Introduction
Burmeister's porpoise (Phocoena spinipinnis) is an endemic species found along the eastern and western coasts of South America. It ranges from Bahía de Paita, Peru (05°01'S) to Chile (42°30'S) in the west, and from Tierra del Fuego, Argentina (42°23'S) to Santa Catarina, Brazil (28°48'S) in the east (Brownell and Praderi, Reference Brownell and Praderi1984; Guerra et al., Reference Guerra-Correa, Van Waerebeek, Kandora and Jorquera1987; Simões-Lopes and Ximenes, Reference Simões-Lopes and Ximenez1989; Van Waerebeek et al., Reference Van Waerebeek, Santillan and Reyes2002). Recently, Weir and Rutherford (Reference Weir and Rutherford2019) reported a stranded specimen of P. spinipinnis in the Falkland Islands (51°40.9'S) in the Patagonian Continental Shelf, a region not previously considered within the species’ geographical range. Throughout its distribution, the species is more commonly reported in shallow inshore waters, although observations of individuals 20–50 km offshore have also been confirmed (Corcuera et al., Reference Corcuera, Monzón, Crespo, Aguilar and Raga1994; Clay et al., Reference Clay, Mangel, Alfaro-Shigueto, Hodgson and Godley2018; Santillán, Reference Santillán2022).
Like many cetaceans, the occurrence of P. spinipinnis is associated with various environmental features in both the southeast Pacific and southwest Atlantic coasts of South America, such as local currents, upwelling events, and contributions from continental runoff (Molina-Schiller et al., Reference Molina-Schiller, Rosales and de Freitas2005). The northern geographical limits on both sides of South America are influenced by the cold waters of the Humboldt Current in Peru and the Falkland/Malvinas Current in Uruguay and Brazil (Reyes and Van Waerebeek, Reference Reyes and Van Waerebeek1995; Molina-Schiller et al., Reference Molina-Schiller, Rosales and de Freitas2005). Although the holotype specimen was found in the La Plata River, Argentina, in 1865 (Burmeister, Reference Burmeister1865; Brownell and Praderi, Reference Brownell and Praderi1984), most knowledge about the species has come from stranded or by-caught specimens, due to its elusive and inconspicuous swimming behaviour and tendency to form small groups (Brownell and Praderi, Reference Brownell and Praderi1984; Corcuera et al., Reference Corcuera, Monzon, Aguilar, Borrell and Raga1995; Goodall et al., Reference Goodall, Würsig, Würsig, Harris and Norris1995a; Reyes and Van Waerebeek, Reference Reyes and Van Waerebeek1995; Rosa et al., Reference Rosa, Milinkovitch, Van Waerebeek, Berck, Oporto, Alfaro-Shigueto, Van Bressem, Goodall and Cassens2005; Garcia-Godos et al., Reference Garcia-Godos, Van Waerebeek, Reyes, Alfaro-Schigueto and Arias-Schreiber2007; Galatius et al., Reference Galatius, Berta, Frandsen and Goodall2011; Weir and Rutherford, Reference Weir and Rutherford2019; Marchesi et al., Reference Marchesi, Galatius, Zaffino, Coscarella and González-José2022; Padula et al., Reference Padula, Machado, Milmann, de León, Gana, Wickert, Argañaraz, Bastida, Rodríguez and Denuncio2023).
The first records of P. spinipinnis along the Brazilian coast date back to the mid- to late 1980s (Pinedo, Reference Pinedo1989; Simões-Lopes and Ximenez, Reference Simões-Lopes and Ximenez1989) when stranded carcasses were reported in the states of Rio Grande do Sul and Santa Catarina (28°48'S) (Figure 1). This extended the known distribution northward by 900 km from its previously known range in Uruguay. A few decades later, a record of P. spinipinnis was reported in Anchieta, Espírito Santo, southeastern Brazil, with no further details provided other than the geographical location of the stranding (Mayorga et al., Reference Mayorga, Vanstreels, Bhering, Mamede, Costa, Pinheiro, Reis, Trazzi, Meirelles, Ribeiro and Siciliano2020). This has remained the northernmost occurrence for the species in the southwestern Atlantic Ocean.
Figure 1. Previously known northernmost range of Phocoena spinipinnis in the Southwestern Atlantic Ocean (SWAO) in Santa Catarina state (SC) (black dot), new occurrence reported in this paper (red star) in Rio de Janeiro state (RJ) 930 km northward, and the occurrence reported in Mayorga et al. (Reference Mayorga, Vanstreels, Bhering, Mamede, Costa, Pinheiro, Reis, Trazzi, Meirelles, Ribeiro and Siciliano2020) in Espírito Santo State (ES) (black star). The monitoring areas for PMP-BS and Instituto Orca are represented by coastal orange and red polygons, respectively.
Based on two stranded carcasses found in 2014 and 2021, this study provides additional information on the occurrence of P. spinipinnis in southeastern Brazil in the southwestern Atlantic Ocean. It describes necropsy findings for the specimen previously reported in Anchieta by Mayorga et al. (Reference Mayorga, Vanstreels, Bhering, Mamede, Costa, Pinheiro, Reis, Trazzi, Meirelles, Ribeiro and Siciliano2020) and a new stranding in the state of Rio de Janeiro.
Materials and methods
The Laboratório de Mamíferos Aquáticos e Bioindicadores at Universidade do Estado do Rio de Janeiro (MAQUA/UERJ) is one of the institutions that monitors marine mammal strandings along approximately 1160 km of the central-south coast of the state of Rio de Janeiro in southeastern Brazil. Since 2017, a monitoring programme, the ‘Projeto de Monitoramento de Praias da Bacia de Santos (PMP-BS)’ has been conducted along the southern and southeastern Brazilian coast. This programme was established to meet the requirements of the federal environmental licensing institute, ‘Instituto Brasileiro do Meio Ambiente e Recursos Renováveis’ (IBAMA), for oil and natural gas production and extraction in the Santos Basin. The aim of PMP-BS is to assess the potential impacts of oil and gas activities on seabirds, sea turtles, and marine mammals through beach stranding monitoring, veterinary care to live animals, and necropsies of deceased individuals. The project covers 15 stors from Laguna/Santa Catarina to Saquarema/Rio de Janeiro, spanning southern to southeastern Brazil (Figure 1). The MAQUA/UERJ team is specifically responsible for collecting and conducting necropsies on stranded marine mammal carcasses in sectors 11–15, which encompass the south to central Rio de Janeiro State (Petrobras, 2023). Carcasses are typically reported through two methods: (1) active beach monitoring by technicians and researchers, who search for carcasses, or (2) reports from residents, visitors, tourists, or anyone in coastal areas who voluntarily report strandings, primarily through institutional phone numbers.
On 2 April 2021, residents of Praia da Vila, Saquarema municipality (22°54’4”W; 42°29’54”S) (Figure 1) reported a stranded dolphin carcass identified by the field team as P. spinipinnis. The total body length (TBL), sex, body condition, decomposition code, and photographs were taken in the field to document the in situ conditions of the specimen as found by the research team. The decomposition code was recorded following Geraci and Lounsbury (Reference Geraci, Lounsbury and Yates2005). The carcass was subsequently taken to the MAQUA/UERJ laboratory, where a necropsy was performed on 14 April 2021.
On 25 June 2014, a stranded carcass of P. spinipinnis was found in Praia de Parati, Anchieta municipality, Espírito Santo (see Mayorga et al., Reference Mayorga, Vanstreels, Bhering, Mamede, Costa, Pinheiro, Reis, Trazzi, Meirelles, Ribeiro and Siciliano2020 for detailed methods). Necropsy was performed on 1 July 2014.
Necropsies were performed by trained personnel, including marine mammal veterinarians. Teeth were collected in order to estimate age by the dentine growth layer groups (GLGs) (Perrin and Myrick, Reference Perrin and Myrick1980; Hohn et al., Reference Hohn, Scott, Wells, Sweeny and Irvine1989).
To evaluate vertebral count and cranial measurements, the carcass remains were macerated for approximately 120 days until the skeleton was completely free of tissue residue. The skeleton was then cleaned with mild soap and a brush, followed by air-drying under ambient conditions.
Thirty cranial measurements were taken using a 300 mm Vernier caliper, following Perrin (Reference Perrin1975) and Goldin and Vishnyakova (Reference Goldin and Vishnyakova2015). Some measurements described by Perrin (Reference Perrin1975) were not feasible due to the loss of specific parts of the skull.
Similar stranding monitoring is also conducted by Instituto ORCA, which collects stranded carcasses along approximately 260 km of the state of Espírito Santo coast in southeastern Brazil (methods described in Mayorga et al., Reference Mayorga, Vanstreels, Bhering, Mamede, Costa, Pinheiro, Reis, Trazzi, Meirelles, Ribeiro and Siciliano2020) (Figure 1). The characteristics of the specimen stranded in Anchieta, Espírito Santo and first reported by Mayorga et al. (Reference Mayorga, Vanstreels, Bhering, Mamede, Costa, Pinheiro, Reis, Trazzi, Meirelles, Ribeiro and Siciliano2020), were also described based on necropsy findings. However, age, vertebral count, and cranial measurements were not determined for this specimen.
Results
In situ observations in Praia da Vila revealed an almost entirely skinless carcass of Phocoena spinipinnis, measuring 154 cm of TBL, and in late decomposition (code 4 according to Geraci and Lounsbury, Reference Geraci, Lounsbury and Yates2005), with missing eyes and partially macerated jaws (Figure 2). Four suggestive post-mortem shark bites were also observed: A – genital slit (27 cm × 11.5 cm); B – umbilicus/thoracic cavity (21 cm × 11.5 cm); C – right ventral lateral thorax (29 cm × 11.5 cm); and D – ventral portion of the head (cervical to zygomatic arch) (20 cm × 11.5 cm) (Figure 2).
Figure 2. Stranded Burmeister's porpoise, Phocoena spinipinnis, in the states of Rio de Janeiro (A–C) and Espírito Santo (D), southeastern Brazil. (A) Head with partially macerated left jaw, ventral laceration by suggestive post-mortem shark bites, presence of teeth and absence of the left eye; (B) Suggestive post-mortem shark bites on umbilicus/thoracic cavity and genital slit; (C) Low, triangular-shaped canted backward dorsal fin; (D) Specimen found stranded in Praia de Parati, Anchieta, Espírito Santo.
Despite its advanced decomposition, necropsy revealed a male specimen confirmed by the preservation of the penis (Figure 3). The stomach was absent, preventing any analysis of its contents. Autolysis had compromised all organs, including those of the respiratory, cardiovascular, reproductive (testicles), endocrine, lymphatic, haematopoietic, and nervous systems, making further investigation impossible. Teeth were preserved, totaling to 15 and 17 pairs in both lower and upper jaws, respectively (Figure 3).
Figure 3. Specimen of Burmeister's porpoise, Phocoena spinipinnis, stranded in the state of Rio de Janeiro, southeastern Brazil in April 2021, during necropsy (A) and evidence of penis (B) and teeth (C).
The vertebral count was 7 cervical (Cv) (Cv1–3 fused), 13 thoracic (Th), 15 lumbar (L), and 27 caudal vertebrae (Cd) (Figure 4). Except for a few caudal vertebrae, epiphyses were not fused. There were also 13 pairs of ribs, with articulations present on the first eight pairs. The age was estimated to be 3 years based on the count of growth layer groups (GLGs). Table 1 shows the 30 cranial measurements obtained from the specimen sampled in Rio de Janeiro.
Figure 4. Vertebral structure of a Burmeister's porpoise, Phocoena spinipinnis, stranded in the state of Rio de Janeiro, southeastern Brazil in April 2021. Cv – cervical; Th – thoracic; Lb – lumbar and Cd – caudal. Scale bars: 5 cm.
Table 1. Skull measurements (mm) of a Burmeister's porpoise (Phocoena spinipinnis) specimen stranded in Praia da Vila, Saquarema, Rio de Janeiro, southeastern Brazil in April, 2021
Necropsy observations of the P. spinipinnis specimen found on Praia de Parati, Anchieta municipality, Espírito Santo reported a 162 cm male individual in a late decomposition state (Figure 2), with small patches of preserved skin tissue on the caudal peduncle and the tip of the dorsal fin; eyes were absent and internal organs exhibited gas formation. Two unidentified teleost fishes were found in the stomach content. The testicles measured between 12 and 15 cm each. Teeth were preserved, adding up to 13 and 17 pairs in both lower and upper jaws, respectively (Figure 5).
Figure 5. Dorsal, ventral, and lateral view of the skull, and inner and outer side of the left mandible of a Burmeister's porpoise, Phocoena spinipinnis, stranded in the state of Rio de Janeiro, southeastern Brazil, in April 2021. Scale bars: 5 cm.
Discussion
We report here the two northernmost occurrences of P. spinipinnis in the Southwestern Atlantic Ocean to date and the first record of the species in Rio de Janeiro State, to our knowledge. This phocoenid species is described as not exceeding a total body length of more than 200 cm (Goodall et al., Reference Goodall, Würsig, Würsig, Harris and Norris1995a). One of the main characteristics of P. spinipinnis described by Goodall et al. (Reference Goodall, Würsig, Würsig, Harris and Norris1995a) is the blunt head without a distinct beak, with the forehead dropping rather abruptly to the rostrum tip. Additionally, the species is noted for a short gape and eyes positioned forward of the blowhole. In addition to the spatulate teeth typical to phocoenids, one of the species’ diagnostic features is the low, triangular canted backward dorsal fin located posterior to the midpoint of the body and covered with tiny tubercles similar to spines on its leading edge.
Due to the advanced stage of carcass decomposition, we were unable to determine the coloration of either specimen. However, in both cases, the presence of spatulate teeth, the blunt head, and the distinctive dorsal fin shape matched the previously described characteristics of P. spinipinnis, making misidentification highly unlikely. The vertebral count for the Rio de Janeiro specimen was similar to that previously reported in the literature (Brownell and Praderi, Reference Brownell and Praderi1984; Reyes, Reference Reyes, Würsig, Thewissen and Kovacs2018), although a lower number of caudal vertebrae was observed in this study. Additionally, we could not rule out some skeletal loss due to shark bites, despite the specimen appearing to be well preserved.
The total body length and epiphyseal fusion, observed in less than 10% of the vertebral column, suggest a physically immature individual in Rio de Janeiro (Corcuera et al., Reference Corcuera, Monzon, Aguilar, Borrell and Raga1995; Reyes and Van Waerebeek, Reference Reyes and Van Waerebeek1995). Male P. spinipinnis were previously reported to not attain sexual maturity between 158 and 175 cm (Goodall et al., Reference Goodall, Würsig, Würsig, Harris and Norris1995a; Reyes and Van Waerebeek, Reference Reyes and Van Waerebeek1995). However, Corcuera et al. (Reference Corcuera, Monzon, Aguilar, Borrell and Raga1995) observed physically mature male specimens at 169 cm and 3 + GLGs. At this stage, the authors also reported a vertebrae fusion of more than 40%, contrasting with our findings for the studied specimen. An important observation regarding the skull of the Rio de Janeiro specimen is that it was clearly not fully fused, suggesting an immature individual with a condylobasal length attaining 272 mm. In contrast, Molina-Schiller (Reference Molina-Schiller2006) reported that males attain physical maturity when the condylobasal length is ⩾266 mm. Although this difference may be due to geographic variations among populations, the authors did not have a sufficient sample size from Brazilian waters (n = 2) to confirm significant differences. Recent data on maturity for P. spinipinnis reported pubescent individuals ranging from 142 to 154 cm (Vega et al., Reference Vega, Van Waerebeek, Alfaro-Shigueto, Reyes and Van Bressem2022), providing further evidence to classify the maturity status of the Rio de Janeiro specimen. Accounting for total body length, the specimen found in Espírito Santo could be classified as mature according to previous studies (Goodall et al., Reference Goodall, Würsig, Würsig, Harris and Norris1995a; Reyes and Van Waerebeek, Reference Reyes and Van Waerebeek1995). Furthermore, Vega et al. (Reference Vega, Van Waerebeek, Alfaro-Shigueto, Reyes and Van Bressem2022) reported mean testicle and total body lengths of 119.4 mm and 166.39 cm, respectively, which corroborate findings for the Espírito Santo specimen.
Although the carcasses were highly decomposed, it seems unlikely that they drifted from its known previous northernmost range in southern Brazil (Simões-Lopes and Ximenez, Reference Simões-Lopes and Ximenez1989) to the states of Rio de Janeiro and Espírito Santo, which are 930 and 1280 km further north, respectively. The strandings were reported right after the end of the austral summer in Rio de Janeiro and the beginning of the austral autumn in Espírito Santo. These timings are not consistent with a strong northward movement of Subtropical Convergence (the encounter of a cold northward flow of Falkland/Malvinas current with a warmer southward flow of Brazil current), occurring primarily during the austral winter, and previously recognized as one of the main oceanographic features influencing the occurrence of P. spinipinnis in Brazilian waters (Molina-Schiller et al., Reference Molina-Schiller, Rosales and de Freitas2005). Given the rarity of these stranding events, this suggests a potential occurrence of P. spinipinnis further north in Brazilian waters.
While the influence of the Subtropical Convergence seems unlikely in our case, at least three other factors should be considered: (1) the species’ unobtrusive swimming behaviour and small group formation (Goodall et al., Reference Goodall, Norris, Harris, Oporto and Castello1995b; Santillán, Reference Santillán2022); (2) the South and Southeastern Brazilian continental shelf, which varies in width from 70 to 230 km offshore with depths of ⩽200 m (Mahiques et al., Reference Mahiques, Sousa, Furtado, Tessler, Toledo, Burone, Figueira, Klein, Martins and Alves2010); and (3) the presence of the nutrient-rich South Atlantic Central Waters (SACW) in mid- and outer continental shelf, along with its upwelling near the study area (Castelão and Barth, Reference Castelão and Barth2006). The former may suggest more challenging conditions for sightings by scientific expeditions, while the second supports the possibility of groups travelling further north within deeper waters of the continental shelf. Phocoena spinipinnis was already reported in waters up to 100 m in depth (Clay et al., Reference Clay, Mangel, Alfaro-Shigueto, Hodgson and Godley2018), resulting in decreased sighting probability due to limited scientific effort in offshore waters and rough sea conditions. The presence of nutrient-rich waters supports the occurrence of the species in a highly productive area. The water temperatures and salinities are below the representative values known to limit species’ geographical distribution in both the Pacific and Atlantic coasts (>24 °C and >36 psu, respectively) (Molina-Schiller et al., Reference Molina-Schiller, Rosales and de Freitas2005). In some areas of the South Brazilian Bight, including the Rio de Janeiro coast, SACW are characterized by cold waters (<20 °C) and salinities ranging from 35 to 36 psu (Stramma and England, Reference Stramma and England1999; Brandini et al., Reference Brandini, Nogueira, Simião, Codina and Noernberg2014; Castro, Reference Castro2014), comprising oceanographic features previously associated with P. spinipinnis occurrences (Goodall et al., Reference Goodall, Würsig, Würsig, Harris and Norris1995a; Molina-Schiller et al., Reference Molina-Schiller, Rosales and de Freitas2005; Reyes, Reference Reyes, Würsig, Thewissen and Kovacs2018).
Despite no evidence of bycatch being found, a fourth, albeit remote, possibility is that both specimens were taken as bycatch further south and subsequently dumped at sea. Despite these hypotheses, P. spinipinnis is extremely rare in Brazilian waters. Analyses of stranding data spanning over 30 years of effort in Southern Brazil reported only one specimen in the state of Santa Catarina and six in the state of Rio Grande do Sul (Prado et al., Reference Prado, Mattos, Silva and Secchi2016; Vianna et al., Reference Vianna, Loch, Castilho, Gaidzinski, Cremer and Simões-Lopes2016). The report from Vianna et al. (Reference Vianna, Loch, Castilho, Gaidzinski, Cremer and Simões-Lopes2016) is the same specimen reported by Simões-Lopes and Ximenez (Reference Simões-Lopes and Ximenez1989), making it the only record for Santa Catarina state to date. It is noteworthy that both studies describe systematic efforts within their local stranding monitoring programmes, thereby enhancing their chances of encountering dead mammals washed ashore and underscoring the rarity of the species and the robustness of the analysed data.
The information presented here results from systematic cetacean stranding monitoring, which involves continuing engagement with the public. Through this engagement, local residents and visitors actively contribute by reporting stranding occurrences to the scientific community enhancing the effectiveness of the monitoring programme. While these occurrences of P. spinipinnis may be considered extralimital, we report the first record in the state of Rio de Janeiro, Southeast Brazil, and provide new biological information on the species along its northernmost distributional range on the South American Atlantic border. Although no evidence of allopatric dispersion was investigated, the occurrence of pubescent and mature male individuals in such a distant location from southern Brazil is noteworthy. Finally, the continuation of these stranding monitoring efforts should enable further investigation into the species’ biological aspects in case of future occurrences.
Data
The data supporting the conclusions of this article are partially available at Sistema de Informação de Monitoramento da Biota Aquática under ID 508609, and Mayorga et al. (Reference Mayorga, Vanstreels, Bhering, Mamede, Costa, Pinheiro, Reis, Trazzi, Meirelles, Ribeiro and Siciliano2020) as listed in the References.
Acknowledgements
We gratefully acknowledge the logistical support provided by Universidade do Estado do Rio de Janeiro and the Faculdade de Oceanografia. We extend our thanks to the teams at MAQUA/UERJ and Instituto ORCA for their field and necropsy assistance during this study. Additionally, we express our appreciation to the residents of Saquarema and Parati beaches for their contributions in reporting the stranding of specimens in the states of Rio de Janeiro and Espírito Santo. The authors would also like to thank the two anonymous reviewers, as well as colleagues Lis Bittencourt, Nara Oliveira-Ferreria and Róisín Jordan, for their contributions to the final version of the manuscript. We also extend our gratitude to Associate Editor Dr Jenna Riekkola for her thoughtful comments and contributions to improving this manuscript. Carcasses were collected under licenses ABIO 755-2016 and SISBio 64724-11.
Author contributions
Rafael Ramos Carvalho: Conceptualization, data curation, formal analysis, investigation, methodology, resources, supervision, validation, visualization, writing – original draft, writing – review and edit. Joana Ikeda: Data curation, investigation, formal analysis, methodology, validation, writing – review and edit. Yasmin Daoualibi: Data curation, investigation, formal analysis, methodology, validation, writing – review and edit. Emi B. Guari: Data curation, investigation, formal analysis, methodology, validation, writing – review and edit. Pedro Teixeira: Data curation, investigation, formal analysis, methodology, validation, writing – review and edit. Elitieri B. Santos-Neto: Data curation, investigation, methodology, formal analysis, resources, validation, writing – review and edit. José Lailson-Brito: Funding acquisition, conceptualization, data curation, methodology, resources, supervision, validation, visualization, writing – review and edit. Lupercio Barbosa: Data curation, investigation, resources, supervision, validation, visualization, writing – review and editing. Marcelo Ramos-Nogueira: Data curation, investigation, resources, supervision, validation, visualization, writing – review and editing. Alexandre F. Azevedo: Funding acquisition, conceptualization, data curation, methodology, resources, supervision, validation, visualization, writing – review and edit.
Financial support
This work was supported by the Projeto de Monitoramento de Praias da Bacia de Santos e Espírito Santo (PMP-BS/PMP-ES). PMP is a monitoring program required by Instituto Brasileiro do Meio Ambiente dos Recursos Renováveis (IBAMA) and conducted by Petrobras. The work was also financed by Associação Cultural e de Pesquisa Noel Rosa. The Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) have supported research developed by MAQUA/UERJ. AA has research grants from CNPq (PQ-1B 307458/ 2022-9), FAPERJ (CNE E-26/200.397/2023) and UERJ (Prociencia), and JL-B has research grants from CNPq (PQ-1D 315.276/2021-5), and UERJ (Prociencia).
Competing interests
The authors declare no conflicts of interests.
