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Evidencias de un ataque de orca a una cria de ballena franca austral en el sur de Brasil.

Evidences of attack of a killer whale on a calf southern right whale in Southern Brazil

The killer whale (Orcinus orca) is a large top predator that feeds on a variety of prey, including over 30 cetacean species worldwide (e. g., Jefferson et al., 1991; Ford and Reeves, 2008; Ford, 2009; Weller, 2009). The diet of killer whales varies greatly among populations, and prey specialization is usually one of the defining characteristics of the different ecotypes (e. g., Baird et al., 1992; Pitman and Ensor, 2003; Weller, 2009; De Bruyn et al., 2013). In Antarctic and subantarctic waters, for instance, five distinct ecotypes of killer whales (types A, B-big, B-small, C and D) have been proposed (Pitman and Ensor, 2003; Pitman et al., 2011). Whereas some morphotypes prey mainly on marine mammals (types A and B-big), others are suspected to have a diet based on penguins (type B-small) or fishes (type C and, probably, type D) (De Bruyn et al., 2013).

In South America, along the Patagonian coast of Peninsula Valdes, Argentina, killer whales prey mainly on South American sea lions (Otaria flavescens) and southern elephant seals (Mirounga leonina) (Thomas and Taber, 1984; Lopez and Lopez, 1985; Hoelzel 1991; Bastida et al., 2007), although attacks to southern right whales (Eubalaena australis) (Harris and Garcia, 1986; Jefferson et al., 1991; Sironi et al., 2008), dusky dolphins (Lagenorhynchus obscurus) and common dolphins (Delphinus delphis) have been reported (Coscarella et al., 2015).

For the Brazilian waters, the feeding habitats and distribution of killer whales are still poorly known and only two cetaceans have been reported as prey items of the species: the franciscana (Pontoporia blainvillei) (Ott and Danilewicz, 1998; Santos and Netto, 2005) and the Burmeister's porpoise (Phocoena spinipinnis) (Dalla Rosa, 1995).

Herein we report the first evidence of a killer whale attack on a southern right whale in Brazilian waters and present new records of O. orca in coastal waters of the southernmost region of Brazil. The original database include records of stranding southern right whales collected by a marine mammal research team (GEMARS--Grupo de Estudos de Mamiferos Aquaticos do Rio Grande do Sul) during regular beach surveys over 25 years (1991-2016) between Torres (29[degrees]19'S, 49[degrees]42'W) and the Lagoa do Peixe National Park (31[degrees]21'S, 51[degrees]02'W), in southern Brazil. Opportunistic sighting of killer whales south of the Cape of Santa Marta Grande (28[degrees]36'S, 48[degrees]49'W) have been made onboard fishing vessels or documented in video by recreational sailors from 2003 to early 2017. Additional sightings of killer whales in coastal waters from Cape of Santa Marta Grande to Chui River mouth (33[degrees]45'S, 53[degrees]22'W) were recorded during aerial surveys to estimate franciscana abundance in 2004 and 2014 (see Danilewicz et al., 2010). For every killer whale sighting, information regarding date, location and number of individuals were recorded.

On 24 July 2008, a newborn southern right whale was found dead (GEMARS 1304) at Balneario Quintao (30[degrees]19'S, 50[degrees]16'W), on the northern coast of Rio Grande do Sul (RS). The female calf (Fig. 1), with 595 cm of total length, still had vestiges of the umbilical cord. The specimen presented several tooth marks on both dorsal and ventral surfaces of the right pectoral fin (Fig. 2A) and on the left fluke margin (Fig. 2B). Separation of the rake marks ranged from 3.0 to 3.5 cm, which is characteristic of an adult killer whale (Scheffer, 1969). The marks were also very similar to those reported in a southern right whale calf found dead on Golfo San Jose, Argentina, following an attack by adult killer whales (Harris and Garcia, 1986).

Killer whales use a variety of hunting strategies to debilitate and kill their preys. Attacking killer whales are known, for instance, to grasp large whales by the flukes and pectoral flippers in an attempt to slow or stop their movement, or even drown their prey by pulling them underwater (Silber et al., 1990; Barrett-Lennard et al., 2011). Therefore, considering that grasping and dragging its prey is a common behavior of killer whales and previous attacks on southern right whales are known (Harris and Garcia, 1986; Jefferson et al., 1991; Sironi et al., 2008), it seems reasonable to assume that the marks found on the calf reported here were produced when the whale was still alive.

Southern right whales migrate to southern Brazil during winter and spring for breeding and calving (Groch et al., 2005; Danilewicz et al., 2016). The main aggregation areas roughly extend from 27oS to 30oS of latitude. Mother and calve pairs occur usually in waters close to the shore (< 10 m deep), with peak abundance between August and October (Groch et al., 2005; Danilewicz et al., 2016). Killer whales, on the other hand, have been reported in southern Brazil throughout the year, usually near the shelf break and the continental slope, in waters depth ranging from 110 to 3500 m (Castello and Pinedo, 1986; Pinedo et al., 2002; Dalla Rosa and Secchi, 2007; Passadore et al., 2015; Di Tullio et al., 2016). Nevertheless, as reported here, in a few occasions killer whales have also been sighted close to shore, mainly during the summer (December through February) (Table 1). The finding of the remains of three franciscana specimens, a dolphin species that inhabit waters mainly up to 30 m (Danilewicz et al., 2009), in the stomach of a killer whale found dead in northern coast of RS on December 19th, 1993 (Ott and Danilewicz, 1998) is also noteworthy.

Therefore, although both killer whales and southern right whales occur in southern Brazil, their spatial and temporal distributions seem to be quite different, reducing the probability of encounters. In fact, we provide the first evidence of predator-prey interaction between these species in the region. From a total of 19 southern right whales found dead during 25 years in the study area, there is no other record of this ecological interaction. Nevertheless, there are several documented records of attacks or harassments of killer whales on southern right whales in the calving and nursing grounds in Argentina and South Africa (e. g., Jefferson et al., 1991; Sironi et al., 2008), although they do not seem to be a regular food source of killer whales (Bastida et al., 2007; Best et al., 2010; Coscarella et al., 2015).

At the present, scarce information is available about the stock discreteness and foraging habits of killer whales in Brazilian waters. Based on sighting data, including the long movements of a photo-identified adult male, it has been suggested that killer whales in southeastern Brazil present a similar behavior to the "transient" killer whales of the northeastern Pacific (Siciliano et al., 1999; Santos and Silva, 2009). These "transient" killer whales form small groups that prey on marine mammals and have an unpredictable occurrence in coastal waters (Ford, 2009). The killer whale sightings in southern Brazil (Table 1) as well as the prey-interaction described here seem also to fit in this foraging behavior. Nevertheless, considering the scarcity of information on killer whales from Brazilian waters and the great behavioral flexibility of the species in a global scale (De Bruyn et al., 2013), it seems premature to classify the killer whales of this region in any specific ecotype.

Despite this uncertainty, the migratory movements of three adult female killer whales identified as the type B and tagged in Antarctic were recorded in offshore waters of RS (around 30oS) (Durban and Pitman, 2011). In addition, a recent molecular study assigned one of the killer whales stranded on the southern coast of RS (around 32oS) to type C with high probability (Morin et al., 2015). Therefore, it seems that more than one stock of killer whales could inhabit the waters of southern Brazil, as suspected by other authors (Dalla Rosa, 1995; Passadore et al., 2015).

In conclusion, although killer whales seem to have primarily an oceanic distribution in southern Brazil and feed mainly on large fishes near the continental slope (Secchi and Vaske Jr., 1998; Dalla Rosa and Secchi, 2007; Passadore et al., 2015), the species, or at least some of the existent stocks, can also eventually search and prey upon coastal whales and dolphins in the region.

Recibido 13 febrero 2017. Aceptado 31 marzo 2017. Editor asociado: R Bastida

Acknowledgments. The authors would like to thank all colleagues and volunteers that collaborated with GEMARS over the years, in special Sandra Krieger, Jonathas Barreto and Roberto Rosa for help to collect the data on the southern right whale calf. We are also grateful to the UERGS, CECLIMAR/IB/UFRGS and MORG-FURG for the logistical support. Andre Barreto and Marta Cremer allowed us to use unpublished data. Alexandre Azevedo, Artur Andriolo, Emanuel Ferreira and Pablo Denuncio participated of the franciscana aerial surveys. We are also in debt with Julian Lemos and Vanessa Andrade for the information and video on the sighting of killer whales at Balneario Rincao. Finally, we would like to thank Ricardo Bastida and an anonymous reviewer, which contributed to improving the quality of the publication. This work was supported through grants from CNPq (#572180/2008-0), FMNA and Programa Petrobras Ambiental. The Research Group ECOA/CNPq contributed to this study.

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Paulo H. Ott (1,2), Federico Sucunza (2,3,4), Janaina Wickert (2,5,6), Daniel Danilewicz (2,3,7), and Mauricio Tavares (5,6)

(1) Universidade Estadual do Rio Grande do Sul (UERGS), Unidade do Litoral Norte, Osorio, RS, Brazil. [Correspondence: Paulo Henrique Ott <paulo.henrique.ott@gmail.com >].

(2) Grupo de Estudos de Mamiferos Aquaticos do Rio Grande do Sul (GEMARS), Torres, RS, Brazil.

(3) Instituto Aqualie, Juiz de Fora, MG, Brazil.

(4) Programa de Pos-Graduacao em Ecologia, Universidade Federal de Juiz de Fora (UFJF), Juiz de Fora, MG, Brazil.

(5) Programa de Pos-Graduacao em Biologia Animal, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil.

(6) Centro de Estudos Costeiros, Limnologicos e Marinhos do Instituto de Biociencias da Universidade Federal do Rio Grande do Sul (CECLIMAR/IB/UFRGS), Imbe, RS, Brazil.

(7) Programa de Pos-Graduacao em Zoologia, Universidade Estadual de Santa Cruz (UESC), Ilheus, BA, Brazil.

Caption: Fig. 1. Southern right whale (Eubalaena australis) calf found dead (GEMARS 1304) on the northern coast of Rio Grande do Sul, southern Brazil, with evidences of attack by a killer whale (Orcinus orca).

Caption: Fig. 2. Detail of the tooth rakes (white arrows) of a killer whale (Orcinus orca) on the right pectoral fin (A), and left fluke margin (B), of the southern right whale (Eubalaena australis) calf found dead (GEMARS 1304) on the northern coast of Rio Grande do Sul, southern Brazil. Ruler in (A) is 20 cm long. A few whale-lice (Cyamus sp.) are also visible in (B).
Table 1 Sightings of killer whales (Orcinus orca) in inshore
waters of southern Brazil, between the Cape of Santa Marta
Grande (28[degrees]36'S) and Chui river mouth (33[degrees]45'S).
SC = Santa Catarina. RS = Rio Grande do Sul.

Date          Location                  Distance    Depth
                                       from shore    (m)
                                          (km)

28 Dec 1978   Rio Grande, RS             110/18     25/21
                (32[degrees]16'S,
                51[degrees]58'W)
21 Jul 1997   Cape of Santa Marta,        32.4       63
                SC (28[degrees]41'S,
                48[degrees]39'W)
30 Jan 2003   Balneario Pinhal,            1        < 10
                RS (30[degrees]14'S,
                50[degrees]13'W)
16 Jan 2004   Passo de Torres,             2         10
                SC (29[degrees]19'S,
                49[degrees]41'W)
24 Feb 2004   Rio Grande, RS               24        16
                (32[degrees]52'S,
                52[degrees]14'W)
23 Jan 2014   Santa Vitoria do             44        30
                Palmar, RS
                (33[degrees]25'S,
                52[degrees]17'W)
26 Jan 2017   Balneario Rincao, SC        3.8        30
                (28[degrees]50'S,
                49[degrees]10'W)

Date               Group            Source
                Composition

28 Dec 1978   2 adults,          Castello and
                1subadult,         Pinedo
                1juvenile          (1986) (a)
21 Jul 1997   1 individual       Pinedo
                                   et al.
                                   (2002) (b)
30 Jan 2003   1 adult male       This study

16 Jan 2004   Mother-calf pair   This study

24 Feb 2004   2 individuals      This study

23 Jan 2014   1 individual       This study

26 Jan 2017   6-8 individuals,   This study
                including one
                adult male

(a) Castello and Pinedo (1986) cited this sighting as 110 km from
the coast and 25 m depth. However, based on the coordinates
presented, the corresponding locality is about 18 km from the coast
and 21 m depth. (b) Detailed location provided by A. Barreto (pers.
comm.).
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Author:Ott, Paulo H.; Sucunza, Federico; Wickert, Janaina; Danilewicz, Daniel; Tavares, Mauricio
Publication:Mastozoologia Neotropical
Date:Jun 1, 2017
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