- Marine Record
- Open Access
Anthropogenic impact on a pregnant Cuvier’s beaked whale (Ziphius cavirostris) stranded in Brazil
Marine Biodiversity Records volume 9, Article number: 30 (2016)
Because of their usually cryptic behaviour, most knowledge on the biology of beaked whales are from records of stranded animals. Although the Cuvier’s beaked whale (Ziphius cavirostris) is the best known species of the ziphiidae family, little information on its reproduction is available.
Here we report on the stranding of a dead pregnant female with clear signs of anthropogenic impact, including the presence of a fishing artefact in the stomach.
The region of the stranding (north-eastern coast of Brazil) is an area of increasing interest for oil and gas exploitation. Conservation concerns may arise from findings such as the one presented and discussed here.
Among all living ziphiids, the Cuvier’s beaked whale Ziphius cavirostris (Cuvier, 1823) is the best known species, with a cosmopolitan distribution (Heyning, 1989; Reeves et al., 2002), having been recorded in offshore waters of all major oceans except in polar regions (Bastida et al., 2007). Although studies on diving and acoustic behaviour with successful tag deployment have significantly improved knowledge on their biology (Baird et al., 2006; Tyack et al., 2006; Schorr et al., 2014; DeRuiter et al., 2013), most information available still comes from the examination of stranded individuals (McLeod et al., 2006). That happens because their oceanic habitat and cryptic surface behaviour (Baird et al., 2006) pose difficulties for the study of the species in the wild (Schorr et al., 2014). In a recent synthesis presented to the International Whaling Commission, Wojtek and Norman (2013) found that Z. cavirostris accounted for one third of the beaked whale stranding records around the world. Although most stranded calves considered in the study occurred along March–September, the majority of records mentioned were for the Northern Hemisphere, and little information on the species’ reproduction is currently available in the literature.
In Brazil, both sighting and stranding records of Cuvier’s beaked whale have been reported (Carvalho, 1969; Carvalho, 1975; Zanelatto et al., 1995; Pinedo et al., 2001; Batista et al., 2012; Caon et al., 2009; Meirelles et al., 2009; Ott et al., 2009; Mayorga et al., 2010) and its occurrence in the area is not as rare as previously thought (Batista et al., 2012). The presence of foetus was reported only twice for individuals stranded on the Brazilian coast, in São Paulo and Paraíba States (Carvalho, 1975; Pinedo et al., 2001). The present work reports an unusual stranding of a pregnant Cuvier’s beaked whale in Brazil, being the first to present clear signs of impact from anthropogenic activities for the north-eastern region of the country.
Methods and results
On 25 January 2010, a dead Cuvier’s beaked whale was found stranded at Ipitanga beach (12.9°S, 38.3°W), municipality of Lauro de Freitas. The stranding site is close to the capital city of Bahia state, Salvador, north-eastern Brazil (Fig. 1). The fresh carcass of the 5.5 m (total length) female (Fig. 2) was transported to the Instituto Mamíferos Aquáticos (IMA) where a necropsy was conducted.
During the gross examination, unidentified parasite cysts were found in the blubber. Fibrosis associated with encapsulated helminths in the tissue of the lungs was also observed. Stomach chambers (Mead, 2007) contents were examined, which included a considerable piece of fishing net obstructing the passage from the oesophagus to the main stomach. Small amount of hard remains of prey (i.e. cephalopod beaks and fish otoliths) were present mainly in the pyloric chamber, but no signs of recent feeding (i.e. prey flesh) were apparent inside any portion of the digestive tract. The whale was carrying a 221.3 cm foetus (total length) in advanced stage of development (Fig. 3). Parasites, stomach contents, bones and tissue samples were collected and preserved for future analyses. The adult and foetus are deposited in the IMA’s biological collection, under numbers CCPM#0425 and CCPM#0426, respectively. Besides the fibrosis and parasites in the lungs, the piece of fishing net in the stomach and parasite cysts in the blubber, nothing worthy of note was found during the necropsy.
Ziphius cavirostris are rarely found near the shore except close to submarine canyons, around islands and where the continental shelf is very narrow (Heyning & Mead, 2009). This latter feature is exactly what happens to the region of the present stranding, where the Brazilian continental shelf is at its narrowest (Knoppers et al., 1999) with deep waters being relatively close to the shore (Fig. 1). The area is very close to Baía de Todos os Santos (BTS), a bay with calm waters where there is a high level of large ship traffic, entering and leaving several ports every day. Between 2000 and 2014, an average of 1374 ships per year have arrived at the two largest ports in the BTS (CODEBA, 2014). In addition to large ship traffic the BTS also present a high level of tour boats traffic, and a catamaran boat has already been reported to strike an unidentified large whale near Itaparica Island (Talento 2005), along one of the several touristic routes in the bay. Ship strikes causing lethal wounds in whales are recognized as important threats to cetaceans (e.g. Laist et al., 2001; Jensen & Silber, 2004; Dolman et al. 2006; Bezamat et al., 2014), and there are at least 256 documented collisions between whales/dolphins and vessels for the Southern Hemisphere (Waerebeek et al., 2007). Also, the coast of Bahia is a region of great interest to the oil and gas industry and exploration activities are about to expand in the near future (Milani et al., 2000; Suguio & Martin, 2013), which imply in an increase in both large ship traffic and oceanic noise. Whether these pose significant threats to Cuvier's beaked whales in the area, is something yet to be determined.
It was not possible to determine precisely the original use of the present piece of fishing net, but its characteristics point it could had been part of a trawling-net. Marine debris, particularly plastic, have been reported in the stomach contents of Z. cavirostris (e.g. Walker & Coe, 1990; Podestà & Meotti 1991; Poncelet et al., 2000; Allen et al. 2011). In the whale reported here, the obstruction caused by the fishing artefact in the digestive tract must have resulted in the inability of this animal to feed. In addition, the bronchial fibrosis probably compromised normal breathing, as respiratory parasites are already known to have affected the health of cetaceans in the North Sea and Eastern Pacific and Atlantic Oceans (Baker, 1992; Cornaglia et al., 2000; Parsons & Jefferson, 2000; Fauquier et al., 2009). Summed to all that, a higher metabolic demand, which mammals present during pregnancy (Schillo, 2009), should have aggravated the pathological condition of the animal. In this sense, it is very reasonable to assume that the ingestion of the piece of fishing net by the animal probably caused its death.
Even though Cuvier’s beaked whale is currently considered as a species of “Least Concern” by the International Union for Conservation of Nature (IUCN), it presents “Insufficient Data” status at the national Brazilian evaluation. Therefore all new information for the area, either regarding stranded or sighted animals, is extremely important, so as the pregnancy reported here. However, although the total length of the present foetus represents approximately 80 % of the estimate length at birth for this species (Heyning & Mead, 2009; Reidenberg & Laitman, 2009), more information is needed before we can determine if the area could be a potential breeding/nursing ground. This report highlights the need to adopt regional guidelines to reduce the risk of impact on marine mammals by human activities, like the effective implementation of law 117/96 from the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA 2014). It is also strongly advisable that educational and informative actions that help preventing the marine pollution are adopted, so threats from marine debris can be minimized.
Allen BM, Brownell RL, Mead JG Species review of Cuvier’s beaked whale, Ziphius cavirostris (report SC/63/SM17). In: Scientific Committee Documents. International Whaling Commission. 2011. https://swfsc.noaa.gov/publications/CR/2011/2011Allen2.pdf. Accessed 25 Apr 2016.
Baird RW, Webster DL, McSweeney DJ, Ligon AD, Schorr GS, Barlow J. Diving behaviour of Cuvier’s (Ziphius cavirostris) and Blainville’s (Mesoplodon densirostris) beaked whales in Hawai’i. Can J Zool. 2006;84:1120–28.
Baker JR. Causes of mortality and parasites and incidental lesions in dolphins and whales from British waters. Vet Rec. 1992;130:569–72.
Bastida R, Rodríguez D, Secchi ER, Silva VMF. Mamíferos acuáticos de Sudamérica y Antártida. Buenos Aires: Vázquez Mazzini Editores; 2007.
Batista RLG, Schiavetti A, Santos UAD, Reis MSS. Cetaceans registered on the coast of Ilhéus, Bahia, north-eastern Brazil. Biota Neotrop. 2012;12:31–8.
Bezamat C, Wedekin L, Simões-Lopes PC. Potential ship strikes and density of humpback whale in the Abrolhos Bank breeding ground, Brazil. Aquat Conserv. 2014. doi:10.1002/aqc.2523.
Caon G, Moreira MB, Hoffmann LS, Ditullio J, Valdez FP, Fruet P, et al. Os mamíferos marinhos. In: Viana DL, Hazin FHV, Souza MAC, editors. O arquipélago de São Pedro e São Paulo: 10 anos de estação científica. Brasília: SECIRM; 2009. p. 278–85.
Carvalho JP. Sobre a provável ocorrência de “Baleia de Cuvier” no litoral de São Paulo. Revista Nacional de Pesca. 1969;10:8–11.
Carvalho CT. Ocorrências de mamíferos marinhos no litoral do Brasil. Boletim Técnico do Instituto Florestal, São Paulo. 1975;16:13–32.
CODEBA. Companhia das docas do estado da Bahia, autoridade portuária. Available from: http://www.codeba.com.br. Accessed 31 Oct 2014.
Cornaglia E, Rebora L, Gili C, Di Guardo G. Histopathological and immunohistochemical studies on cetaceans found stranded on the coast of Italy between 1990 and 1997. J Vet Med A Physiol Pathol Clin Med. 2000;47:129–42.
Cuvier G. Recherches sur les ossemens fossiles. Paris: G. Dufour et E. d’Ocagne; 1823.
DeRuiter SL, Southall BL, Calambokidis J, Zimmer WM, Sadykova D, Falcone EA, et al. First direct measurements of behavioural responses by Cuvier's beaked whales to mid-frequency active sonar. Biol Lett. 2013. doi:10.1098/rsbl.2013.0223.
Dolman S, Williams-Grey V, Asmutis-Silva R, Isaac S. Vessel collision and cetaceans: what happens when they don’t miss the boat. In: Reports and Publications. Whale and Dolphin Conservation. 2006. http://uk.whales.org/sites/default/files/whales-and-ship-strikes.pdf. Accessed 25 Apr 2016.
Fauquier DA, Kinsel MJ, Dailey MD, Sutton GE, Stolen MK, Wells RS, et al. Prevalence and pathology of lungworm infection in bottlenose dolphins Tursiops truncatus from southwest Florida. Dis Aquat Organ. 2009;88:85–90.
Heyning JE. Cuvier’s beaked whale Ziphius cavirostris G. Cuvier, 1823. In: Ridgway SH, Harrison RJ, editors. Handbook of Marine Mammals, volume 4: River dolphins and the larger toothed whales. London: Academic; 1989. p. 289–308.
Heyning JE, Mead JG. Cuvier’s beaked whale (Ziphius cavirostris). In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. 2nd ed. San Diego: Academic; 2009. p. 294–6.
IBAMA. Portaria IBAMA N° 117, de 26 de Dezembro de 1996. http://www.icmbio.gov.br/cepsul/images/stories/legislacao/Portaria/1996/p_ibama_117_1996_protecaocetaceos_alterada_p_ibama_24_2002.pdf. Accessed 31 Oct 2014.
Jensen AS, Silber GK. Large whale ship strike database. In: OPR Tech Memos. National Oceanic and Atmospheric Administration. 2004. http://www.nmfs.noaa.gov/pr/pdfs/shipstrike/lwssdata.pdf. Accessed 25 Apr 2016.
Knoppers B, Ekau W, Figueiredo AG. The coast and shelf of east and northeast Brazil and material transport. Geo-Mar Lett. 1999;19:171–8.
Laist DW, Knowlton AR, Mead JG, Collet AS, Podesta M. Collisions between ships and whales. Mar Mam Sci. 2001;17:35–75.
MacLeod CD, Perrin WF, Pitman R, Barlow J, Ballance L, D’Amico A, et al. Known and inferred distributions of beaked whale species (Cetacea: Ziphiidae). J Cetac Res Manage. 2006;7:271–86.
Mayorga LFSP, Barbosa LA, Bhering RCC. Primeiros registros de encalhe de Ziphius cavirostris (Cetacea, Odontoceti) na costa do Espírito Santo, Brasil. Biotemas. 2010;23:223–6.
Mead JG. Stomach anatomy and use in defining systemic relationships of the cetacean family ziphiidae (beaked whales). Anat Rec. 2007;290:581–95.
Meirelles ACO, Monteiro-Neto C, Martin AMA, Costa AF, Barros HMDR, Alves MDO. Cetacean strandings on the coast of Ceará, North-Eastern Brazil (1992-2005). J Mar Biol Assoc UK. 2009;89:1–8.
Milani EJ, Brandão JASL, Zalán PV, Gamboa LAP. Petróleo na margem continental Brasileira: Geologia, exploração, resultados e perspectivas. Rev Bras Geof. 2000;18:351–96.
Ott PH, Tavares M, Moreno IB, Oliveira LR, Danilewicz D. Os cetáceos do arquipélago de São Pedro e São Paulo, Brasil. In: Mohr LV, Castro JWA, Costa PMS, Alves JV, editors. Ilhas oceânicas Brasileiras: Da pesquisa ao manejo. Brasília: SECIRM; 2009. p. 284–300.
Parsons ECM, Jefferson TA. Post-mortem investigations on stranded dolphins and porpoises from Hong Kong waters. J Wildl Dis. 2000;36:342–56.
Pinedo MC, Lammardo MP, Barreto AS. Review of Ziphius cavirostris, Mesoplodon grayi and Lagenodelphis hosei (Cetacea: Ziphiidae and Delphinidae) in Brazilian waters, with new records from southern Brazil. Atlantica. 2001;23:67–76.
Podestà M, Meotti C. The stomach contents of a Cuvier’s beaked whale Ziphius cavirostris, and a Risso’s dolphin Grampus griseus, stranded in Italy. Eur Res Cetaceans. 1991;5:58–61.
Poncelet E, Van Canneyt O, Boubert JJ. Considerable amount of plastic debris in the stomach of a Cuvier’s beaked whale (Ziphius cavirostris) washed ashore on the French Atlantic coast. Eur Res Cetaceans. 2000;14:44–7.
Reeves RR, Stewart BS, Clapham PJ, Powell JA. National Audubon Society guide to marine mammals of the world. New York: Knopf; 2002.
Reidenberg JS, Laitman JT. Cetacean prenatal development. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. 2nd ed. San Diego: Academic; 2009. p. 220–30.
Schillo KK. The reproductive physiology of mammals: From farm to field and beyond. New York: Delmar Publishers; 2009.
Schorr GS, Falcone EA, Moretti DJ, Andrews RD. First long-term behavioral records from Cuvier’s beaked whales (Ziphius cavirostris) reveal record-breaking dives. PLoS ONE. 2014. doi:10.1371/journal.pone.0092633.
Suguio K, Martin L. The role of neotectonics in the evolution of the Brazilian coast. Geonomos. 2013;4:45–53.
Talento B. Baleia se choca em catamarã no mar da Bahia. In: O Estadão Online. 2005. http://noticias.ambientebrasil.com.br/clipping/2005/08/01/20266-baleia-se-choca-em-catamara-no-mar-da-bahia.html. Accessed 31 Oct 2014.
Tyack PL, Johnson M, Soto NA, Sturlese A, Madsen PT. Extreme diving of beaked whales. J Exp Biol. 2006;209:4238–53.
Waerebeek KV, Baker AN, Félix F, Gedamke J, Iñiguez M, Sanino GP, et al. Vessel collisions with small cetaceans worldwide and with large whales in the Southern Hemisphere, an initial assessment. Lajam. 2007;6:43–69.
Walker WA, Coe JM. Survey of marine debris ingestion by odontocete cetaceans. In: Shomura RS, Godfrey ML, editors. Proceedings of the Second International Conference on Marine Debris, Hawaii, volume 1. US Dept. of Commerce. NOAA Tech. Memo. NMFS, NOAA-TM-NMFS-SWFSC-154. 1990;2:747-74.
Wojtek B, Norman S A. Ziphius cavirostris strandings: a short review (report SC/65a/SM01). In: Scientific Committee Documents. International Whaling Commission. 2013. https://archive.iwc.int/pages/view.php?ref=4708&search=wojtek&offset=0&order_by=relevance&sort=DESC&archive=0&k=&restypes=1,2,3,4. Accessed 25 Apr 2016.
Zanelatto RC, Bittencourt ML, Corrêa MFM, Domit LG. Ziphius cavirostris Cuvier, 1823 (Cetacea, Ziphiidae) on the Brazilian coast, with notes on biometry. Iheringia, Sér Zool. 1995;79:141–7.
The authors thank Luiz Boaventura and all the team of the Instituto Mamíferos Aquáticos (IMA) for their help during necropsy procedures. IMA also provided materials and logistical help for the procedures. The municipality of Lauro de Freitas provided the transportation of the carcass to the necropsy site. Three anonymous reviewers made important contributions to the final version of this manuscript.
Availability of supporting data
The dataset supporting the conclusions of this article is included within the article as photographs.
GAB, LRAS and PRBF conducted the necropsy, took photographs and collected samples. GAB, IOBM, MSSR, LRAS and PRBF wrote the manuscript together. All authors have read and approved the final version of the manuscript.
GAB and PRBF have degrees in veterinary medicine.
The authors declare that they have no competing interests.
Ethics approval and consent to participate
This study was part of the routine work of the Instituto Mamíferos Aquáticos (Projeto MAMA). The institution is member of the Aquatic Mammals Stranding Network of North-eastern Brazil (REMANE), implemented by the Brazilian Institute of Environment and Renewable Natural Resources in 2000 (IBAMA; ordinance n. 39, of 28 June 2000).