) Does urbanization cause stress in wild birds during development? Insights from feather corticosterone levels in juvenile house sparrows (Passer domesticus). Ecology and Evolution 9(1): 640-652. https://doi.org/10.1002/ece3.4788
  » https://doi.org/10.1002/ece3.4788
• Borchers DL, Efford MG (2008) Spatially explicit maximum likelihood methods for capture-recapture studies. Biometrics 64: 377-385. https://doi.org/10.1111/j.1541-0420.2007.00927.x
  » https://doi.org/10.1111/j.1541-0420.2007.00927.x
• Bower DS, Hutchinson M, Georges A (2012) Movement and habitat use of Australia’s largest snake-necked turtle: Implications for water management. Journal of Zoology 287: 76-80. https://doi.org/10.1111/j.1469-7998.2011.00891.x
  » https://doi.org/10.1111/j.1469-7998.2011.00891.x
• Brito ES, Vogt RC, Valadão RM, França LF, Penha J, Strüssmann C (2018) Population ecology of the freshwater turtle Mesoclemmys vanderhaegei (Testudines: Chelidae). Herpetological Conservation and Biology 13: 355-365.
• Brito ES, Rodrigues EAS, Ferrão M, Ferreira VL, Tomas WM, Strüssmann C (2020) Acanthochelys macrocephala (Big-headed Pantanal Swamp Turtle). Population and movement. Herpetological Review 51(1): 104-105.
• Bujes CS, Molina FB, Verrastro L (2011) Population characteristics of Trachemys dorbigni (Testudines, Emydidae) from Delta do Jacuí State Park, Rio Grande do Sul, Southern Brazil. South American Journal of Herpetology 6: 27-34. https://doi.org/10.2994/057.006.0104
  » https://doi.org/10.2994/057.006.0104
• Cadi A, Joly P (2003) Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Canadian Journal of Zoology 81(1): 1392-1398. https://doi.org/10.1139/z03-108
  » https://doi.org/10.1139/z03-108
• Calenge C, Dufour AB (2006) Eigenanalysis of selection ratios from animal radio-tracking data. Ecology 87: 2349-2355. https://doi.org/10.1890/0012-9658(2006)87[2349:EOSRFA]2.0.CO;2
  » https://doi.org/10.1890/0012-9658(2006)87[2349:EOSRFA]2.0.CO;2
• Carvalho VT, Martínez JG, Hernández-Rangel SM, Astolfi-Filho S, Vogt RC, Farias IP, Hrbek T (2017) Giving IDs to turtles: SNP markers for assignment of individuals to lineages of the geographically structured Phrynops geoffroanus (Chelidae: Testudines). Conservation Genetics Resources 9(1): 157-163. https://doi.org/10.1007/s12686-016-0626-8
  » https://doi.org/10.1007/s12686-016-0626-8
• Carvalho VT, Vogt RC, Rojas RR, Nunes MS, Fraga R, Ávila RW, et al. (2022) Four in One: Cryptic Diversity in Geoffroy’s Side-Necked Turtle Phrynops geoffroanus (Schweigger 1812) (Testudines: Pleurodira: Chelidae) in Brazil. Diversity 14(5): 1-16. https://doi.org/0.3390/d14050360
  » https://doi.org/0.3390/d14050360
• Ciccheto JRM, Grou CEV, Rocha SB (2018) Novos registros de ocorrência de Trachemys dorbigni no Brasil. In: Oldiges DP (Ed.) Estudo da Herpetofauna Brasileira. Editora Atena, Ponta Grossa, 42-50. https://www.atenaeditora.com.br/catalogo/ebook/estudo-da-herpetofauna-brasileira
  » https://www.atenaeditora.com.br/catalogo/ebook/estudo-da-herpetofauna-brasileira
• Compton BW, Rhymer JM, Mccollough M (2002) Habitat selection by Wood Turtles (Clemmys insculpta): an application of paired logistic. Ecology 83: 833-843. https://doi.org/10.2307/3071885
  » https://doi.org/10.2307/3071885
• Congdon JD, Greene JL, Gibbons JW (1986) Biomass of freshwater turtles: a geographic comparison. The American Midland Naturalist 115: 165-173. https://doi.org/10.2307/2425846
  » https://doi.org/10.2307/2425846
• Cosentino BJ, Schooley RL, Phillips CA (2010) Wetland hydrology, area, and isolation influence occupancy and spatial turnover of the painted turtle, Chrysemys picta Landscape Ecology 25: 1589-1600. https://doi.org/10.1007/s10980-010-9529-3
  » https://doi.org/10.1007/s10980-010-9529-3
• Deffune G, Klosowski ES (1995) Variabilidade mensal e interanual das precipitações pluviométricas de Maringá, 1976-1994. Revista Unicesumar 17: 501-510.
• De Leão SP, Famelli S, Vogt RC (2019) Home range of Yellow-Spotted Amazon River Turtles (Podocnemis unifilis) (Testudines: Podocnemididae) in the Trombetas River Biological Reserve, Pará, Brazil. Chelonian Conservation and Biology 18: 10-18. https://doi.org/10.2744/CCB-1273.1
  » https://doi.org/10.2744/CCB-1273.1
• Edge CB, Steinberg BD, Brooks RJ, Litzgus JD (2010) Habitat selection by Blanding’s turtles (Emydoidea blandingii) in a relatively pristine landscape. Ecoscience 17: 90-99. https://doi.org/10.2980/17-1-3317
  » https://doi.org/10.2980/17-1-3317
• Efford MG, Dawson DK, Robbins CS (2004) DENSITY: Software for analysing capture-recapture data from passive detector arrays. Animal Biodiversity and Conservation 27: 217-228.
• Efford MG, Warburton B, Coleman MC, Barker RJ (2005) A field test of two methods for density estimation. Wildlife Society Bulletin 33: 731-738. https://doi.org/10.2193/0091-7648(2005)33[731:AFTOTM]2.0.CO;2
  » https://doi.org/10.2193/0091-7648(2005)33[731:AFTOTM]2.0.CO;2
• Efford MG, Dawson DK, Jhala YV, Qureshi Q (2015) Density-dependent home-range size revealed by spatially explicit capture-recapture. Ecography 38: 001-013. https://doi.org/10.1111/ecog.01511
  » https://doi.org/10.1111/ecog.01511
• Fachín-Terán A, Vogt RC, Thorbjarnarson JB (2006) Seasonal movements of Podocnemis sextuberculata (Testudines: Podocnemididae) in the Mamirauá sustainable development reserve, Amazonas, Brazil. Chelonian Conservation and Biology 5: 18-24. https://doi.org/10.2744/1071-8443(2006)5[18:SMOPST]2.0.CO;2
  » https://doi.org/10.2744/1071-8443(2006)5[18:SMOPST]2.0.CO;2
• Fagundes C, Bager A, Cechin SC (2010) Trachemys dorbigni in an anthropic environment in southern Brazil: I) Sexual size dimorphism and population estimates. Herpetological Journal 20: 185-193.
• Fagundes CK, Vogt RC, Souza RA, Marco Jr P (2018) Vulnerability of turtles to deforestation in the Brazilian Amazon: Indicating priority areas for conservation. Biological Conservation 226: 300-310. https://doi.org/10.1016/j.biocon.2018.08.009
  » https://doi.org/10.1016/j.biocon.2018.08.009
• Famelli S, Souza FL, Georges A, Bertoluci J (2016) Movement patterns and activity of the Brazilian snake-necked turtle Hydromedusa maximiliani (Testudines: Chelidae) in southeastern Brazil. Amphibia-Reptilia 37: 1-14. https://doi.org/10.1163/15685381-00003047
  » https://doi.org/10.1163/15685381-00003047
• Figueiredo PICC (2014) Verificação da ocorrência de hibridação entre tartaruga-tigre-d’água, Trachemys dorbigni (Duméril and Bibron, 1835) e tartaruga-americana, Trachemys scripta (Thunberg and Schoepff, 1792) (Testudines, Emydidae). B.Sc. Thesis, Universidade Estadual do Rio Grande do Sul, Imbé, 33 pp. https://lume.ufrgs.br/handle/10183/107650
  » https://lume.ufrgs.br/handle/10183/107650
• Fonseca E, Both C, Cechin SZ, Winck G (2021) Pet distribution modelling: Untangling the invasive potential of Trachemys dorbigni (Emydidae) in Americas. Plos One 16(11): e0259626. https://doi.org/10.1371/journal.pone.0259626
  » https://doi.org/10.1371/journal.pone.0259626
• Forero-Medina G, Cárdenas-Arevalo G, Castaño-Mora OV (2011) Abundance, home range, and movement patterns of the endemic species Dahl’s Toad-Headed Turtle (Mesoclemmys dahli) in Cesar, Colombia. Chelonian Conservation and Biology 10(2): 228-236.
• Fortin G, Blouin-Demers G, Dubois Y (2012) Landscape composition weakly affects home range size in Blanding’s turtles (Emydoidea blandingii). Écoscience 19: 191-197. https://doi.org/10.2980/19-3-3528
  » https://doi.org/10.2980/19-3-3528
• French SS, Webb AC, Hudson SB, Virgin EE (2018) Town and country reptiles: A review of reptilian responses to urbanization. Integrative and Comparative Biology 58(5): 948-966. https://doi.org/10.1093/icb/icy052
  » https://doi.org/10.1093/icb/icy052
• Gavina MKA, Tahara T, Tainaka K, Ito H, Morita S, Ichinose G, et al. (2018) Multi-species coexistence in Lotka-Volterra competitive systems with crowding effects. Nature 8: 1-8. https://doi.org/10.1038/s41598-017-19044-9
  » https://doi.org/10.1038/s41598-017-19044-9
• Ghaffari H, Ihlow F, Plummer MV, Karami M, Khorasani N, Safaei-Mahroo B, Rödder D (2014) Home range and habitat selection of the endangered Euphrates Softshell Turtle Rafetus euphraticus in a fragmented habitat in Southwestern Iran. Chelonian Conservation and Biology 13: 202-215. https://doi.org/10.1002/aqc.3698
  » https://doi.org/10.1002/aqc.3698
• GISD (2024) Global Invasive Species Database. Species profile: Trachemys scripta elegans, Species profile: Trachemys scripta elegans, https://www.iucngisd.org/gisd/species.php?sc=71 [Accessed: 30/01/2024]
  » https://www.iucngisd.org/gisd/species.php?sc=71
• Gotelli NJ (2001) A Primer of Ecology. Sinauer Associates, Massachusetts, 291 pp.
• Grou CEV, Rocha SB, Cavalcanti LD, Oda FH, Alves DC, Oliveira LM, Zawadzki CH (2024) Anthropic influence on chelonian composition in a metropolitan region of Southern Brazil. Revista Observatório de la Economia Latinoamericana 22(7): 1-20. https://doi.org/10.55905/oelv22n7-176
  » https://doi.org/10.55905/oelv22n7-176
• Guedes TB, Entiauspe-Neto OM, Costa HC (2023) Lista de répteis do Brasil: atualização de 2022. Herpetologia Brasileira 12(1): 56-161. https://doi.org/10.5281/zenodo.7829013
  » https://doi.org/10.5281/zenodo.7829013
• Guzy JC, Price SJ, Dorcas ME (2013) The spatial configuration of greenspace affects semi-aquatic turtle occupancy and species richness in a suburban landscape. Landscape and Urban Planning 117: 46-56. https://doi.org/10.1016/j.landurbplan.2013.04.011
  » https://doi.org/10.1016/j.landurbplan.2013.04.011
• Hardin G (1960) The competitive exclusion principle. Science 131: 1292-1297.
• Hill SK, Vodopich DS (2013) Habitat use and basking behavior of a freshwater turtle community along an urban gradient. Chelonian Conservation and Biology 12: 275-282. https://doi.org/10.2744/CCB-0961.1
  » https://doi.org/10.2744/CCB-0961.1
• Howell HJ, Seigel RA (2019) The effects of road mortality on small, isolated turtle populations. Journal of Herpetology 53(1): 39-46. https://doi.org/10.1670/18-022
  » https://doi.org/10.1670/18-022
• Honora BT, Degrassi AL, Stephens RB, Rowe RJ (2019) Influence of field technique, density, and sex on home range and overlap of the southern red-backed vole (Myodes gapperi). Canadian Journal of Zoology 9(1): 1-35.
• Huey RB (1991) Physiological consequences of habitat selection. American Naturalist 137: S91-S115.
• Hunt SD, Guzy JC, Price SJ, Halstead BJ, Eskew EA, Dorcas ME (2013) Responses of riparian reptile communities to damming and urbanization. Biological Conservation 157: 277-284. https://doi.org/10.1016/j.biocon.2012.08.035
  » https://doi.org/10.1016/j.biocon.2012.08.035
• IUCN (2024) The IUCN Red List of Threatened Species. International Union for Conservation of Nature [ International Union for Conservation of Nature [ https://www.iucnredlist.org/ Accessed: 31/01/2024]
  » https://www.iucnredlist.org/
• Jaeger C, Cobb V (2012) Comparative spatial ecologies of female painted turtles (Chrysemys picta) and red-eared sliders (Trachemys scripta) at Reelfoot Lake, Tennessee. Chelonian Conservation and Biology 11(1): 59-67. https://doi.org/10.2744/CCB-0949.1
  » https://doi.org/10.2744/CCB-0949.1
• Köppen W (1978) Climatologia: con un estudio de los climas de la tierra. Fundo de Cultura Econômica, Buenos Aires, 478 pp.
• Lambert MR, McKenzie JM, Screen RM, Clause AG, Johnson BB, Mount GG, et al. (2019) Experimental removal of introduced slider turtles offers new insight into competition with a native, threatened turtle. PeerJ 7: e7444. https://doi.org/10.7717/peerj.7444
  » https://doi.org/10.7717/peerj.7444
• Latham SR, Sirén APK, Reitsma LR (2022) Space use and resource selection of Wood Turtles (Glyptemys insculpta) in the northeastern part of its range. Canadian Journal of Zoology 101: 20-31. https://doi.org/10.1139/cjz-2022-0052
  » https://doi.org/10.1139/cjz-2022-0052
• Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecological Monographs 62: 67-118.
• Lewis EL, Iverson JB, Smith GR, Rettig JE (2018) Body size and growth in Red-eared slider (Trachemys scripta elegans) at the Northern edge of its range: Does Bergmann’s rule apply? Herpetological Conservation and Biology 13(3): 700-710.
• Lindeman P (2020) A few moments with turtles: the value of freshwater Chelonians as watchable urban wildlife. Chelonian Conservation and Biology 19(2): 291-297. https://doi.org/10.2744/CCB-1421.1
  » https://doi.org/10.2744/CCB-1421.1
• Litzgus JD, Mousseau TA (2006) Home range and seasonal activity of Southern Spotted Turtles (Clemmys guttata): implications for management. Copeia 2004: 804-817. https://doi.org/10.1643/CH-04024R1
  » https://doi.org/10.1643/CH-04024R1
• Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. Blackwell Publishing, Chichester, 2^nd ed., 444 pp.
• Luiselli L (2008) Resource partitioning in freshwater turtle communities: A null model meta-analysis of available data. Acta Oecologica 34(1): 80-88. https://doi.org/10.1016/j.actao.2008.04.001
  » https://doi.org/10.1016/j.actao.2008.04.001
• Mali I, Weckerly FW, Simpson TR, Forstner MRJ (2016) Small scale-high resolution terrestrial activity of Trachemys scripta elegans, harvest intensity, and immediate movement responses following harvest events. Copeia 104(3): 677-682. https://doi.org.10.1643/CH-15-367
  » https://doi.org.10.1643/CH-15-367
• Manly BFJ, Mcdonald LL, Thomas DL, Mcdonald TL, Erickson WP (2002) Resource selection by animals: statistical design and analysis for field studies. Kluwer Academic Publishers, Boston, 221 pp.
• Marchand MN, Litvaitis JA (2004) Effects of habitat features and landscape composition on the population structure of a common aquatic turtle in a region undergoing rapid development. Conservation Biology 18: 758-767. https://doi.org/10.1111/j.1523-1739.2004.00019.x
  » https://doi.org/10.1111/j.1523-1739.2004.00019.x
• Martins FI, Souza FL, Costa HTM (2010) Feeding habits of Phrynops geoffroanus (Chelidae) in an urban river in central Brazil. Chelonian Conservation and Biology 9: 294-297. https://doi.org/10.2744/CCB-0809.1
  » https://doi.org/10.2744/CCB-0809.1
• Martins RA, Assalim AM, Molina FB (2014) The presence of Red-eared slider, Trachemys scripta elegans (Wied, 1838) (Testudines, Emydidae), an invasive species in the Paraibuna river basin, Southeastern Brazil. Herpetology Notes 7: 437-441.
• Michalski F, Norris D, Quintana I, Valerio A, Gibbs JP (2020) Substrate influences human removal of freshwater turtle nests in the eastern Brazilian Amazon. Nature 10: 8082. https://doi.org/10.1038/s41598-020-65074-1
  » https://doi.org/10.1038/s41598-020-65074-1
• Molina FB, Ferronato BO, Souza FL (2016) Freshwater Turtles in Natural, Rural and Urban Ecosystems in São Paulo State, Southeastern Brazil. In: Gheler-Costa C, Lyra-Jorge M, Verdade LM (Eds) Biodiversity in Agricultural Landscapes of Southeastern Brazil. De Gruyter Open, São Paulo, 151-162.
• Morreale SJ, Gibbons JW, Congdon JD (1984) Significance of activity and movement in the yellow-bellied slider turtle (Pseudemys scripta). Canadian Journal of Zoololgy 62: 1038-1042. https://doi.org/10.1139/z84-148
  » https://doi.org/10.1139/z84-148
• Morrow JL, Howard JH, Smith SA, Poppel DK (2001) Home range and movements of the Bog Turtle (Clemmys muhlenbergii) in Maryland. Journal of Herpetology 35: 68-73.
• Müller MMP, Ortega Z, Antunes PC, Seino LL, Hammarstron MJ, Balbino-Silva ACF, Oliveira-Santos LGR (2019) The home range of adult Phrynops geoffroanus (Testudines, Chelidae) in relation to sex and body mass. Herpetozoa 32: 259-265. https://doi.org/10.3897/herpetozoa.32.e38237
  » https://doi.org/10.3897/herpetozoa.32.e38237
• Munscher E, Gladkaya V, Stein J, Butterfield BP, Adams R, Gray J, et al. (2021) Movements of Western Alligator Snapping Turtles, Macrochelys temminckii (Testudines, Chelydridae), in an urban ecosystem: Buffalo Bayou, Houston, Texas. Herpetology Notes 14: 985-994.
• Painter C, Christman B (2000) Geographic distribution. Trachemys scripta Herpetological Review 253: 31.
• Paterson JE, Steinberg BD, Litzgus JD (2012) Generally specialized or especially general? Habitat selection by Snapping Turtles (Chelydra serpentina) in central Ontario. Canadian Journal of Zoology 90: 139-149. https://doi.org/10.1139/Z11-118
  » https://doi.org/10.1139/Z11-118
• Paul MJ, Meyer JL (2001) Streams in the urban landscape. Annual Review of Ecology and Systematics 32: 333-365.
• Pearson SH, Avery HW, Spotila JR (2015) Juvenile invasive red-eared slider turtles negatively impact the growth of native turtles: Implications for global freshwater turtle populations. Biological Conservation 186: 115-121. https://doi.org/10.1016/j.biocon.2015.03.001
  » https://doi.org/10.1016/j.biocon.2015.03.001
• Pérez-Santigosa N, Florencio M, Hidalgo-Vila J, Díaz-Paniagua C (2011) Does the exotic invader turtle, Trachemys scripta elegans, compete for food with coexisting native turtles? Amphibia-Reptilia 32(2): 167-175.
• Pérez-Santigosa N, Hidalgo-Vila J, Díaz-Paniagua C (2013) Comparing activity patterns and aquatic home range areas among exotic and native turtles in southern Spain. Chelonian Conservation and Biology 2(12): 313-319.
• Petrozzi F, Ajong SN, Pacini N, Dendi D, Bi SG, Fa JE, Luiselli L (2021) Spatial niche expansion at multiple habitat scales of a tropical freshwater turtle in the absence of a potential competitor. Diversity 13(55): 1-12. https://doi.org/10.3390/d13020055
  » https://doi.org/10.3390/d13020055
• Polo-Cavia N, López P, Martín J (2009) Interspecific differences in chemosensory responses of freshwater turtles: Consequences for competition between native and invasive species. Biological Invasions 11(2): 431-440. https://doi.org/10.1007/s10530-008-9260-z
  » https://doi.org/10.1007/s10530-008-9260-z
• Polo-Cavia N, López P, Martín J (2010) Competitive interactions during basking between native and invasive freshwater turtle species. Biological Invasions 12(7): 2141-2152. https://doi.org/10.1007/s10530-009-9615-0
  » https://doi.org/10.1007/s10530-009-9615-0
• Polo-Cavia N, López P, Martín J (2011) Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions 13(6): 1387-1396. https://doi.org/10.1007/s10530-010-9897-2
  » https://doi.org/10.1007/s10530-010-9897-2
• Plummer MV (1977) Activity, habitat and population structure in the Turtle, Trionyx muticus Copeia 1977: 431-440.
• Quesnelle PE, Fahrig L, Lindsay KE (2013) Effects of habitat loss, habitat configuration and matrix composition on declining wetland species. Biological Conservation 160: 200-208. https://doi.org/10.1016/j.biocon.2013.01.020
  » https://doi.org/10.1016/j.biocon.2013.01.020
• Rees M, Roe JH, Georges A (2009) Life in the suburbs: behavior and survival of a freshwater turtle in response to drought and urbanization. Biological Conservation 142: 3172-3181. https://doi.org/10.1016/j.biocon.2009.08.019
  » https://doi.org/10.1016/j.biocon.2009.08.019
• Richardson KS, Rouco C, Jewell C, French NP, Buddle B, Tompkins D (2017) Investigating brushtail possum (Trichosurus vulpecula) home range size determinants in a New Zealand native forest. Wildlife Research 44: 316-323.
• Rocha SB, Rouco C, Grou CEV, Ferreira VL (2022) Population characteristics and movement of native and exotics turtles in urban area. Research Square (Preprint). https://doi.org.10.21203/rs.3.rs-2175982/v1
  » https://doi.org.10.21203/rs.3.rs-2175982/v1
• Rocha SB, Grou CEV, Rouco C (2024) A novel approach to urban turtle sampling: Assessing Hookless Fishing with clip and two conventional methods. Annals of Brazilian Academy of Sciences 96(Suppl. 1): e20231185. https://doi.org/10.1590/0001-3765202420231185
  » https://doi.org/10.1590/0001-3765202420231185
• Romagosa CM (2015) Contribution of the live animal trade to biological invasions. In: Canning-Clode J (Ed.) Biological invasions in changing ecosystems - Vectors, ecological impacts, management and predictions. De Gruyter Open Poland, Warsaw, 116-134.
• Row JR, Blouin-Demers G (2006) Kernels are not accurate estimators of home-range size for Herpetofauna. Copeia 4: 797-802.
• R Core Team (2022) A language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
  » https://www.R-project.org/
• Rueda-Almonacid JV, Carr JL, Mittermeier RA, Rodriguez-Mahecha JV, Mast RB, Vogt RC, et al. (2007) Las Tortugas y los Cocodrilianos de los países andinos del trópico. Conservación Internacional, Bogotá, 597 pp.
• Ryan TJ, Conner CA, Douthitt BA, Sterrett SC, Salsbury CM (2008) Movement and habitat use of two aquatic turtles (Graptemys geographica and Trachemys scripta) in an urban landscape. Urban Ecosystems 11: 213-225. https://doi.org/10.1007/s11252-008-0049-8
  » https://doi.org/10.1007/s11252-008-0049-8
• Ryan TJ, Peterman WE, Stephens JD, Sterrett SC (2014) Movement and habitat use of the snapping turtle in an urban landscape. Urban Ecosystems 17: 613-623. https://doi.org/10.1007/s11252-013-0324-1
  » https://doi.org/10.1007/s11252-013-0324-1
• Sanchez J, Hudgens B (2015) Interactions between density, home range behaviors, and contact rates in the Channel Island fox (Urocyon littoralis). Ecology and Evolution 5(12): 2466-2477. https://doi.org/10.1002/ece3.1533
  » https://doi.org/10.1002/ece3.1533
• Santini L, González-Suárez M, Russo D, Gonzalez-Voyer A, Von Hardenberg A, Ancillotto L (2019) One strategy does not fit all: determinants of urban adaptation in mammals. Ecology Letters 22(2): 365-376. https://doi.org/10.1111/ele.13199
  » https://doi.org/10.1111/ele.13199
• Santos TG, Vasconcelos TS, Molina FB, Zaher H (2009) First record of Trachemys dorbigni (Duméril & Bibron, 1835) (Testudines, Emydidae) in a remnant of Mesophytic Semideciduous Forest of São Paulo State, southeastern Brazil. Herpetological Bulletin 108: 27-30.
• Santos EM, Souza DTMTO, Mascarenhas-Junior PB, Santos RL, Rameh-de-Albuquerque LC, Correia JMS (2020) Exotic testudines Trachemys elegans (Wied-Neuwied, 1839) and Trachemys dorbigni (Duméril and Bibron, 1835) in an Atlantic Forest fragment, Northeastern Brazil. Herpetology Notes 13: 1013-1016.
• Segurado P, Figueiredo D (2007) Coexistence of two freshwater turtle species along a Mediterranean stream: The role of spatial and temporal heterogeneity. Acta Oecologica 32: 134-144. https://doi.org/10.1016/j.actao.2007.03.015
  » https://doi.org/10.1016/j.actao.2007.03.015
• SEMA (2010) Bacias Hidrográficas do Paraná. Secretaria do Meio Ambiente, Maringá, 138 pp.
• SEMA (2011) Plano Municipal de conservação e recuperação da Mata Atlântica, Maringá - Paraná. Secretaria do Meio Ambiente, Maringá, 113 pp.
• SEMA (2020) Plano de Manejo do Parque do Ingá. Secretaria do Meio Ambiente, Maringá, 414 pp.
• Slabbekoorn H, Peet M (2003) Birds sing at a higher pitch in urban noise. Nature 424: 267-267.
• Silva I, Crane M, Marshall BM, Strine CT (2020) Reptiles on the wrong track? Moving beyond traditional estimators with dynamic Brownian Bridge Movement Models. Movement Ecology 8: 43. https://doi.org/10.1186/s40462-020-00229-3
  » https://doi.org/10.1186/s40462-020-00229-3
• Slavenko A, Itescu Y, Ihlow F, Meiri S (2016) Home is where the shell is: Predicting turtle home range sizes. Journal of Animal Ecology 85: 106-114. https://doi.org/10.1111/1365-2656.12446
  » https://doi.org/10.1111/1365-2656.12446
• Souza FL, Abe AS (2000) Feeding ecology, density and biomass of the freshwater turtle, Phrynops geoffroanus, inhabiting a polluted urban river in south-eastern Brazil. Journal of Zoology 252: 437-446.
• Souza FL, Abe AS (2001) Population structure and reprodutive aspects of the freshwater turtle, Phrynops geoffroanus, inhabiting an urban river in Southeastern Brazil. Neotropical Fauna and Environment 36(1): 57-62.
• Souza FL, Raizer J, Costa HYM, Martins FI (2008) Dispersal of Phrynops geoffroanus (Chelidae) in an urban river in central Brazil. Chelonian Conservation and Biology 7: 257-261. https://doi.org/10.2744/CCB-0698.1
  » https://doi.org/10.2744/CCB-0698.1
• Spinks PQ, Pauly GB, Crayon JJ, Shaffer HB (2003) Survival of the western pond turtle (Emys marmorata) in an urban California environment. Biological Conservation 113: 257-267. https://doi.org/10.1016/S0006-3207(02)00392-0
  » https://doi.org/10.1016/S0006-3207(02)00392-0
• Standing KL, Herman TB, Morrison IP (1999) Nesting ecology of Blanding’s turtle (Emydoidea blandingii) in Nova Scotia, the northeastern limit of the species’ range. Journal of Zoology 77: 1609-1614. https://doi.org/10.1139/z99-122
  » https://doi.org/10.1139/z99-122
• Taniguchi M, Lovich JE, Mine K, Ueno S, Kamezaki N (2017) Unusual population attributes of invasive red-eared slider turtles (Trachemys scripta elegans) in Japan: Do they have a performance advantage? Aquatic Invasions 12(1): 97-108. https://doi.org/10.3391/ai.2017.12.1.10
  » https://doi.org/10.3391/ai.2017.12.1.10
• Thomson RC, Spinks PQ, Shaffer HB (2010) Distribution and abundance of invasive red-eared sliders (Trachemys scripta elegans) in California’s Sacramento river basin and possible impacts on native western pond turtles (Emys marmorata). Chelonian Conservation and Biology 9: 297-302.
• Tortato MA, Bressan RF, Kunz TS (2014) Reproduction of two exotic species of Trachemys Agassiz, 1857 (Testudines, Emydidae) at Parque Estadual da Serra do Tabuleiro, state of Santa Catarina, southern Brazil. Herpetology Notes 7: 11-15.
• Villaseñor NR, Driscoll DA, Gibbons P, Calhoun AJK, Lindenmayer DB (2017) The relative importance of aquatic and terrestrial variables for frogs in an urbanizing landscape: Key insights for sustainable urban development. Landscape and Urban Planning 157: 26-35. https://doi.org/10.1016/j.landurbplan.2016.06.006
  » https://doi.org/10.1016/j.landurbplan.2016.06.006
• Vogt RC, Guzman SG (1988) Food partitioning in a Neotropical freshwater turtle community. Copeia 1988: 37-47.
• Zar JH (1996) Biostatistical Analysis. Prentice Hall, New York, 620 pp.
• Zenni RD, Brito MFG, Creed JC, Antar GM, Fabricante JR, Silva-Forsberg MC, et al. (2024) Status e tendências sobre espécies exóticas invasoras no Brasil. In: Dechoum MS, Junqueira AOR, Orsi ML (Org) Relatório Temático sobre Espécies Exóticas Invasoras, Biodiversidade e Serviços Ecossistêmicos. Editora Cubo, São Carlos, 49-91. https://doi.org/10.4322/978-65-00-87228-6.cap2
  » https://doi.org/10.4322/978-65-00-87228-6.cap2
• Ziller SR, Zalba S (2007) Propostas de ação para prevenção e controle de espécies exóticas invasoras. Natureza e Conservação 5(2): 8-15.

ADDITIONAL NOTES

• ZooBank register
  https://zoobank.org/6329EFF4-D0BD-4752-84BF-94F3F887208A
• How to cite this article
  Rocha SB, Rouco C, Grou CEV, Ferreira VL (2024) Freshwater turtle (Reptilia: Testudines) assemblage from an urban protected Atlantic Forest remnant: population density, movement and habitat preference. Zoologia 42: e24009. https://doi.org/10.1590/S1984-4689.v42.e24009
• Published by
  Sociedade Brasileira de Zoologia at Scientific Electronic Library Online - https://www.scielo.br/zool

• Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Code 001). SBR was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Code 001) and the Universidad de Córdoba by the postdoctoral contract (Plan Propio de Investigación).

Edited by

• Editorial responsibility
  Fabricius M.C.B. Domingos

Publication Dates

• Publication in this collection
  27 Jan 2025
• Date of issue
  2025

History

• Received
  07 Feb 2024
• Accepted
  29 Oct 2024