The large and continuous decline of marine megafauna has caused serious consequences on the viability of coastal ecosystems worldwide (Jackson et al. 2001). Sea turtles are directly or indirectly impacted by a variety of threats such as pollution, habitat loss, climate change, interaction with fisheries, and ingestion of marine debris (Bugoni et al. 2001; Attademo 2007; Thompson et al. 2009; Hamann et al. 2010). Some of these threats have been observed in the coast of Rio Grande do Norte (RN), northeastern Brazil, where small-scale, multispecies fishing with set nets is practiced by small boats operating mainly in the coastal zone (Cunha et al. 2012). A large amount of the overall debris ingested by sea turtles in Brazil consists of plastic bags, which even in small amounts may lead to gastrointestinal obstruction such as faecaloma (i.e., mass of hardened feces considered as a phatological intestinal condition) or visceral rupture, and consequently death (Hutchinson and Simmons 1991; Bjorndal et al. 1994; Bjorndal 1997; Orós et al. 2005; Santos et al. 2015; Colferai et al. 2017).

Sea turtle strandings provide valuable data on the frequency of occurrence and distribution of marine vertebrate species in adjacent areas, contributing to the study of marine turtle stocks in foraging areas (Maldini et al. 2005; Pyenson 2010; Peltier et al. 2012). Strandings involving all sea turtle species occurring in Brazil, predominantly Chelonia mydas, were registered in the Potiguar Basin, RN, during 2010 and 2011 (Fragoso et al. 2012). Nevertheless, in spite of the studies on the diversity and distribution of marine turtles in the proposed region (Marcovaldi and Laurent 1996; Soto and Beheregaray 1997; Trigo 2000; Bugoni et al. 2001; Silva et al. 2007; Marcovaldi et al. 2010; Reis et al. 2011), data on their actual presence in this area are still limited.

This article describes the composition, spatial distribution, seasonality, and signs of anthropogenic interaction in sea turtle species stranded in the Potiguar Basin during a 7-yr period (from 2010 to 2016) and is aimed at providing data to support future management and conservation measures to protect local marine species.

Methods. — This study was carried out along approximately 300 km of the northeastern Brazilian coast, between the municipal district of Caiçara do Norte (5°4′1.15″S, 36°4′36.41″W) in RN State and the municipal district of Icapuí (4°38′48.28″S, 37°32′52.08″W) in Ceará State (CE) within the Potiguar Basin (Fig. 1).

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Since 2010, the Costa Branca Cetacean Project – University of Rio Grande do Norte State (Projeto Cetáceos da Costa Branca – Universidade do Estado do Rio Grande do Norte [PCCB-UERN]) has conducted the Beach Monitoring Program in the Potiguar Basin (Programa de Monitoramento de Praias da Bacia Potiguar [PMP-BP]), Brazil. The PMP-BP is part of an environmental constraint compliance enforced by the Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA) over the presalt oil exploitation operated by Petróleo Brasileiro S.A. (Petrobras; agreement no. 2500. 005657510.2).

We analyzed data obtained during daily monitoring throughout 7 uninterrupted years (from 1 January 2010 to 31 December 2016) by trained field-team personnel using a traction vehicle (quadricycle type) and a portable global positioning system (GPS) to record the location of dead or debilitated stranded sea turtles. The latter were clinically evaluated by veterinarians and conducted to a rehabilitation center in Areia Branca, RN. We examined the carcass condition of all stranded sea turtles in order to record external signs of anthropogenic interaction (e.g., fragments and marks of fishing nets, knife-cut signs). Moderately decomposed specimens (condition codes D2 and D3) (Flint et al. 2009) were necropsied and examined for the presence of marine debris in their gastrointestinal tract and signs of drowning (presence of water in the celomic cavity). These debris were collected and preserved in 70% alcohol solution and classified into four categories: soft plastic (transparent and colored), rigid plastic, fishing artifacts, and others (i.e., rubber, elastic, artificial sponges, styrofoam, and piercing objects).

Curved carapace length (nuchal to notch length between supracaudal scales) (Bolten 1999) was recorded using a flexible tape. Owing to the high temperatures recorded in northeastern Brazil, which can compromise the viability of histological analysis, we did not collect gonad samples. Therefore, we distinguished between juveniles and adults according to size of the examined sea turtles, referring to the smallest size recorded for nesting females in the largest and closest nesting area for each species in Brazil: ≥ 90 cm for C. mydas (Almeida et al. 2011), ≥ 83 cm for hawksbill turtles (Eretmochelys imbricata; Santos et al. 2010), ≥ 62.5 cm for olive ridley turtles (Lepidochelys olivacea; Silva et al. 2007), ≥ 86.5 cm for loggerhead turtles (Caretta caretta; Lima et al. 2012), and ≥ 139 cm for leatherback turtles (Dermochelys coriacea; Thomé et al. 2007). In our study, all specimens smaller than these minimum sizes for nesting females were classified as juveniles.

All procedures for sea turtle rescue and handling, and sample collection, were approved by the Chico Mendes Institute for Biodiversity Conservation (ICMBio), Ministry of the Environment through the Biodiversity Information and Authorization System (SISBIO) no. 13694-6, and Authorization and Information in Biodiversity (ABIO) no. 615/2015.

The Kolmogorov-Smirnov test was performed to verify data distribution. The Kruskal-Wallis test was used to 1) assess the number of strandings among different monitoring sites, 2) compare the frequency of strandings among the monitoring years, and 3) assess the number of records according to sea turtle species. A multivariate correspondence analysis (ANACOR) was applied to evaluate the correlation among the recorded species and the stranding location. Statistical analyses were performed with STATISTIC 7 software and at a significance level (alpha) of 0.05 for all tests.

Results. — A total of 4760 stranded sea turtles, including the 5 species occurring in Brazil, were recorded. The green sea turtle was the most common species, observed in 81.01% of the cases (n = 4205; p < 0.00001). The hawksbill sea turtle represented 3.51% (n = 167) of the strandings followed by olive ridleys (1.74%; n = 83), loggerheads (0.86%; n = 41), and leatherbacks (0.04%; n = 2). In 12.84% of the cases, it was not possible to identify the species due to the carcasses' advanced decomposition state (code D4 according to Flint et al. 2009).

The majority of recorded strandings involved juvenile sea turtles (69.64%; n = 3315), with variable class sizes according to the species. Stretch A had the highest number of sea turtle strandings (n = 2262; 47.52%) followed by stretches B (n = 1556; 32.69%), C (n = 515; 10.82%), and D (n = 427; 8.97%; p < 0.00001) (Fig. 2A). The correlation between location and species showed that C. mydas individuals were most commonly recorded in stretches A and B and E. imbricata in stretch C (marked cells > 10). The remaining species showed no particular correlation with any of the monitored areas.

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We observed a monthly variation in the number of sea turtle strandings, with an increasing trend for all the studied years between September and January and a downward trend in the following months (Fig. 2B). The analysis of annual stranding occurrence showed that all species occurred annually during the 7 studied years except for D. coriacea, recorded only in 2011 and 2014, and C. caretta which was not found in 2015. There was no significant difference among strandings for all species together throughout the studied years (p > 0.8366) (Fig. 2C).

The carcass condition analysis revealed marks of fishing nets or knife-cut signs in 579 specimens of C. mydas, 14 of E. imbricata, 13 of L. olivacea, and 9 of C. caretta. We found no marks on the examined leatherback sea turtles. Therefore, our results demonstrated that 94.15% of anthropogenic interactions occurred in C. mydas: 55.27% with fishing artifacts, 30.05% with cutting objects, 4.32% with injuries (head and carapace trauma related to punctures and punctual marks), and 4.15% with watercraft collision. There were also specimens with signs of drowning (1.04%; 6/579), projectile wounds (0.35%), and unidentified anthropogenic interaction (4.84%).

In regard to other sea turtle species, we observed a predominance of marks related to fishing artifacts in hawksbill (85.71%), olive ridley (84.62%), and loggerhead (77.78%) sea turtles. Marks caused by cutting objects occurred in 22.22% of the C. caretta, 7.69% of the L. olivacea, and 7.14% of the E. imbricata specimens. Head and carapace injuries (trauma) and drowning were registered, respectively, in 1 hawksbill and 1 olive ridley sea turtle.

Upon necropsy, 76% of the examined green sea turtles presented ulceration, inflammation, perforation, faecalomas, or other gross lesions caused by ingested marine debris. Plastic was the most frequent marine debris observed in C. mydas (82%): transparent soft (82%), colored soft (78%), and rigid (73%). Fishing artifacts and other types of marine debris were found, respectively, in 72% and 13% of the specimens.

Discussion. — Green sea turtles represented the majority of strandings (81.01%). Similar results were observed in other studies conducted in northeastern, southeastern, and southern Brazil (Trigo 2000; Bugoni et al. 2001; Reis et al. 2011; Poli et al. 2014). Previous studies on the size class of the stranded marine turtles in northeastern Brazil revealed that most green sea turtles observed during monitoring were juveniles (Gavilan-Leandro et al. 2013). Although our data were not based on capture–mark–recapture or telemetry, our findings suggest the study area as a possible feeding ground for green sea turtles.

Stretch A presented the highest number of strandings. According to Tabosa (2002), current and wind conditions tend to carry stranded animals to the north/west, possibly increasing the number of registered strandings in this area. In all species, especially C. mydas, such events occurred more frequently between September and January. Musick and Limpus (1997) suggested that some sea turtle populations living in temperate zones perform migrations to foraging areas at higher latitudes during summer and lower latitudes during winter while those of tropical environments exhibit more localized movements. Thus, C. mydas individuals registered in the Potiguar Basin were possibly looking for optimal developmental conditions, especially during the warmer months of the year.

Anthropic interaction was directly related to fishing in 55.27% of the strandings. Bugoni et al. (2001) recorded external signs of interaction with fisheries in 5.1% of the studied specimens. However, these findings are probably underestimated because interaction with fisheries is quite difficult to observe because fishing nets often do not leave visible marks on carcasses (Monteiro 2004).

It has been well known that the incidental catch in coastal and oceanic fisheries cause injury or death of several sea turtle species and are an important threat to them (Hall et al. 2000; Lewison et al. 2004). The Brazilian commercial longline fleet is responsible for a high frequency of sea turtle bycatch, and research carried out between 2001 and 2005 demonstrated incidental bycatch in northeastern Brazilian waters (Sales et al. 2008). In the west coast of RN, small boats operate mainly in coastal waters using gill nets and bottom trawls to target fish and shrimp (Cunha et al. 2012; Bomfim 2014). Considering that incidental catches occur all year round, we found a considerable number of sea turtle strandings related to fishing throughout the study period.

Green sea turtles were the most commonly affected species by coastal fishing (e.g., set nets), probably because of their coastal feeding habits (Gallo et al. 2006) associated with increasing and uncontrolled fishing (Domingo et al. 2006; Sales et al. 2008) such as the multispecies fishing activities performed at the Potiguar Basin (Attademo 2007).

Coastal environments are also increasingly affected by debris of human origin (Thompson et al. 2009). Plastic materials of different types and colors, and fishing artifacts, were the most common types of marine debris found in the gastrointestinal contents of the evaluated sea turtles (61.73%). Similar results were obtained in studies on C. mydas and C. caretta (Bugoni et al. 2001; Tomás et al. 2008). Small debris amounts are considered lethal and the direct cause of death in many animal species due to gastrointestinal tract obstruction or the presence of perforated ulcers (Day et al. 1985; Bjorndal et al. 1994; Bjorndal 1997). Intestinal and stomach obstruction, emaciation, and low weight were observed in green sea turtles that died due to debris-caused chronic processes (Santos et al. 2015; Colferai et al. 2017). Our research concurs with these findings: 67.86% (n = 76) of the necropsied sea turtles had complications due to marine debris ingestion, eventually leading to death.

Among all studied species, C. mydas presented the highest level of ingested anthropogenic marine debris (National Research Council 1990). Green sea turtles are known for their ontogenetic shift from omnivorous to herbivorous (Mortimer 1982; Bjorndal 1997) and their diet that is mainly based on seagrass and/or macroalgae, which may explain why these species are more affected by the presence of anthropogenic marine debris, because they usually do not chase preys (Bjorndal et al. 1994; Spotila 2004) and are found closer to the coast, where human impacts are cumulative. Green sea turtles are visual feeders and have the ability to distinguish colors (Mathger et al. 2007; Fritsches and Warrant 2013); therefore, the intake of colorful material may occur when these animals confuse it with their natural food, or by accident, as marine debris can often be found deposited on algae banks (Guerbet-Bartholo et al. 2011). Similarly to previous studies (Santos et al. 2015; Colferai et al. 2017), ingested plastic (mostly of transparent plastic) was found in 82 of the 100 evaluated green sea turtles.

In conclusion, green turtles presented the highest number of marine turtle strandings in the Potiguar Basin. Although fishing was the most common anthropogenic interaction in the study area, this study highlights the ingestion of marine debris as a serious threat to the conservation of marine turtles. Our results indicate that the Potiguar Basin is a significant habitat for sea turtles, especially for C. mydas, therefore requiring increased research efforts, environmental education (including recycling programs, information about reusable items, and waste reduction), and conservation of these endangered species.