Cephalopods in the Diet of Nonbreeding Black-Browed and Grey-Headed Albatrosses from South Georgia

Polar Biol (2015) 38:631–641 DOI 10.1007/s00300-014-1626-3 ORIGINAL PAPER Cephalopods in the diet of nonbreeding black-browed and grey-headed albatrosses from South Georgia Pedro M. Alvito • Rui Rosa • Richard A. Phillips • Yves Cherel • Filipe Ceia • Miguel Guerreiro • Jose´ Seco • Alexandra Baeta • Rui P. Vieira • Jose´ C. Xavier Received: 12 January 2014 / Revised: 12 November 2014 / Accepted: 17 November 2014 / Published online: 7 December 2014 Ó Springer-Verlag Berlin Heidelberg 2014 Abstract The food and feeding ecology of albatrosses ([80 % by mass) was scavenged, and that scavenging is during the nonbreeding season is still poorly known, par- much more important during the nonbreeding season than ticularly with regard to the cephalopod component. This would be expected from breeding-season diets. The was studied in black-browed Thalassarche melanophris diversity of cephalopods consumed by nonbreeding birds in and grey-headed T. chrysostoma albatrosses by analysing our study was similar to that recorded during previous boluses collected shortly after adults returned to colonies at breeding seasons, but included two new species [Moro- Bird Island, South Georgia (54°S, 38°W), in 2009. Based teuthis sp. B (Imber) and ?Mastigoteuthis A (Clarke)]. on stable isotopic analyses of the lower beaks, we deter- Based on similarities in LRL, d13C and d15N, the squid mined the habitat and trophic level (from d13C and d15N, consumed may have been from the same oceanic popula- respectively) of the most important cephalopods and tions or region, with the exception of Taonius sp. B (Voss) assessed the relative importance of scavenging in terms of and K. longimana, which, based on significant differences the albatrosses’ feeding regimes. Based on lower rostral in d15N values, suggest that they may have originated from lengths (LRLs), the main cephalopod species in the diets of different stocks, indicating differences in the albatrosses’ both albatrosses was Kondakovia longimana, by frequency feeding regimes. of occurrence (F [ 90 %), number (N [ 40 %) and mass (M [ 80 %). The large estimated mass of many squid, Keywords Antarctica Á Albatrosses Á Cephalopods Á including K. longimana, suggests that a high proportion Thalassarche melanophris Á Thalassarche chrysostoma P. M. Alvito (&) Á F. Ceia Á M. Guerreiro Á J. Seco Á Introduction A. Baeta Á R. P. Vieira Á J. C. Xavier MARE-Marine and Environmental Research Centre, University of Coimbra, 3001-401 Coimbra, Portugal Albatrosses are regarded as apex predators in subantarctic e-mail: [email protected] and Antarctic ecosystems, feeding on a wide diversity of prey, including cephalopods (Xavier and Cherel 2009). R. Rosa These molluscs play an important role in the ecology of the Laborato´rio Marı´timo da Guia, Centro de Oceanografia, Faculdade de Cieˆncias da Universidade de Lisboa, Av. Nossa Southern Ocean, as key links in the food web between Senhora do Cabo, 939, 2750-374 Cascais, Portugal abundant mesopelagic fish and crustaceans, and higher predators such as albatrosses and marine mammals (Collins R. A. Phillips Á J. C. Xavier and Rodhouse 2006). Although free-living cephalopods in British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, the Southern Ocean are elusive, which limits opportunities UK for ship-based studies, albatrosses can be used as biological sampling tools; the tracking and diet sampling of these Y. Cherel marine birds improve our knowledge not only of their Centre d’Etudes Biologiques de Chize´, UMR 7372 du CNRS- Universite´ de La Rochelle, BP 14, 79360 Villiers-en-Bois, foraging behaviour but also of the distribution and ecology France of their cephalopod prey (Xavier et al. 2006). 123 632 Polar Biol (2015) 38:631–641 Albatrosses cover vast distances when foraging during period, (2) estimate the size of individual squid to assess the breeding and nonbreeding periods (Nel et al. 2001; the relative importance of scavenging versus predation and Phillips et al. 2004; Xavier et al. 2004; Croxall et al. 2005). (3) determine the habitat and trophic level of the most Black-browed (Thalassarche melanophris) and grey- important cephalopod species using stable isotope analy- headed (T. chrysostoma) albatrosses nest in dense colonies ses. Diet composition was based on analysis of boluses on subantarctic islands, including at South Georgia, which (pellets or casts) regurgitated voluntarily by adult alba- hold the largest grey-headed, and third largest black-bro- trosses shortly after they returned to South Georgia to wed albatross populations, respectively, in the world breed, at the end of the austral winter. Each bolus contains (Poncet et al. 2006). Tracking data from Bird Island indi- accumulated prey items (mainly cephalopod beaks), con- cate that during the chick-rearing period (January to June), sumed in the latter part of the nonbreeding period, almost both species forage mainly in Antarctic and subantarctic certainly over a period of several weeks given the long waters (Xavier et al. 2003b; Phillips et al. 2004). During residency time of squid beaks in the stomach of seabirds the nonbreeding season, most black-browed albatrosses recorded in previous studies (Furness et al. 1984). The from South Georgia migrate to waters off southern Africa, primary advantages of analysing boluses include the ease and a small minority to the Patagonian Shelf or Australasia of collection and minimal disturbance of birds, since han- (Phillips et al. 2005). There is even greater individual dling is not required (Xavier et al. 2005). Stable isotope variation in migration strategies of grey-headed alba- ratios were analysed in lower beaks found in these boluses trosses. Although most birds utilise oceanic waters, they to determine the habitat (d13C) and relative trophic level may remain entirely in the southwest Atlantic or spend (d15N) of the squid, the former based on the negative lat- varying proportions of time in the Atlantic, Indian and itudinal gradient in d13C in the Southern Ocean (Cherel and Pacific oceans and can make one or two circumpolar Hobson 2005). Hence, d13C values indicate water mass migrations around the Antarctic continent (Croxall et al. (subtropical vs. subantarctic or Antarctic), and higher vs. 2005). Stable isotope analyses of feathers confirm that lower values for d15N reflect the relative dependency on black-browed albatrosses from South Georgia moult in fish or squid compared with crustaceans (Cherel and productive neritic waters of the Benguela Current during Hobson 2007). Cephalopod beaks are hard structures which the nonbreeding period, but that grey-headed albatrosses grow by accretion of proteins and chitin, and there is no moult in subantarctic waters, near the subtropical front turnover after synthesis. Consequently, they retain mole- (Phillips et al. 2009; Cherel et al. 2013). cules built up from early development to time of death, and Previous studies of black-browed and grey-headed their isotopic signature integrates the feeding ecology of albatrosses during the chick-rearing period at South the animal over its whole life (Cherel and Hobson 2005). Georgia highlighted the considerable annual variation in dietary components, although black-browed albatrosses typically fed on crustaceans, cephalopods and fish (36–40, Materials and methods 31 and 27–35 %, respectively, of the diet by mass), and grey-headed albatrosses on cephalopods (50–55 % by Sampling mass) and, to a lesser extent, lamprey Geotria australis (10 % by mass) and other prey (Prince 1980; Rodhouse and Boluses, regurgitated by adult black-browed and grey- Prince 1993; Xavier et al. 2003a, 2013). Although many headed albatrosses that had recently arrived at colonies at live prey are obtained by plunge diving (Cherel and Klages Bird Island, South Georgia (54°000S38°030W), were col- 1998), a number of the cephalopods (comprising as much lected from the ground during daily visits from September as 13–14 % of the estimated total mass of all prey) were to December 2009 (Fig. 1; Table 1). All samples were potentially obtained by scavenging (Xavier and Croxall either identified and measured at Bird Island or frozen at 2007). Prior to the present study, the species composition -20 °C and analysed at the British Antarctic Survey of the diet of most albatrosses during the nonbreeding (BAS) headquarters (Cambridge, UK) or the Marine and period was unknown due to the difficulties of sampling Environmental Research Centre (MARE) of the University birds that spend their entire time at sea. Nonetheless, stable of Coimbra (Coimbra, Portugal). The components of the isotope analyses of feathers indicated that grey-headed and boluses (mostly indigestible items such as cephalopod black-browed albatrosses fed, respectively, at low to mid, beaks, cephalopod spermatophores, salps and penguin or at high trophic levels, within the Southern Ocean feathers; Xavier et al. 2003c) were identified to species (Phillips et al. 2009). level when possible. As seabirds retain squid beaks in the The aims of the present study were to (1) investigate the fore-gut for considerable periods (Furness et al. 1984), cephalopod component of the diet of black-browed and these beaks represent cephalopods consumed in the final grey-headed albatrosses at the end of the nonbreeding weeks of the nonbreeding period. No fish or crustacean 123 Polar Biol (2015) 38:631–641 633 remains were recorded. Cephalopod beaks were separated scavenging levels (cephalopods were put into 500 g cate- into upper and lower, and the former were counted and gories) followed Croxall and Prince (1994). discarded. The lower beaks were cleaned, counted and identified whenever possible to species level, and the lower Stable isotope analyses rostral length (LRL) measured using vernier calipers to the nearest 0.1 mm (Xavier and Cherel 2009). Allometric Lower beaks were cleaned and preserved in 70 % ethanol, equations were used to estimate dorsal mantle length (ML, dried subsequently in an oven at 50 °C for 6–24 h to drive mm) and the original wet body mass (M, g) from LRL off the ethanol, reduced to a fine powder, and then part of using Xavier and Cherel (2009), Piatkowski et al.

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