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The term “unusual mortality event” (UME) is defined, according to the Marine Mammal Protection Act in U.S. national policy, as a stranding that is unexpected involving a significant die-off of any marine mammal population (NOAA 2015). Between the seven criteria that determine whether a mortality event is ‘unusual,’ it includes ‘higher than expected numbers of stranded marine mammals in a given time and location’ (NOAA 2015). In this paper, we have also considered the term UME for sea turtles, in view of a significant stranding of leatherback turtles that occurred mainly in October 2016, on the southern coast of São Paulo State, Brazil.

The leatherback turtle (Dermochelys coriacea) is the largest sea turtle species with a worldwide tropical and subtropical distribution (Eckert 2006). It is a highly pelagic animal that spends most of its life in the open sea, feeding on jellyfish, salps, and other gelatinous organisms distributed in the water column (Marquez 1990). Houghton et al. (2006) suggested that jellyfish aggregations are associated with leatherback distribution in the northeast Atlantic. Leatherback turtles are able to perform transoceanic migrations from reproductive to foraging zones and back (Benson et al. 2007), and also among Temporary Residence Areas (TRAs) in neritic and oceanic domains according to multiple oceanographic conditions (Fossette et al. 2010). In Brazil, they are often seen at sea along the coast, with a higher concentration of individuals along the southern and southeastern coasts (Barata et al. 2004; Monteiro et al. 2016). The Brazilian nesting population for this species is restricted to a few individuals on the northern coast of Espírito Santo State (Thomé et al. 2007), although rare nesting has been observed in other locations along the coast (Barata & Fabiano 2002; Bezerra et al. 2014).

The International Union for the Conservation of Nature (IUCN) currently classify Dermochelys coriacea as Vulnerable, but in Brazil, it is listed as Critically Endangered on the Brazilian list of threatened species (Tiwari et al. 2013; MMA 2014). Major threats include incidental capture by industrial fisheries (Lewison et al. 2004; Fiedler et al. 2012) and destruction of coastal nesting habitats (Pritchard 1996), and in the special case of the main nesting area for Brazilian leatherback population next to Rio Doce Mouth in Espírito Santo State, contamination due to the most serious environmental disaster in Brazil, the Samarco mining waste dam collapse, that occurred in 2015 (Miranda &Marques 2016). High priority should be placed on the monitoring of leatherback distribution, population levels and threats, as a way to continually assess the status of the species (IUCN/SSC 1995). According to multi-scale “regional management units” (RMUs) (Wallace et al. 2010), the leatherback turtle RMU in the SW Atlantic is considered in the High Risk - High Threat category, therefore, the most urgent conservation interventions are necessary in this region (Wallace et al. 2011); this includes the Brazilian coast.

Here we report on an UME of leatherback turtles, which occurred in 2016, on the southeastern coast of Brazil, correlating the cause with biological, environmental and anthropogenic factors. The results contribute to monitoring the status of the species in the South Atlantic in support of conservation efforts.

The study area is located on the southern coast of São Paulo State, on the oceanic side of three islands: Iguape, Ilha Comprida and Ilha do Cardoso (Cananeia), a total of 136 km in length (Fig. 1). The highest rainfall rates occur from January to March, with a monthly average of 266.9 mm, while the lowest rates are recorded in July and August, with a monthly average of 95.3 mm (Silva 1989). From January to September, southwest winds predominate and, from October to December, the prevailing winds come from the east (Bergamo 2000). In the coastal region, wave trains predominate from the southeast quadrant, with a wave height of approximately 1 m (Araujo 2005). The residual tidal currents and the residual littoral transport of sediment act in the northeast direction, parallel to the coast (Picarelli et al. 2002).

Figure 1. Study area located on the oceanic face of Ilha do Cardoso, Ilha Comprida and Iguape, southern coast of São Paulo State, Brazil. The colored dots indicate stranding locations of leatherback turtles according to sex from August 2015 to July 2017, a total of 20 individuals in Ilha Comprida, 5 in Iguape and 4 in Ilha do Cardoso.

Leatherback turtle stranding data were obtained via daily beach surveys of Projeto de Monitoramento de Praias da Bacia de Santos (PMP-BS) conducted by Instituto de Pesquisas Cananeia (IPeC), from August 2015 to July 2017, along 100 km of Iguape, Ilha Comprida and Ilha do Cardoso. The PMP-BS is one of the conditions required by IBAMA as part of the environmental licensing process for oil and gas exploration, production and transport in the Pre-Salt region (25.08333°S, 42.5833°W to 25.9167°S, 43.5667°W), between the isobaths of 2,100 - 2,300 m.

Each leatherback turtle was photographed, measured (curved carapace length = CCL and total length = head to tail) and we recorded date, latitude, longitude, tag numbers (if present), and decomposition stage defined as COD 2 = freshly dead, COD 3 = moderate decomposition, COD 4 = advanced decomposition and COD 5 = mummified or only bone remains. We also recorded signs of anthropogenic interactions. Necropsies of carcasses at CODs 2, 3 and 4 were performed to evaluate possible cause of death, sex identification, and samples were collected for histopathological, contaminant, and genetic analyses.

Leatherback turtles were considered adult if CCL was larger than the minimum size at the nearest nesting site in Espírito Santo: 139 cm (Thomé et al. 2007). All the information was included in the Aquatic Biota Monitoring System (SIMBA) and screened by a filter tool to perform data analysis.

We recorded 29 dead stranded leatherback turtles between August 2015 and July 2017 in the study area; October 2016 was the month with the highest stranding occurrence (n = 15), but the UME began the previous month of September (n = 3) and continued into early November 2016 (n = 4), with a total of 22 recorded stranded turtles (Fig. 2). The mean size of leatherback turtles was CCL = 138.0 cm ± 17.2 SD, range: 98 - 171 cm (n = 17), and mean total length = 186.1 cm ± 19.4 SD, range: 140 - 218 cm (n = 17). Eleven specimens were considered adults and six were subadults. Most of these animals were in the advanced decomposition stage, mainly COD 4 (n = 12) (Fig. 3).

Figure 2. Dermochelys coriacea strandings from August 2015 to July 2017 in the study area.

Figure3. Percentage of dead leatherback turtles according to decomposition stage. COD 2: n = 3; COD 3: n = 6; COD 4: n = 12; COD 5: n = 8 (see text for COD descriptions).

Of the 29 individuals, 13 were males, five were females and 11 were of indeterminate sex due the advanced decomposition stage. Fig. 1 shows the location of each leatherback stranded according to sex, within the study area. The female turtles were concentrated further north in Ilha Comprida and Iguape, while males were recorded along the three island coasts. Sex could not be determined for the majority of individuals distributed along Ilha do Cardoso and Ilha Comprida.

On 22 October 2016, we found a dead leatherback turtle with a flipper tag (ASF 14479) on Jureia beach, Iguape, São Paulo State, Brazil (24.59°S and 47.28°W). The stranded carcass was severely decomposed (COD 4), measuring approximately 193 cm in total length, from head to tail. This female leatherback turtle had been originally tagged on 23 November 2009 at Mayumba National Park (3.75°S and 10.99°E) in southern Gabon, in the east Atlantic, measuring 142 cm (CCL), and was observed re-nesting on 21 December 2009 on the same beach.

During beach surveys, unusual strandings of non-target fauna (other than marine birds, marine mammals and sea turtles) were also recorded. In October 2016, the same period of the UME of leatherback turtles, we also recorded unusual blooms of jellyfish (Scyphozoa) washed ashore, mainly in Ilha Comprida. Six leatherback turtles presented jellyfish and crustaceans in their stomach contents. Out of 18 leatherback turtle carcasses necropsied, 11 presented signs of interaction with fishing gears (Fig. 4) and four had ingested small amounts of plastic debris.

Figure 4. Male leatherback turtle (CCL = 144 cm) found in October 2016 at Ilha Comprida, SP, with linear cutaneous marks on neck and flippers suggesting gill net entanglement.

The highest number of leatherback strandings in October 2016 (n = 15/29), early austral spring, in the southern coast of São Paulo, could be explained by an association of important factors: jellyfish abundance and distribution, a La Niña event (NOAA 2016), and fishing effort during this period (Mendonça 2015). Monteiro et al. (2016) cited a mass-stranding event of 84 leatherback turtles recorded in November and December 2005 in Rio Grande do Sul, and associated the cause to unusual blooms of jellyfish that probably promoted a leatherback aggregation nearshore, thereby increasing the risk of bycatch in coastal fisheries. The same hypothesis may explain our observations. Jellyfish blooms also occurred during the period of leatherback UME in October 2016, as evidenced by large quantities of jellyfish washed ashore and recorded by beach surveys, mainly in Ilha Comprida, where the highest number of stranded leatherbacks was also recorded (n = 20/29). Both UMEs of leatherbacks in 2005 in Rio Grande do Sul and in 2016 in São Paulo occurred in La Niña years. This phenomenon usually increases winds from the southeast in the Southern Hemisphere (trade winds), that may have brought more jellyfish from oceanic to coastal waters, hence increasing the number of foraging leatherback turtles and the chances of incidental capture in fisheries, as seen in Monteiro et al. (2016). Leatherback distribution has previously been linked to jellyfish hotspots in the northeast Atlantic (Houghton et al. 2006) and TRAs corresponding to foraging areas all around the Atlantic Ocean (Fossette et al. 2010), which corroborate the findings in our study. Considering that we recorded carcasses at COD 2 (n = 3) and COD 3 (n = 6) stages, it is assumed that at least these nine turtles died in nearshore waters, victims of bycatch in coastal fisheries. In fact, we recorded 11 individuals with anthropogenic interaction marks related to fishing activities, mainly gillnets. Koch et al. (2013) verified that for turtle carcasses, there is a negative relationship between distance from shore and likelihood of stranding on the coast, and animals that die offshore may never strand.

Eckert (2006) proposed that movements of leatherback turtles from one foraging area to another are driven by the opportunity to forage in areas of distinct oceanic structure, which serve to concentrate their gelatinous prey (e.g., salps, Scyphomedusae, Siphonophora) either at or below the surface. Fossette et al. (2010) identified nine TRAs in the neritic domain, confirming that leatherback turtles are also neritic foragers; the authors verified that these TRAs were associated with mesoscale surface oceanographic features of different types, such as altimetric features and/or surface chlorophyll a concentration (Fossette et al. 2010). Thus, the oceanographic features of the southern coast of São Paulo State influenced by La Niña in October 2016, provided conditions for leatherbacks using the TRAs near the study area to forage on jellyfish nearshore, becoming more susceptible to fishery bycatch and stranding.

The nesting season for leatherback turtles in the nearest nesting site in Espírito Santo to the study area (approximately 1,120 km of distance) is from September to March, corroborating the presence of mature adults during the UME in the study area. The turtles could also have approached neritic waters possibly in the course of breeding or post-nesting migrations. Higher numbers of males (n = 13/29) than females (n = 5/29) suggest that females could be more concentrated northward near, the nesting areas in Espírito Santo, possibly in their internesting intervals between clutch deposition events. However, the female leatherback tagged in Gabon indicated that stranded individuals may belong to different Atlantic populations. Fossette et al. (2010), in fact, showed that two satellite-tagged individuals from different nesting populations (Southeast and Southwest Atlantic) used the same TRA, suggesting a potential connection between turtles from both sides of the South Atlantic.

Billes et al. (2006) already presented evidence of leatherback movement from Africa to Brazil reporting three females tagged in Gabon between 2002 and 2003, recovered in southern and southeastern Brazil, after two years. The stranded female leatherback tagged in Gabon in 2009 found in the present UME, was recaptured after seven years, the longest interval recorded for the species on Brazilian coasts. In addition to mark-recapture with metal tags and/or PIT tags, genetic analysis (Vargas et al. 2008) and satellite telemetry (Fossette et al. 2010; Witt et al. 2011) also confirm the important role played by the southern waters of South America for Gabon’s leatherback nesting population, the largest rookery for this species.

Most stranded individuals observed were severely decomposed, making it impossible to determine the cause of death. However, evidence of anthropogenic interactions was recorded, including fishery bycatch and plastic debris. During the UME period, no “extraordinary” fishing effort occurred in the study area according to local fisheries inspection institutions (personal communication to the authors). Mendonça (2015) reported that the highest average fish landing in the southern coast of São Paulo in 2010 was October to February, overlapping with the UME period. We presume that jellyfish blooms initially aggregate leatherback turtles to forage, increasing their vulnerability to capture by legal coastal fisheries. Plastic may easily be mistaken for jellyfish by leatherback turtles, potentially causing blockage of the gut (Mrosovsky et al. 2009). In the present study, four individuals ingested non-lethal amounts of plastic, which may potentially reduce the extent of the gut from which absorption can occur and may well impair health and reproduction (Mrosovsky et al. 2009).

The UME of 22 leatherback turtles in September, October and early November 2016 on the southern coast of São Paulo State was significant due to the current conservation status of the species. Unusual blooms of jellyfish during that period were driven from oceanic to shallow waters by the increase of SE trade winds caused by La Niña, possibly attracting leatherback turtles to forage and increasing their risk of bycatch in coastal fisheries. The results of histopathological and contaminant analyses may contribute to a better explanatory diagnosis for this UME.

Understanding and investigating UMEs of threatened species such as leatherback turtles is extremely important because they can serve as indicators of ocean health, giving insight into larger environmental issues. However, stranded carcasses represent a minimum measure that usually does not exceed 10 - 20% of total at-sea mortality (Epperly et al. 1996; Koch et al. 2013), meaning that many more turtles were probably dead at sea than the number observed washed ashore. Contaminated food, plastic debris and overfishing are examples of main threats that this species and many others are facing. Conservation of highly migratory marine species such as Dermochelys coriacea requires international cooperation for implementation of transboundary management strategies to be truly effective.

Acknowledgments. We are grateful to the Instituto de Pesquisas Cananéia (IPeC) for logistics support. Sea turtle research in Gabon was carried out by Aventures Sans Frontieres and the Wildlife Conservation Society and is funded by the Marine Turtle Conservation Fund (United States Fish and Wildlife Service, Department of the Interior). We are grateful to all the field teams involved in monitoring and tagging of Gabon’s nesting leatherbacks.

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