INTRODUCTION
Stranded cetaceans have been an important source of information on the species distribution over time and they have also been the main way to obtain samples used for natural history and conservation studies of these species. Technological advances have led to the use of other sampling methods and new field studies have been developed, such as acoustic, satellite tracking or diving behaviour, but strandings can be a good approach for local species diversity and distribution studies (Pyenson, Reference Pyenson2011) and above all for little-known species, such as the family Ziphiidae (MacLeod et al., Reference MacLeod, Perrin, Pitman, Barlow, Ballance, D'Amico, Gerrodette, Joyce, Mullin, Palka and Waring2006). Beaked whales are medium-sized cetaceans, all live in open oceans and feed on deep-water squid and fish (Mead, Reference Mead, Perrin, Würsig and Thewissen2009). As extreme divers, the Cuvier's beaked whale Ziphius cavirostris (Cuvier, 1823) has the mammalian dive record of 2992 m and 137.5 min (Schorr et al., Reference Schorr, Falcone, Moretti and Andrews2014). The family has a wide-ranging distribution around the world, from both ice edges to the equator, but knowledge of the 21 recognized species of beaked whales varies greatly due to the limited information about some of them (Dalebout et al., Reference Dalebout, Baker, Mead, Cockcroft and Yamada2004; MacLeod et al., Reference MacLeod, Perrin, Pitman, Barlow, Ballance, D'Amico, Gerrodette, Joyce, Mullin, Palka and Waring2006). Cuvier's beaked whale is the most widely distributed beaked whale species in the Atlantic (Ross, Reference Ross1984; MacLeod et al., Reference MacLeod, Pierce and Santos2004, Reference MacLeod, Perrin, Pitman, Barlow, Ballance, D'Amico, Gerrodette, Joyce, Mullin, Palka and Waring2006; Otley et al., Reference Otley, Smith and Dalebout2012; Bachara & Norman, Reference Bachara and Norman2013); together with the Sowerby's beaked whale Mesoplodon bidens (Sowerby, 1804), the Blainville's beaked whale Mesoplodon densirostris (Blainville, 1817), the Gervais’ beaked whale Mesoplodon europaeus (Gervais, 1855) and True's beaked whale Mesoplodon mirus (True, 1913) they have a regular occurrence in the North Atlantic and therefore they have a potential distribution in the studied area (MacLeod, Reference MacLeod2000; Pitman, Reference Pitman, Perrin, Würsig and Thewissen2009).
In Galicia (NW Spain) stranded cetaceans, seals and sea turtles are found each year (López et al., Reference López, Santos, Pierce, González, Valeiras and Guerra2002, Reference López, Covelo, Valeiras, Martínez-Cedeira, Alonso and Díaz2014). The most frequent families of cetaceans are Delphinidae, Phocoenidae, Balaenopteridae and Physeteridae, although less frequent individuals of Kogiidae and Ziphiidae are also found – they are classified as rare species because they represent less than 1% of total stranding records (López, Reference López2003). Only three individuals of the family Ziphiidae have been reported in the literature before 1990 for this area, all of them Cuvier's beaked whales (Penas-Patiño & Piñeiro, Reference Penas-Patiño and Piñeiro1989). Nevertheless, the skull of one of them located in a beach in Fisterra in 1983 and conserved in the Osteological Collection of the Marine Mammal Section of the Sociedade Galega de Historia Natural (MA0285A01) in Ferrol (Spain) has been identified as a Sowerby's beaked whale (I. Miján and J. I. Díaz, personal communication). Three other Cuvier's beaked whales stranded in 1990, 1991 and 1995 have been reported in two diet studies (González et al., Reference González, López, Guerra and Barreiro1994; Santos et al., Reference Santos, Pierce, Herman, Lopez, Guerra, Mente and Clarke2001a) and one more stranded in 1998 was cited by Covelo & Martínez (Reference Covelo and Martínez2001).
The aim of this work is: (i) to analyse the strandings from 1990 to 2013 in order to know the Ziphiidae species that have been registered in the area and their frequency, and (ii) evaluate the seasonal and geographic patterns of occurrence of the strandings.
MATERIALS AND METHODS
Study area
Galicia is an autonomous region located in NW Spain (Figure 1), with a coastline of 1195 km from 41°52′N 008°52′W to 43°33′N 007°02′W at the north-east Atlantic Ocean. This area has the influence of winds from south and south-west in autumn and winter, but in spring and summer it changes because of the northward displacement of the Os Açores High that promotes northerly winds, inducing a high primary productivity due to the coastal upwelling process, that typically occurs between March and September (Fraga, Reference Fraga1981; Ríos et al., Reference Ríos, Pérez and Fraga1992; Figueiras et al., Reference Figueiras, Labarta and Fernández2002), although some upwelling events have been reported for autumn and winter (Álvarez et al., Reference Álvarez, Prego, deCastro and Varela2012).
Beaked whales stranded in the coast of Galicia between 1990 and 2013.
Data collection and analysis
A stranding network was established in Galicia in 1990 and carried out by NGO Coordinadora para o Estudo dos Mamíferos Mariños (CEMMA), in order to locate stranded cetaceans, pinnipeds and sea turtles, ensuring the biological samples collection and the rehabilitation actions for live animals. Basic data recorded includes species, location, biometrics, sex identification, body condition and external examination for each animal. Photographs were also obtained. Necropsies were carried out on fresh and moderate decomposed animals. Both external studies and necropsies followed standardized protocols (Kuiken & García, Reference Kuiken and García1991; Geraci & Lounsbury, Reference Geraci and Lounsbury1993; SEC, 1999). In order to compare and evaluate spatial patterns along the Galician coast, the coastline was divided in three areas of similar length for the data analysis (Figure 1): North coast (from Eo River estuary to Mugardos), North-west coast (from Ares to Punta Couso (Ribeira)), and South coast (from Punta Couso (Ribeira) to Miño River estuary). Due to the reduced number of individuals data were grouped by season to study seasonal patterns into winter (January–March), spring (April–June), summer (July–September) and autumn (October–December). Chi-squared tests were used to study two hypotheses, that strandings do not differ between (i) the three areas and (ii) the four seasons along the year. To study the possible pattern of changes over time, the analysis was carried out for the whole dataset (from 1990 to 2013) and between two time periods: 1990–2002 and 2003–2013.
RESULTS
Between 1990 and 2013 a total of 4646 stranded cetaceans were recorded by the Galician stranding network. Of them, 21 (0.45%) belonged to the Ziphiidae family: 15 Cuvier's beaked whales, two Sowerby's beaked whales, one Blainville beaked whale, one True's beaked whale and two unidentified animals, Table 1, Figure 1. Ten animals were found at the North area, six at the Northwest area and five at the South area. The Cuvier's beaked whale found in Vares on 1 October 1998 is not considered for monthly analysis as the skull was recovered by fishermen from the bottom of the sea, so the real stranding date is unknown. The number of strandings was higher in October, February, March and April, and there were no records for any species in the summer season (July–September) (Figure 2). None of the animals had signs of interaction with fishing gear or bycatch.
Monthly distribution of the beaked whales strandings in the coast of Galicia between 1990 and 2013. Black: all the species (N = 20). Grey: Cuvier's beaked whale (N = 14).
Beaked whales stranded in the coast of Galicia between 1990 and 2013.
M: male. F: female. I: indeterminate sex. (−) means that the length is incomplete due to amputation or decomposition of the body.
Cuvier's beaked whale
Of the 15 individuals reported (71.4% of the Ziphiidae), five were males between 510 and 572 cm, six were females between 450 and 650 cm and the sex could not be determined for four individuals. Nine individuals were found in the North area, three in the North-west area and other three in the South area (Figure 1), but the distribution did not differ significantly between the areas (χ2 = 4.80, d.f. = 2, P = 0.090). The months with more strandings were February and April, with no records between July and September (Figure 2). When strandings are grouped by season, differences were found to be not statistically significant (χ2 = 6.00, d.f. = 3, P = 0.112). In contrast, if records are grouped into two time periods (1990–2002 and 2003–2013) to study geographic or seasonal pattern changes over time, the geographic distributions differ significantly (χ2 = 8.76, d.f. = 2, P = 0.013) and they also differed significantly depending on the season (χ2 = 10.80, d.f. = 3, P = 0.013). Between 1990 and 2002 strandings were recorded only in autumn and winter, and located along the three areas with similar values. Between 2003 and 2013 most of them were registered in spring and all of them in the North area (Figure 3).
Cuvier's beaked whales strandings by (A) geographic (N = 15) and (B) seasonal distribution (N = 14). Black: 1990–2002. Grey: 2003–2013.
Sowerby's beaked whale
Only two individuals of this species were found (9.5% of the Ziphiidae): a male of 425 cm located in the North-west coast, and a female of 364 cm located in the South coast (Figure 1), both of them in the autumn period. The male complete skeleton was stored in the Osteological Collection of the Marine Mammal Section of the Sociedade Galega de Historia Natural, Ferrol (MA1004E00). With only two animals it is not possible to analyse seasonal and geographic patterns with statistical significance.
True's beaked whale
Only one individual was found (4.8% of the Ziphiidae): a female of 497 cm located in the North-west coast (Figure 1) in the autumn period. The skull was stored in the Osteological Collection of the Marine Mammal Section of the Sociedade Galega de Historia Natural, Ferrol (MA0157E01).
Blainville's beaked whale
Just one individual was recorded (4.8% of the Ziphiidae): a male of 436 cm located in the North-west coast (Figure 1) in the winter period. The complete skeleton was stored in the Osteological Collection of the Marine Mammal Section of the Sociedade Galega de Historia Natural, Ferrol (MA0158E00).
DISCUSSION
The low number of strandings of individuals of the family Ziphiidae during the last 24 years confirm the sporadic presence of the species in Galicia that were reflected in previous reviews (Penas-Patiño & Piñeiro, Reference Penas-Patiño and Piñeiro1989; López, Reference López2003). It has to be considered that the present work focuses on stranded animals, and therefore only the presence of the species can be studied. Different experiences carried out with offshore tagged dead dolphins proved that the stranding rate of the floating carcasses varied widely: 0% in South-west England (de Boer et al., Reference de Boer, Saulino, Leopold, Reijnders and Simmonds2012), 8.0% in the Atlantic French coast (Peltier et al., Reference Peltier, Dabin, Daniel, Van Canneyt, Dorémus, Huon and Ridoux2012) and 26.7% in the Galician coast with drifts between 27 and 320 km before getting ashore (Martínez-Cedeira et al., Reference Martínez-Cedeira, Morales, García, Parada, Covelo and López2011). Then it has to be considered that the absence of records does not mean that the species is not present in the area, as it could be possible that the dead animals did not reach the shore and are not recorded. In the case of the family Ziphiidae there are even some species that have never been seen alive in the wild and everything that is known about their distribution has been inferred from strandings (MacLeod et al., Reference MacLeod, Perrin, Pitman, Barlow, Ballance, D'Amico, Gerrodette, Joyce, Mullin, Palka and Waring2006; Pitman, Reference Pitman, Perrin, Würsig and Thewissen2009). The presence of the two previously known species for the studied area (Cuvier's beaked whale and Sowerby's beaked whale) was confirmed with new records, and two new species were found (True's beaked whale and Blainville's beaked whale). Although mass strandings are known for these species (Heyning & Mead, Reference Heyning, Mead, Perrin, Würsig and Thewissen2009; Pitman, Reference Pitman, Perrin, Würsig and Thewissen2009; Bachara et al., Reference Bachara, Cermeño and Norman2014) all the records in the Galician coast were single-animal strandings. Beaked whales inhabit deep ocean waters (>2000 m deep) or continental slopes (200–2000 m) and are rarely seen over the continental shelf (Pitman, Reference Pitman, Perrin, Würsig and Thewissen2009), so they are not expected to be close to the Galician coast, where there is a continental shelf of 30–60 km (Fariña et al., Reference Fariña, Freire and González-Gurriarán1997). Therefore the stranded animals have been moved by currents or winds towards the coast and most of them presented in an advanced state of decomposition. Just two individuals (9.5% of total) stranded alive and one died on the same day.
Cuvier's beaked whale
In Spain the first recorded individual was a male captured near Santander in the Cantabrian coast in 1893 (Cabrera, Reference Cabrera1914). This has also been the most common beaked whale species in Galicia, with strandings all over the studied period and along the three considered areas. In the other areas of the East Atlantic, such as the coast of France, seasonal differences in strandings were described, with peaks in winter and spring (Robineau & di Natale, Reference Robineau, di Natale, Robineau, Duguy and Klima1995; Smith, Reference Smith2010). In UK and Ireland a similar pattern was found, with most strandings between winter and spring with peaks in January and July (MacLeod et al., Reference MacLeod, Pierce and Santos2004; Smith, Reference Smith2010; Rogan & Hernández-Milián, Reference Rogan and Hernández-Milián2011). In Portugal there were few strandings, and then it was not possible to detect any seasonal trends (Sequeira, Reference Sequeira1990; Ferreira et al., Reference Ferreira, Marçalo, Nicolau, Araújo, Santos, Pinheiro, Lopes, Mendes, Vaqueiro, Medina, Cascalho, Sequeira, Eira and Vingada2012). However, some seasonal local migrations were suggested for the Cuvier's beaked whale and other beaked whales species in UK and Northern Sea from stranded animals (Santos et al., Reference Santos, Pierce, Smeenk, Addink, Kinze, Tougaard and Herman2001b; MacLeod et al., Reference MacLeod, Pierce and Santos2004; Fernández et al., Reference Fernández, Pierce, MacLeod, Brownlow, Reid, Rogan, Addink, Deaville, Jepson and Santos2014) and even higher migrations from southern areas were inferred in diet studies of the Cuvier's beaked whale (MacLeod et al., Reference MacLeod, Pierce and Santos2004), and a sightings study in the Bay of Biscay proved that there is a seasonal northward movement from the south during spring through summer (Smith, Reference Smith2010). In Galicia annually seasonal patterns were not observed with statistical significance, but there was never a stranding between July and September. Considering two periods (1990–2002 and 2003–2013) the seasonal and geographic occurrence patterns changed with statistical significance along the years in the studied area. Between 1990 and 2002 the strandings were located along the three considered areas and only in autumn and winter, while in the last decade all the strandings were located in the north area and 85.7% in the spring period, when there is a prevalence of northern winds. It has been suggested that warming of local waters can lead to change in the local community of cetacean species (MacLeod et al., Reference MacLeod, Bannon, Pierce, Schweder, Learmonth, Herman and Reid2005) and it is known that the water temperature has increased in the Mediterranean Outflow Waters that reach the Galician slope from the south by 0.020°C per year (González-Pola et al., Reference González-Pola, Lavín and Vargas-Yáñez2005) and has also increased in the Eastern North Atlantic Central Water in the central Bay of Biscay at a maximum rate of 0.11°C per decade (Gómez-Gesteira et al., Reference Gómez-Gesteira, deCastro, Santos, Álvarez and Costoya2013), but the movement caused by warming does not seem to be the case of this species, since the Cuvier's beaked whale has a wide distribution from tropical to sub-polar waters (MacLeod et al., Reference MacLeod, Perrin, Pitman, Barlow, Ballance, D'Amico, Gerrodette, Joyce, Mullin, Palka and Waring2006).
The maximum size for the species is 7 m, both for males and females, and the average length for sexual maturity is 580 cm for females and 550 cm for males (Heyning, Reference Heyning, Ridgway and Harrison1989). Here, the larger animal recorded was a female of 650 cm and two of the stranded females and a male were adults.
Mesoplodon species
The Sowerby's beaked whale is endemic to the North Atlantic and the majority of stranding records are from northern Europe, mainly from the British Isles (Mead, Reference Mead, Ridgeway and Harrison1989). The record of this species in Galicia is not unexpected as some individuals had stranded in southern locations, such as Madeira (Maul & Sergeant, Reference Maul and Sergeant1977), Azores (Bachara et al., Reference Bachara, Cermeño and Norman2014), Portugal (Ferreira et al., Reference Ferreira, Marçalo, Nicolau, Araújo, Santos, Pinheiro, Lopes, Mendes, Vaqueiro, Medina, Cascalho, Sequeira, Eira and Vingada2012), Andalucia (Bellido et al., Reference Bellido, Cabot, Farfán, Castillo, Martín, Mons, Muñoz, Vázquez and Real2009) and the Canary Islands (Martín et al., Reference Martín, Tejedor, Pérez-Gil, Dalebout, Arbelo and Fernández2011). The two individuals stranded in the Galician coast in autumn, but no seasonal pattern can be inferred from just two records. In the closer areas they were found in different seasons: in Andalucia stranded in September (Bellido et al., Reference Bellido, Cabot, Farfán, Castillo, Martín, Mons, Muñoz, Vázquez and Real2009), in the Canary Islands stranded in April (Martín et al., Reference Martín, Tejedor, Pérez-Gil, Dalebout, Arbelo and Fernández2011) and in Euskadi (N of Spain) in July (Bachara et al., Reference Bachara, Cermeño and Norman2014). Both males and females can reach lengths of 5.5 m. Both individuals reported in this work are considered juveniles.
The True's beaked whale in the North Atlantic is distributed in temperate waters, and in the East Atlantic from Ireland to the Canary Islands (Vonk & Martin, Reference Vonk and Martin1988; Berrow & Rogan, Reference Berrow and Rogan1997; MacLeod et al., Reference MacLeod, Pierce and Santos2004, Reference MacLeod, Perrin, Pitman, Barlow, Ballance, D'Amico, Gerrodette, Joyce, Mullin, Palka and Waring2006; Brownell et al., Reference Brownell, Allen and Mead2011). This is the first known record for Galicia, with the closest records being some sightings in the Bay of Biscay (Weir et al., Reference Weir, Stokes, Martin and Cermeño2004). Two strandings have been reported in Cantabria region (N Spain) (Rey & Cendrero, Reference Rey and Cendrero1980, Reference Rey and Cendrero1981) but they have been considered as probably Cuvier's beaked whales in a recent review (Bachara et al., Reference Bachara, Cermeño and Norman2014). The maximum size for both sexes is slightly over 5 m (Jefferson et al., Reference Jefferson, Leatherwood and Webber1993), so the individual found at the Galician coast is considered an adult female. The total number of records from the northern hemisphere is only 58 (W. Bachara, personal communication).
The Blainville's beaked whale is the species with wider distribution of the genus Mesoplodon and it is thought to be continuous throughout the tropical, sub-tropical and warm-temperate waters of the world's oceans, with occasional occurrences in cold-temperate areas (MacLeod et al., Reference MacLeod, Perrin, Pitman, Barlow, Ballance, D'Amico, Gerrodette, Joyce, Mullin, Palka and Waring2006). It was recorded before in areas near to Galicia, such as Portugal (Sequeira, Reference Sequeira1990) and Andalucia (Valverde, Reference Valverde1996; Bellido et al., Reference Bellido, Cabot, Farfán, Castillo, Martín, Mons, Muñoz, Vázquez and Real2009). The maximum size for both sexes seems to be 4.7 m (Jefferson et al., Reference Jefferson, Leatherwood and Webber1993). The individual stranded in 2002 was 436 cm long, with the arching jaw and two flattened tusks, which allow it be identified as a male. This was the first known record for Galicia.
ACKNOWLEDGEMENTS
We thank the CEMMA volunteers for helping in the field work and data collection, the regional government Xunta de Galicia – Dirección Xeral de Conservación da Natureza for providing all the research permits to attend stranded animals in the field and Ismael Miján for the identification of the Sowerby's beaked whale deposited in the Osteological Collection of the Marine Mammal Section of the Sociedade Galega de Historia Natural, Ferrol. We are grateful to Wojtek Bachara for his helpful suggestions and the anonymous reviewers for their comments to improve the manuscript.
FINANCIAL SUPPORT
The Galician stranding network is supported by the regional government Xunta de Galicia, cofinanced with European Regional Development Funds (ERDF/FEDER). A.LL. is supported by a Doctoral Research Grant SFRH/BD/45339/2008 of the Universidade de Aveiro. A.L. is supported by a Postdoctoral Research Grant SFRH/BPD/82407/2011 CESAM of the Universidade de Aveiro.
