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UNIVERSIDADE DE LISBOA
FACULDADE DE CIÊNCIAS
DEPARTAMENTO DE BIOLOGIA ANIMAL
Albatross-Cephalopod Interactions in Antarctic Ocean:
implications for albatrosses ecology and conservation
Pedro Miguel Oliveira Soromenho de Alvito
Dissertação
MESTRADO EM BIOLOGIA DA CONSERVAÇÃO
2012
UNIVERSIDADE DE LISBOA
FACULDADE DE CIÊNCIAS
DEPARTAMENTO DE BIOLOGIA ANIMAL
Albatross-Cephalopod Interactions in Antarctic Ocean:
implications for albatrosses ecology and conservation
Pedro Miguel Oliveira Soromenho de Alvito
Dissertação
MESTRADO EM BIOLOGIA DA CONSERVAÇÃO
Orientada pelo Doutor Rui Afonso Bairrão da Rosa (CO/LMG) E co-orientada pelo Doutor José Carlos Caetano Xavier
(IMAR-CMA)
2012
i
Acknowledgements
The preparation of a dissertation can be compared to writing a book. On the Alexandre
Dumas novel “The Three Musketeers”, D'Artagnan needed the help of his inseparable
friends to attain his goals. In the same way I am very grateful to those who had helped
me to organize and write this dissertation, in particular to:
Doctor José Xavier and Doctor Rui Rosa for their supervision, support, advices and
help while writing the dissertation, as well as their availability and rapid answers to
questions. I also thank Doctor José Xavier for the opportunity to study the spectacular
life of albatrosses and the enigmatic Antarctic cephalopods, as well as his availability
and transfer of knowledge during the identification of the cephalopod beaks performed
at the Instituto do Mar, University of Coimbra;
My friend Miguel Guerreiro, without who I would not have been aware of this
dissertation, and for his friendship and help over the developmental and experimental
work at Coimbra and Centre d ' Études biologiques of Chizé (France);
All the people from Instituto do Mar, University of Coimbra, who supported me during
my experimental work: Filipe Ceia for supervising the experimental work and
contribute with data on isotopic analysis data (France), Rui Vieira for contributing with
isotopic analysis data, José Seco for the help on samples screening and preparative
work for isotopic analyses, Alexandra Baeta, for contributing with data on isotopic
analysis data (Coimbra). And finally to Gabi, for the continuous kindness and laboratory
suport.
All the people from the Centre d'Etudes biologiques of Chizé, team Ecologie et des
Oiseaux Mammifères Marins (France) who supported me during my visit and
particularly to Doctor Yves Cherel, for his kind reception and mainly the “hard”
discussion on results on stable isotopic analyses.
My lovely family for their patience and support, specially to my parents, brother and
sister and grandmother for their affection and understanding. I also thank my mother
for her support throughout the process of writing the dissertation.
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Abstract and keywords
Albatrosses can be used as biological sampling tools to investigate poorly known
organisms, such as the Southern Ocean cephalopods. The aims of the present study
were to characterize the albatrosses diet, with relevance to the cephalopod component,
during the reproductive period of wandering (Diomedea exulans), black-browed
(Thalassarche melanophrys) and grey-headed (Thalassarche chrysostoma) at Bird
Island (South Georgia), and at the end of inter-breeding/beginning of breeding period
(EIB/BB) of the last two albatross species, to assess the habitat and trophic level of key
cephalopods species by stable isotopes analyses, to compare both sampled periods, to
identify threats and suggest measures to reinforce these albatrosses conservation.
During the reproductive period, black-browed albatross fed mainly on fish, the grey-
headed albatross on cephalopods, and the wandering albatross on both prey. The four
main cephalopod species found in the albatrosses diets were Kondakovia longimana,
Martialia hyadesi, Moroteuthis knipovitchi and Galiteuthis glacialis during the
reproductive period. For the first time, black-browed and grey-headed albatrosses diets
during the EIB/BB period were analyzed. K. longimana was reported as the main
cephalopod species during this period and it was found that scavenging could play an
important role in albatrosses diet.
Based on the stable isotopic signatures of the cephalopod lower beaks, the main
species were from Antarctic and sub-Antarctic waters and could be grouped in four
trophic levels.
The main threats to albatrosses included: i) interaction with fisheries, ii) the possible
lower availability of krill in South Georgia region during the reproductive period, and iii)
the almost absence of the M. hyadesi in grey-headed albatrosses diet. Some measures
to reinforce the conservation of the three studied albatross species are related to the
fishery and krill industries and by a better knowledge of southern ocean cephalopods
distributions and populational trends.
Keywords: Antarctica, albatrosses, cephalopods, trophic relationships, conservation.
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Resumé and keywords (in portuguese)
As populações do albatroz-viajeiro Diomedea exulans, albatroz-de-cabeça-cinzenta
Thalassarche chrysostoma e albatroz-de-sobrancelha-preta Thalassarche
melanophrys, nidificantes em Bird Island na Geórgia do Sul, são alvos de estudos
desde a década de 1960. Esta ilha subantárctica é muito importante para a sua
conservação, porque nela nidificam, a nível mundial, as maiores populações do
albatroz-de-cabeça-cinzenta, e importantes populações das restantes espécies
estudadas. Contudo, desde finais da década de 1970 que, nesta ilha, as populações
nidificantes destes albatrozes têm experimentado decréscimos populacionais,
seguindo a tendência de declínio a nível mundial. A cada ano, dezenas de milhares de
albatrozes são apanhados acidentalmente em linhas de pesca. Os resíduos de
plásticos ingeridos no mar, e a introdução de espécies não-nativas nas ilhas de
nidificação também apresentam riscos adicionais.
A dieta das espécies de albatrozes estudadas inclui uma importante componente de
cefalópodes. Os albatrozes podem ser utilizados como ferramentas de amostragem
biológicas para investigar os organismos pouco conhecidos, tais como os cefalópodes
do Oceano Antárctico. Através do estudo do componente de cefalópodes na dieta dos
albatrozes pode-se conhecer melhor a ecologia e dinâmica populacional dos
cefalópodes do Oceano Antárctico, que de outro modo seria muito difícil de ser obtido.
Através da análise isotópica do rácio do δ13C (13C/12C) e do δ15N (15N / 14N) das
mandíbulas inferiores dos cefalópodes presentes na dieta dos albatrozes pode-se
ainda revelar o habitat e o nível trófico dos cefalópodes, respectivamente. Por
intermediário desta análise já foram descobertas novas relações tróficas e padrões
migratórios dos cefalópodes até então desconhecidos.
Os objectivos do presente estudo consistiram em: i) caracterizar a dieta dos
albatrozes, com relevância para a componente de cefalópodes, durante o período
reprodutor do albatroz-viajeiro, albatroz-de-sobrancelha-preta e albatroz-de-cabeça-
cinzenta, e no final do período não reprodutor /início do período reprodutor (FPNR / IR)
das duas últimas espécies referidas; ii) avaliar o habitat e o nível trófico das principais
espécies de cefalópodes identificadas na dieta dos albatrozes através da análise de
isótopos estáveis; iii) comparar os dois períodos amostrados (reprodutor versus
iv
FPNR/IR); e iv) identificar as ameaças e sugerir medidas para reforçar a conservação
das espécies de albatrozes estudadas.
Os resultados relativos à dieta dos albatrozes mostraram que, durante o período
reprodutor, o albatroz-de-sobrancelha-preta alimentou-se sobretudo de peixe, o
albatroz-de-cabeça-cinzenta de cefalópodes, e o albatroz-viajeiro de ambos os
componentes. As quatro principais espécies de cefalópodes identificadas na dieta dos
albatrozes incluíram Galiteuthis glacialis, Moroteuthis knipovitchi, Martialia hyadesi e
Kondakovia longimana para o período reprodutor. A diversidade dos cefalópodes
registada neste estudo foi menor do que a registada em anos anteriores,
correspondendo a espécies anteriormente descritas por outros autores. Não foram
encontradas espécies de polvos contrariamente a outras referências nesta área. A
maior diversidade de cefalópodes durante o período reprodutor foi registada na dieta
do albatroz-viageiro. A sua dieta incluiu cefalópodes maiores e mais pesados do que
os identificados na dieta dos restantes albatrozes, indicativo de necrofagia. O albatroz-
de-sobrancelha-preta durante o período reprodutor também foi principalmente
necrófago, enquanto que o albatroz-de-cabeça-cinzenta se alimentou maioritariamente
de presas vivas. Para os outros albatrozes, a diversidade de cefalópodes identificada
no período reprodutor foi maior do que a encontrada durante o período FPNR/IR. Pela
primeira vez, as dietas do albatroz-de-sobrancelha-preta e do albatroz-de-cabeça-
cinzenta foram analisadas durante o período FPNR/IR. K. longimana foi a espécie de
cefalópode mais importante para o período FPNR / IR e verificou-se que a necrofagia
poderá ter um papel importante na alimentação dos albatrozes. As únicas espécies de
cefalópodes comuns a ambos os períodos amostrados foram K. longimana, G.
glacialis, Gonatus antarcticus e Taonius sp.B (Voss), pelo que se sugere que possam
ter, sobretudo K. longimana, uma maior importância nos ecossistemas marinhos do
que a que lhes era habitualmente atribuída.
Através da análise isotópica do rácio de δ13C (13C/12C) das mandíbulas inferiores dos
cefalópodes, verificou-se que as principais espécies encontradas na dieta dos
albatrozes apresentaram assinaturas referentes a águas antárcticas e subantárticas.
No primeiro caso, as espécies de cefalópodes associadas foram Batoteuthis skolops e
Psychroteuthis glacialis, e no segundo foram Chiroteuthis veranyi, Histioteuthis
macrohista, Histioteuthis atlantica e Taonius sp. B (Voss). Para além destes
cefalópodes, foram identificadas outras espécies que apresentaram assinaturas
isotópicas referentes às duas massas de água, antárctica e subantártica,
v
nomeadamente, Histioteuthis eltaninae, Moroteuthis knipovitchi, Kondakovia
longimana, Gonatus antarcticus, Martialia hyadesi, Galiteuthis glacialis e Alluroteuthis
antarcticus. Por fim, foi ainda identificada a espécie Illex argentinus com uma
assinatura referente a águas subtropicais.
Através da análise isotópica do rácio de δ15N (15N / 14N) das mandíbulas inferiores dos
cefalópodes, verificou-se que as espécies de cefalópodes poderiam ser agrupadas em
quatro níveis tróficos distintos, compreendendo assinaturas entre os 2.45 a 4.40‰,
6.19 a 6.63‰, 7.15 a 8.83‰ e 9.02 a 12.18‰. No primeiro grupo referido inclui-se
Martialia hyadesi, no segundo Kondakovia longimana (com mandíbulas de tamanho
médio), no terceiro Histioteuthis eltaninae, Moroteuthis knipovitchi, Kondakovia
longimana (com mandíbulas de tamanho grande), Galiteuthis glacialis, Alluroteuthis
antarcticus e Psycroteuthis glacialis, e no último Gonatus antarcticus, Chiroteuthis
veranyi, Illex argentinus, Taonius sp. B (Voss), Histioteuthis macrohista, Histioteuthis
atlantica e Batoteuthis skolops. A ocorrência destes níveis tróficos sugere a existência
de um continuum entre cefalópodes de níveis tróficos inferiores que se alimentam de
crustáceos (como M. hyadesi) e de níveis tróficos superiores que se alimentam de
peixes (como G. antarcticus). Os cefalópodes apresentaram assinaturas mais baixas
do que aquelas geralmente registadas, o que poderá indicar que se alimentaram de
presas que normalmente ocupam níveis tróficos inferiores. Os indivíduos de K.
longimana apresentaram um enriquecimento em N15 com o aumento do tamanho da
mandíbula inferior, como já anteriormente descrito por outros autores.
As principais ameaças identificadas para as espécies de albatrozes estudadas tendo
por base as suas dietas foram: i) a interacção com a pesca, ii) a eventual baixa
disponibilidade de krill Euphausia superba na Geórgia do Sul durante o período
reprodutivo dos albatrozes, que afectou sobretudo o albatroz-de-sobrancelha-preta e
iii) a ausência de M. hyadesi na dieta do albatroz-de-cabeça-cinzenta. A principal
causa do declínio da maioria das espécies de albatrozes é conhecida ou inferida,
como sendo a mortalidade acidental na pesca (bycatch), especialmente na pesca de
palangre e de arrasto, onde os albatrozes são vulneráveis a anzóis, redes de arrasto e
cabos de armação das mesmas. Na dieta do albatroz-viajeiro foram encontrados
anzóis e linhas de pesca, incluindo uma linha de palangre. Foram ainda identificadas
espécies de peixes na dieta do albatroz-viajeiro e do albatroz-de-sobrancelha-preta
alvos da pesca comercial. O albatroz-de-sobrancelha-preta em anos de baixa
disponibilidade de presas não altera a sua área de alimentação, pelo que uma baixa
vi
disponibilidade de krill poderá ser indício de um baixo sucesso reprodutor, contribuindo
para um decréscimo populacional desta espécie. Os dados da dieta do albatroz-de-
cabeça-cinzenta sugerem que poderá ter enfrentado um baixo sucesso reprodutor no
período avaliado devido à quase ausência de M. hyadesi, cujo consumo está
relacionado com o seu sucesso reprodutor.
Tendo por base as ameaças referidas, sugerem-se como medidas para reforçar a
conservação destas três espécies de albatrozes a continuação de acções já iniciadas
como: i) implementação de medidas de mitigação para reduzir as capturas acidentais
de aves marinhas nas frotas de pesca, ii) combate à pesca ilegal, não declarada e não
regulamentada (INN),e iii) controlo da expansão da pesca industrial do krill. Para além
destas, sugere-se fortemente o desenvolvimento e aplicação de novas medidas como
a protecção das zonas potenciais de alimentação dos albatrozes durante os períodos
reprodutor e não reprodutor através do conhecimento das distribuições e tendências
populacionais das principais espécies de cefalópodes por estes capturados.
Palavras-chave: Antárctida, albatrozes, cefalópodes, relações tróficas, conservação.
Index
ACKNOWLEDGEMENTS .................................................................................................................. I
ABSTRACT AND KEYWORDS ........................................................................................................... II
RESUMÉ AND KEYWORDS (IN PORTUGUESE) .................................................................................. III
1. GENERAL INTRODUCTION ......................................................................................................... 1
1.1 Why doing research in the Antarctic?.............................................................................. 1
1.2 The Southern Ocean ....................................................................................................... 1
1.3 Bird Island, South Georgia .............................................................................................. 2
1.4 Studied albatrosses species ............................................................................................ 3
1.5 Southern Ocean cephalopods ......................................................................................... 4
1.6 Albatross-cephalopod interactions .................................................................................. 5
1.7 Albatrosses main threats ................................................................................................. 6
1.8 Stable isotopes: concepts and terminology ..................................................................... 8
1.9 Thesis’ framework ........................................................................................................... 8
1.10 Thesis’ objectives .......................................................................................................... 9
2. MATERIAL AND METHODS ....................................................................................................... 10
2.1 Sampling ........................................................................................................................ 10
2.1.1 Diet Analysis ........................................................................................................... 11
2.2 Isotopic analysis ............................................................................................................ 12
2.3 Statistical analysis ......................................................................................................... 13
3. RESULTS AND DISCUSSION ..................................................................................................... 14
3.1 Black-browed albatross ................................................................................................. 14
3.1.1 Reproductive period ............................................................................................... 14
3.1.2 At the end of inter-breeding/beginning of breeding period (EIB/BB) ...................... 16
3.2 Grey-headed albatross .................................................................................................. 22
3.2.1 Reproductive period ............................................................................................... 22
3.2.2 At the end of inter-breeding/beginning of breeding period (EIB/BB) ...................... 23
3.3 Wandering albatross ..................................................................................................... 24
3.3.1 Reproductive period ............................................................................................... 24
3.4 Characterization and comparison of the reproductive and EIB/BB periods .................. 26
3.5 Comparison between the main cephalopod species found in albatross’ diets ............. 28
3.5.1 Kondakovia longimana ........................................................................................... 29
3.5.2 Galiteuthis glacialis ................................................................................................. 29
3.5.3 Moroteuthis knipovitchi ........................................................................................... 30
3.5.4 Martialia hyadesi .................................................................................................... 30
3.6 Cephalopods habitats and trophic levels ...................................................................... 30
3.6.1 Prey habitats........................................................................................................... 31
3.6.2 Prey trophic levels .................................................................................................. 32
3.7. Main threats and suggested measures to reinforce these albatrosses conservation .. 33
4. CONCLUDING REMARKS ......................................................................................................... 35
REFERENCES ............................................................................................................................ 38
APPENDICES.............................................................................................................................. 45
1
1. General Introduction
1.1 Why doing research in the Antarctic?
Antarctica is a remarkable continent. Remote, hostile and uninhabited, Antarctica is key
to understanding how our world works, and our impact upon it. For example, Antarctica
is important for science because of its profound effect on the Earth's climate and ocean
systems (BAS, 2012; Murphy el at. 2012). Around 30 countries operate Antarctic
research stations where scientists study global environmental issues like climate
change, ozone depletion and ozone hole, ocean circulation, sea level rising, and
sustainable management of marine life (BAS, 2009). Locked in its four kilometre-thick
ice sheet is a unique record of what our planet's climate was like over the past one
million years. Antarctic science has also revealed much about the impact of human
activity on the natural world. As well as being the world's most important natural
laboratory, the Antarctic is a place of great beauty and wonder. However, Antarctica is
fragile and increasingly vulnerable (BAS, 2012) and research is still urgently needed.
1.2 The Southern Ocean
The Southern Ocean, which surrounds the Antarctic continent, consists of a system of
deep-sea basins, separated by three systems of ridges: the Macquarie Ridge (south of
New Zealand and Tasmania), the Scotia Arc (between the Patagonian shelf and the
Antarctic Peninsula) and the Kerguelen Ridge (Carmack, 1990). It is bounded to the
north by the Antarctic Polar Front (APF) or Antarctic Convergence (Carmack, 1990)
(Fig. 1). The location of the APF, where cold Antarctic surface water meets warmer
sub-Antarctic water flowing southeast, varies temporally and spatially (between 47 and
63oS) and is characterized by a distinct change in temperature (2–3oC) and other
oceanographic parameters (Carmack, 1990). It acts as a biological barrier, making the
Southern Ocean a largely closed system. Sea ice covers large areas of the Southern
Ocean; the extent varies seasonally from ~10% in summer to 50% of the total area in
winter (Carmack, 1990). Within the Southern Ocean, sub-Antarctic Islands, such as
South Georgia, Crozet, Kerguelen and Heard, are areas of enhanced productivity and
support large populations of higher predators such as whales, seals and seabirds
(Atkinson et al., 2001), as well as fisheries for toothfish, krill and icefish (Kock, 1992;
Agnew, 2004).
2
1.3 Bird Island, South Georgia
The study site is Bird Island, South Georgia (54°S, 38°W), one of the islands where the
three studied albatross species breed (Xavier et al., 2003a and b). South Georgia is
part of the Scotia Ridge, a mainly submarine arc extending from South America to the
Antarctic Peninsula, with surface extensions at Shag Rocks, South Georgia and the
South Sandwich, South Orkneys and South Shetland Islands (Xavier, 2002; Foster,
1984) (Fig. 1). Located 200 km south of the Antarctic Polar Front, is it a sub-Antarctic
region, although surrounding water mass and its wildlife have mainly polar origin (Orsi
et al., 1995; Peterson, 1992).
Figure 1 – Geographical location of South Georgia and a schematic representation of the surface water circulation in the study area. Arrows represent the direction and water temperature, from blue (cold water) to red (warm water). Legend: ACC-Antarctic Circumpolar Current, APF- Antarctic Polar Front; APFZ - Antarctic Polar Front Zone, SAF - Sub-Antarctic Front, STF - Sub-Tropical Front. The position of the 1000m isobath is also presented (Orsi et al,1995; Hellmer and Bersch, 1985).
3
1.4 Studied albatrosses species
Albatrosses belong to the Diomedeidae family, a group also known as Procellariiformes
or ‘tube noses’ (BAS, 2008). The three species studied here are the black- browed
(Thalassarche melanophrys), grey-headed (Thalassarche chrysostoma) and wandering
(Diomedea exulans) albatrosses (Fig. 2), listed the first two as Vulnerable and the latter
as Endangered by the IUCN Red List of Threatened Species (IUCN 2010 a, b and c).
Black-browed albatross Grey-headed albatross Wandering albatross Thalassarche melanophrys Thalassarche chrysostoma Diomedea exulans Figure 2 – The three species of albatrosses studied here (photos by José Xavier).
Albatrosses cover vast distances when foraging for food (BAS, 2008; Xavier et al.
2004). Grey-headed and black-browed albatrosses are known to forage mostly in
Antarctic waters while breeding (Harrison et al., 1991; Phillips et al, 2007), whereas
wandering albatrosses have a broader foraging range, between 25–64oS and 19–80oW
(Prince et al., 1998). Outside the breeding season, many species (including wandering
and grey-headed albatrosses from South Georgia) migrate long distances, some
circumnavigate around the Antarctic continent (BAS, 2008; Croxall et al, 2005). They
spend over 80% of their life at sea, visiting land only for breeding (WWF, 2012). As well
as being the largest seabirds, with wing spans of up to 3.5m, albatrosses are also the
longest lived, some surviving for more than 60 years. They take many years to reach
sexual maturity, not breeding until they are around 10 years old (BAS, 2008). Male and
female birds form a pair after ritual mating dances and this bond lasts for their lifetime
(WWF, 2012).
The three studied albatross species nest in colonies on sub-antarctic islands, breeding
annually in the case of black -browed albatross and bi-annually in wandering and grey-
headed albatrosses (Xavier et al., 2003a and b). In terms of breeding cycle, black-
browed and gray-headed albatrosses have a reproductive period between September
and June, while wandering albatrosses between November and November-December
4
of the following year (Xavier, 2002; see also Fig. 3). In the present dissertation, when
“reproductive period” is referred it corresponds to chick provisioning, and “at the end of
inter-breeding period/beginning of breeding period” correspond to the period that goes
from arrivals and mating to the incubating phase (Fig. 3).
WA
Arrivals and Mating
Egg Laying
Incubating
Chick provisioning
BBA
GHA
JAN
FEBMAR
APR
MAY
JUNE
JULY
AUGSEP
OCT
NOV
DEC
Figure 3 – Breeding cycle of the three studied albatross species (adapted from ACAP, 2009, 2010a and b). Abbreviations: BBA= black-browed albatrosses; GHA= grey-headed albatrosses; WA=wandering albatrosses; JAN=January; FEB=February; MAR=March; APR= April; AUG=August; SEP= September; OCT= October; NOV=November; DEC=December.
1.5 Southern Ocean cephalopods
The Southern Ocean cephalopod fauna is distinctive, with high levels of squid
endemism and particularly in the octopods. Loliginid squid, sepiids and sepiolids are
absent from the Southern Ocean, and all the squid are oceanic species. The octopods
dominate the neritic cephalopod fauna, with high levels of diversity, probably
associated with niche separation (Collins and Rodhouse, 2006). As in most temperate
cephalopods, Southern Ocean species also appear to be semelparous, but growth
rates are lower and longevity greater than temperate counterparts (Collins and
Rodhouse, 2006). Also, eggs are generally large and fecundity low, with putative long
development times (Collins and Rodhouse, 2006). Reproduction may be seasonal in
the squid but is extended in the octopods (Collins and Rodhouse, 2006). Cephalopods
play an important role in the ecology of the Southern Ocean, linking the abundant
mesopelagic fish and crustaceans with higher predators such as albatross, seals and
5
whales (Collins and Rodhouse, 2006). To date Southern Ocean cephalopods have not
been commercially exploited, but there is potential for exploitation of Martialia hyadesi,
Kondakovia longimana, Moroteuthis knipovitchi and Gonatus antarcticus (Rodhouse
1990; Xavier et al., 2007).
One way to determine the identity and size of these cephalopods is by analyzing their
beaks present on the diet of its predators (most of the times the only way to access
cephalopod material).The cephalopod beaks are divided into an upper and a lower
beak (Fig. 4a and b, respectively), with its own morphology and key measurements. In
this study it will be used the lower rostral length (Fig. 4 b) from the lower beak. Based
on this metric length, several cephalopod characteristics can be estimated, such as
dorsal mantle length (Fig. 4 c) and the original wet body mass (both variables were
estimated in the present study).
Figure 4 – Cephalopod upper beak (a) and lower beak, with lower rostral length (LRL; b), adapted from Xavier and Cherel, 2009. Cephalopod dorsal mantle length (ML; c) adapted from Zeidberg, 2004.
1.6 Albatross-cephalopod interactions
Within seabirds, albatrosses play a key role in the Antarctic ecosystem as top
predators, feeding on a wider diversity of prey (Xavier, 2002), including cephalopods
(Xavier and Cherel, 2009).
Black-browed albatrosses during reproductive period feed mainly on crustaceans, such
as Antarctic krill Euphausia superba, but also cephalopods (e.g. Martialia hyadesi) and
fish, such as icefish Champsocephalus gunnari (Xavier et al., 2003 b; Prince et al.,
1998). On the other hand, grey-headed albatrosses feed mainly on cephalopods, such
a) b) c)
6
as Martialia hyadesi, but also feeds on other preys, such as lamprey Geotria australis
(Catry el al, 2004;; Xavier et al., 2003a,b,c). Black-browed and grey-headed
albatrosses diet during non-breeding period is unknown, as they spend their time at
sea (i.e. there is no possibility of collecting diet samples). During reproductive period,
wandering albatrosses feed mainly cephalopods and fish, catching a varied selection of
cephalopod species (ca. 50 species; mainly cranchiid and onychoteuthid squid, as
Taonius sp.B (Voss) and Kondakovia longimana, respectively) and a more restricted
range of fish (ca. 10 species) (Rodhouse et al., 1987; Croxall et al., 1988; Xavier et al.,
2003a).
Wandering albatrosses feed on larger prey than smaller albatross species (Xavier and
Croxall, 2007) and capture them by surface seizing while black-browed and grey-
headed albatrosses can also feed by plunge diving,
Squid post-spawning death events are also likely to occur during the Antarctic winter
(particularly for onychoteuthids, histioteuthids and cranchiids) and, therefore,
wandering albatrosses, as scavengers, might explore fully this type of resource (Xavier
and Croxall, 2007).
Due to this predator-prey interaction, albatrosses can be used as sampling tools to
investigate poorly studied organisms, such as Southern Ocean cephalopods, and in the
meantime while improving our knowledge in cephalopods we improve our knowledge
on the foraging and feeding behavior of these albatrosses species.
1.7 Albatrosses main threats
Long-term studies at Bird Island, South Georgia, show that numbers of wandering,
black-browed and grey-headed albatrosses have been declining since the late 1970s
(Poncet et al, 2006), following the global trend (IUCN 2010a,b,c). It is a huge problem
to these species because South Georgia holds the largest population of grey-headed
albatross Thalassarche chrysostoma, the second largest of wandering albatross
Diomedea exulans and the third largest black-browed albatross Thalassarche
melanophrys in the world (Gales 1998; Robertson et al. 2003; Lawton et al. 2003).
Each year, tens of thousands of albatrosses are drowned as they scavenge behind
fishing boats (BAS, 2008). Plastic waste ingested at sea, and introduction of non-native
species onto breeding islands pose additional hazards (BAS, 2008). Nonetheless, the
7
main cause of the decline of most albatross species are known to be the incidental
mortality in fisheries (by-catch), especially in longline (Fig. 5) and trawling (Fig. 6)
fisheries, where albatrosses are vulnerable to baited hooks and trawl nets and cables
(Croxall et al., 1990; Nel et al. 2000; Weimerskirch et al., 1997; Schiavini et al., 1998;
Sullivan et al., 2003).
Figure 5 – Longline fishing operation (FAO, 2012).
Figure 6 – Bottom pair trawls (Nédélec and Prado, 1990).
Black-browed and wandering albatrosses are the ones that most interact with
commercial fishing, being possible to see huge flocks following fishing vessels (ACAP,
2009, 2010a). Grey-headed albatrosses are non-common ship followers, but the
presence of some carcasses in fishing lines suggested some (small) level of interaction
(ACAP, 2010b; Xavier et al, 2003c).
The implementation of mitigation measures to reduce seabirds by-catch and an
effective combat to illegal, unreported and unregulated (IUU) fishing are crucial to
prevent these threats to albatrosses (Small, 2005), which allied to a better knowledge
8
of southern ocean cephalopods distributions (and population trends) could enable us to
protect these birds more efficiently by knowing their potential feeding zones
1.8 Stable isotopes: concepts and terminology
Each element (hydrogen, carbon, nitrogen, oxygen) occurs in nature in different forms
called stable isotopes (same number of protons and different number of neutrons).
Stable isotopes with less neutrons are called light elements and those with more
neutrons are called heavy elements. The abundance of each form varies in a global
scale due to physical and biogeochemical factors that influence fractionation
(partitioning of heavy and light isotopes between a source substrate and the product(s);
Peterson and Fry, 1987; Dawson et al, 2002), allowing the creation of a fingerprint of
each site based on differences of isotopic ratios (heavy element / light element;
Dawson et al, 2002).
The isotope ratios of plant and animal tissues represent a temporal integration of
significant physiological and ecological processes on the landscape. The timescale of
this integration depends on the element turnover rate of the tissue or pool in question.
In this study, stable isotope analyses were used in cephalopod lower beaks. These
hard structures grow by accretion of new molecules of proteins and chitin and there is
no turnover after synthesis. Consequently, cephalopod beaks retain molecules built up
from early development to time of death and their isotopic signature integrates the
feeding ecology of the animal over its whole life (Cherel and Hobson, 2005).
For natural abundance, the stable isotope composition of a particular material or
substance is expressed as a ratio relative to an internationally accepted reference
standard, as X = [(Rsample / Rstandard) -1] 1000, where X is the stable isotope of
interest (13C and 15N in this study) and R is the abundance ratio of those isotopes
(Dawson et al, 2002; Stowasser et al, 2012). A positive δ value therefore indicates that
the sample contains more of the heavy isotope than the standard (Dawson et al, 2002).
1.9 Thesis’ framework
This thesis was conducted under the framework of the POLAR project, included in the
Portuguese Polar Program (PROPOLAR) during the International Polar Year of 2007-
2009, which was followed by the CEPH project. The main goal of the POLAR project
was to evaluate the predator-prey interactions in the Southern Ocean in relation to
9
climate change, using new technologies applied to marine ecology, such as stable
isotope signatures. POLAR was a multi-disciplinary product of an international
collaboration with the United Kingdom, France and Germany (Portal Polar, 2008). On
the other hand, the CEPH project aimed to assess the importance of cephalopods in
the Antarctic Ocean, particularly through diet of top predators, including albatrosses,
penguins, seals and fish. This project is an international and multidisciplinary, involving
several countries, and coordinated by the Institute of Marine Research, University of
Coimbra and the British Antarctic Survey.
1.10 Thesis’ objectives
The aim of the present study was to investigate the albatross-cephalopod interactions
in the Southern Ocean, namely by: i) Characterizing the albatrosses diet, with
relevance to the cephalopod component, during the reproductive period of wandering
(Diomedea exulans), black-browed (Thalassarche melanophrys) and grey-headed
(Thalassarche chrysostoma), and at the end of inter-breeding/beginning of breeding
period (EIB/BB) of the last two species; ii) Assessing the habitat and trophic level of
key cephalopods species found in the diet of the three studied albatross species during
the studied periods using stable isotopes analyses; iii) Comparing both sampled
periods (Reproductive versus EIB/BB periods); and iv) Identifying threats and suggest
measures to reinforce these albatrosses conservation.
10
2. Material and Methods
2.1 Sampling
The stomach contents were involuntarily obtained from black-browed (Thalassarche
melanophrys), grey-headed (Thalassarche chrysostoma) and wandering (Diomedea
exulans) albatrosses chicks after been fed by their parents. They were randomly
collected on the colonies off Bird Island, South Georgia (54 ° 00'S, 38 ° 03 'W), from
February to April 2009 for the first two albatrosses, and from May to September 2009
for wandering albatrosses (i.e during the reproductive periods). The method of
obtaining stomach contents consists on reversing the albatrosses and massage its
stomach, if necessary, in order to stimulate regurgitation (Xavier et al, 2003b). Each
chick was sampled only once and several colonies were analyzed in order to make
considerations of the general breeding population on Bird Island. The welfare of the
chicks sampled was monitored after obtaining the data and there were no differences
in survival between birds sampled and not sampled.
While collecting the stomach contents of wandering albatrosses chicks, adults black-
browed and grey-headed albatrosses that arrived to Bird Island to nest had started to
regurgitated voluntarily indigestible items (i.e. cephalopod beaks) that could not be
digested, providing an extraordinary opportunity to collect their boluses. The boluses
were randomly collected near their respective nesting colonies from September to
December of 2009, at the end of inter-breeding period/beginning of the breeding
period. It is worth noting that the present study is the first time to analyze such data
(from the end of inter-breeding period/beginning of the breeding period).
We compared the diet data from the chicks (stomach contents) and the adults
(boluses). As the chicks eat what is given by adults there is no problem of comparing
the data from these two types of sampling.
A total of 80 stomach contents were collected from black-browed (n= 30), grey-headed
(n= 30) and wandering albatrosses (n=20) in 2009, during reproductive period (Table
1). A total of 46 boluses were collected from black-browed (n= 14) and grey-headed
albatrosses (n= 32) in 2009, during the end of inter-breeding/beginning of breeding
period (Table 1).
11
Table 1 – Total number of boluses during reproductive period and stomach contents during the end of inter-breeding/beginning of breeding period (EIBB/BB; samples), total number of cephalopod beaks (upper – including fresh and non-fresh beaks; and lower – fresh beaks), mean number of fresh lower beaks per sample and number of cephalopod species found in black-browed (Thalassarche melanophrys), grey-headed (Thalassarche chrysostoma) and wandering albatrosses (Diomedea exulans).
Albatross species Year Period Cephalopod beaks
Thalassarche melanophrys 2009 Reproductive 30 244 82 2,2
Thalassarche melanophrys 2009 EIB/BB 14 138 5 0,4
Thalassarche chrysostoma 2009 Reproductive 30 580 158 5,4
Thalassarche chrysostoma 2009 EIB/BB 32 346 7 0,2
Diomedea exulans 2009 Reproductive 20 872 130 6,5
10
2
15
3
Number
of samples
Mean number
of lower beaks
per sample
Number of
cephalopod
speciesUpper beaks Lower beaks
6
2.1.1 Diet Analysis
All samples were frozen at -20°C (Xavier et al, 2003b; Clarke, 1986) and immediately
sampled on Bird Island or two years later at the Institute of Marine Research (IMAR-
CMA) of the University of Coimbra, Portugal. The stomach contents were weighted and
then its components separated by categories (cephalopods, crustaceans, fish and
other contents – carrion, debris, hooks and fishing lines, non-food and other food),
following the methodology described by Xavier et al (2003b). The cephalopod beaks
found in the boluses were also identified and counted.
The cephalopod beaks were separated into upper and lower beaks, and the former
were only counted. The lower beaks were cleaned, counted and the lower rostral
length (LRL) measured, using a vernier calipers of 0.1 mm (Xavier and Cherel, 2009).
The lower beaks were identified, whenever possible, to the species level, according to
Xavier and Cherel (2009) and reference collections at the British Antarctic Survey and
at the University of Coimbra.
Allometric equations were used from LRL to estimate dorsal mantle length (ML, mm)
and the original wet body mass (M, g) published by Xavier and Cherel (2009). For
?Mastigotheuthis A (Clarke) it was used Mastigoteuthis psychrophila equations,
because it had no specific equations and both are the only species in the family
Mastigoteuthidae.
To describe the diets, cephalopod beaks that were not fresh (i.e. very darkened, with
abraded wings that were usually broken, and with their surfaces rounded) were
12
considered as having been captured before the time of study and thus were not
included in the analysis (Xavier et al, 2003c).
The analyses of cephalopod component in the three albatross species diet were made
using fresh lower beaks data, from which were inferred the frequency of occurrence (F;
number of samples with that squid species / total number of samples), total number of
lower beaks per cephalopod species (N), estimated mass (M; total, mean, standard
deviation (SD), and range – minima and maxima), estimated mantle lengths (ML; total,
mean, standard deviation (SD), and range – minima and maxima) and lower rostral
lengths (LRL; mean, standard deviation (SD), and range – minima and maxima; Xavier
et al, 2003b). It was also analyzed LRL, M and ML distributions using histograms with
the most important cephalopod species (Xavier et al, 2005).
Identification of different component weights in albatross species diet was presented by
the total percentage of each component by solid mass ± standard deviation (SD).
Finally, the role of scavenging in albatrosses was analyzed by identifying the
percentages of cephalopods heavier than 500g (Croxall and Prince 1994).
2.2 Isotopic analysis
The sample sources for the isotopic measurements were: i) for black-browed and grey-
headed albatrosses during the reproductive period, the chicks stomach contents
mentioned above and also adult boluses ; ii) for wandering albatrosses during
reproductive period, the stomach contents of chicks mentioned above and also
stomach contents from adults (that were collected during the same time period); and iii)
for black-browed and grey-headed albatrosses during the end of inter-breeding
period/beginning of the breeding period, the adult boluses mentioned above . As the
chicks eat what is given by adults, there is no problem of grouping the beaks from
these two types of sampling to analyze their stable isotopic signature.
The cephalopod lower beaks analyzed were cleaned and kept in a 70% ethanol
solution, being subsequently dried in an oven at 50 ° C for 6-24h, and reduced to fine
powder in order to homogenize the sample. Part of the homogenate was then
encapsulated (0.3-0.55mg) for analysis (Cherel and Hobson, 2005). Stable isotope
analyses were made only for cephalopod species with at least 6 lower beaks. There
were analyzed lower beaks of different sizes of Kondakovia longimana and
13
Psychroteuthis glacialis to see if the δ15N signature increases with beak size and if it
means they belonged to different squid populations, respectively.
The trophic level and habitat of the main cephalopod species in the diet of albatrosses
were obtained from the ratio of δ15N (15N/14N) and δ13C (13C/12C), respectively, through
a Continuous Flow Isotope Ratio Mass Spectrometer (CFIRMS). The results are
presented in δ connotation as deviations to the standard references in parts per
thousand (‰) according to the following equation: X = [(Rsample / Rstandard) -1] 1000,
where X represents 13C or 15N and Rsample the ratios 13C/12C or 15N/14N. Rstandard
represents the international reference standard V-PDB ("Vienna" - PeeDee formation)
and atmospheric N2 (AIR) for δ13C and δ15N, respectively (Dawson et al, 2002;
Stowasser et al, 2012).
Since there is no study referring the isotopic values of ocean fronts near South
Georgia, especially from squid beaks data, the isotopic position of the ocean fronts
presented here was based on Jaeger et al (2010) for Crozet island.
A total of 14 species of cephalopods were analyzed for stable isotopes in order to
understand their habitat use (13 C) and trophic level (15 N); 9 species from black-browed
albatrosses diet (out of total 5 cephalopod species presented in fresh lower beaks data
(FLBD) and 4 species from non-fresh lower beaks data (NFLBD)); 13 species from
grey-headed albatrosses diet (out of total 9 cephalopod species presented in FLBD
and 4 species from NFLBD); and 9 species from wandering albatrosses diets (out of
total 8 cephalopod species presented in FLBD and 1 specie from NFLBD; beaks from
the same specie with different sizes were counted only once; see below).
2.3 Statistical analysis
One-way ANOVA or Kruskal-Wallis (p-value<0.05) were used to examine whether
there were any significant differences among the LRL, M, ML and isotopic values in
each albatross and cephalopod species. Tukey´s test was subsequently used (p-
value<0.05). The data were analysed using Statistica version 10 and Sigmaplot 12.0.
14
3. Results and Discussion
3.1 Black-browed albatross
3.1.1 Reproductive period
Black-browed albatrosses fed mainly, by solid mass, on fish (54 ± 36.7%), followed by
cephalopods (35 ± 35.1%), crustaceans (7 ± 25.6%) and others contents (4 ± 8.4%).
Within the cephalopod component, based on fresh lower beaks identification, the
diversity found in stomach contents comprised 6 squid species (Table 1). The most
important cephalopod species found were Kondakovia longimana (F=26.7%, N=26.8%,
M=51.7%), Moroteuthis knipovitchi (F=36.7%, N=34.1%, M=33.5%) and Galiteuthis
glacialis (F=26.7%, N=30.5%, M=7.1%; Table 2).
Table 2 – Cephalopod component (lower beaks) in the diet of black-browed albatrosses during the reproductive period and during the end of inter-breeding/beginning of breeding period (EIBB/BB). Abbreviations: frequency of occurrence (F); total number of lower beaks (N); estimated mass (M); estimated dorsal mantle length (ML) and lower rostral length (LRL). SD= standard deviation. Only those prey species that represented F or N ≥ 20%, M ≥ 5% or had the minimums and/or the maximums in the studied variables were included.
Batoteuthidae 3,3 1,2 0,1 35,5 172,7 4,1
Cranchiidae 26,7 30,5 7,1 100,7 ± 13,1 447,4 ± 26,2 5,3 ± 0,3
( 74,7 – 129,1 ) ( 392,1 – 501,0 ) ( 4,6 – 5,9 )
Neoteuthidae 10,0 6,1 6,5 460,7 ± 366,2 167,8 ± 55,6 4,9 ± 1,6
( 95,6 – 965,3 ) ( 104,2 – 233,6 ) ( 3,1 – 6,8 )
Onychoteuthidae 26,7 26,8 51,7 836,0 ± 783,6 305,9 ± 84,9 8,8 ± 2,3
( 153,7 – 3193,4 ) ( 182,9 – 515,0 ) ( 5,5 – 14,4 )
36,7 34,1 33,5 425,2 ± 114,1 278,8 ± 27,4 6,2 ± 0,4
( 268,7 – 671,5 ) ( 237,3 – 330,9 ) ( 5,5 – 7,0 )
Cranchiidae 7,1 20,0 1,0 102,0 450,7 5,3
Gonatidae 7,1 20,0 1,3 134,1 183,8 5,3
Onychoteuthidae 14,3 60,0 97,7 3343,2 ± 680,2 521,3 ± 35,5 14,6 ± 1,0
( 2666,9 – 4027,3 ) ( 485,2 – 556,1 ) ( 13,6 – 15,5 )
Alluroteuthis
antarcticus
Kondakovia
longimana
Moroteuthis
knipovitchi
Galiteuthis
glacialis
Gonatus
antarcticus
Kondakovia
longimana
Galiteuthis
glacialis
Batoteuthis
skolops
mean ± SD
(range)
Black-browed albatrosses during EIB/BB period
F
(%)
N
(%)
LRL (mm)
%Family
F
(%)
Cephalopod
Species
Family
M (g)
mean ± SD
(range)
N
(%)
LRL (mm)
Cephalopod
Species %mean ± SD
(range)
mean ± SD
(range)
ML (mm)
Black-browed albatrosses during reproductive period
mean ± SD
(range)
M (g)
mean ± SD
(range)
ML (mm)
15
The lower rostral lengths (LRL) ranged from 3.1 to 14.4 mm (Fig. 7a), while the
estimated mass (M) ranged from 35.5 to 3193.4 g (Fig. 8a) and estimated mantle
lengths (ML) ranged from 104.2 to 515.0 mm (Fig. 9a). The mean LRL ranged between
4.1 mm (Batoteuthis skolops) and 8.8 ± 2.3 mm (Kondakovia longimana; Table 2).
Mean M ranged between 35.5 g (Batoteuthis skolops) and 836 ± 783.6 g (Kondakovia
longimana; Table 2), and mean ML ranged between 167.8 ± 55.6 mm (Alluroteuthis
antarcticus) and 447.4 ± 26.2 mm (Galiteuthis glacialis; Table 2).
In terms of carbon signatures, squid lower beaks ranged from -25.44‰ (large beaks
from Psychroteuthis glacialis) to -20.97‰ (Histioteuthis eltaninae; Fig. 10a), comprising
8 cephalopod species (out of total 5 cephalopod species presented in fresh lower
beaks data and 3 species from non-fresh lower beaks data). The number of squid
species from “Antarctic” and “sub-Antarctic” waters were 7 and 3, respectively (Fig.
10a) and the number of lower beaks per water masses were 70% and 30% (Table 3),
respectively.
Table 3 – Number of cephalopod lower beaks (used in isotopic analyses) per water mass in the diet of black-browed (Thalassarche melanophrys), grey-headed (Thalassarche chrysostoma) and wandering albatrosses (Diomedea exulans) during the reproductive period and for black-browed and grey-headed albatrosses during the end of inter-breeding/beginning of breeding period (EIB/BB).
Antarctic SubAntarctic Subtropical
Thalassarche melanophrys Reproductive 70,0 30,0 -
Thalassarche melanophrys EIB/BB 23,8 76,2 -
Thalassarche chrysostoma Reproductive 83,0 17,0 -
Thalassarche chrysostoma EIB/BB 36,6 63,4 -
Diomedea exulans Reproductive 32,7 59,4 7,9
Albatross species Period Number of lower beaks per water
masses (%)
In terms of nitrogen signatures, squid lower beaks ranged from 2.45‰ (Martialia
hyadesi) to 10.44‰ (Gonatus antarcticus; Fig. 11a).
Regarding the scavenging behaviour, a total of 31.7% of cephalopods was potentially
scavenged by black-browed albatrosses (assuming squid heavier than 500 g were
scavenged), corresponding to 64.8% of the total estimated mass of cephalopods
consumed.
16
3.1.2 At the end of inter-breeding/beginning of breeding period
(EIB/BB)
The cephalopod diversity found in boluses comprised 3 squid species (based on fresh
lower beaks identification; Table 1), and the most important one found was Kondakovia
longimana (F=14.3%, N=60%, M=97.7%; Table 2).
Lower rostral lengths (LRL) ranged from 5.3 to 15.5 mm (Fig. 7b), estimated mass (M)
ranged from 102 to 4027.3 g (Fig. 8b) and estimated mantle lengths (ML) ranged from
183.8 to 556.1 mm (Fig. 9b).
The mean LRL of the cephalopod species ranged between 5.3 mm (Galiteuthis
glacialis and Gonatus antarcticus) and 14.6 ± 1 mm (Kondakovia longimana; Table 2).
Mean M ranged between 102 g (Galiteuthis glacialis) and 3343.2 ± 680.2 g
(Kondakovia longimana; Table 2), and mean ML ranged between 183.8 mm (Gonatus
antarcticus) and 521.3 ± 35.5 mm (Kondakovia longimana; Table 2).
In terms of carbon signatures, squid lower beaks ranged from -23.73‰ (Galiteuthis
glacialis) to -21.24‰ (Moroteuthis knipovitchi; Fig. 10b),comprising 5 cephalopod
species (out of total 3 cephalopod species presented in fresh lower beaks data and 2
species from non-fresh lower beaks data). The number of squid species from
“Antarctic” and “sub-Antarctic” waters were 1 and 4, respectively (Fig. 10b), and the
number of lower beaks per water masses were 23.8% and 76.2% (Table 5),
respectively.
In terms of nitrogen signatures, squid lower beaks ranged from 8‰ (large beaks of
Kondakovia longimana) to 11.48‰ (Taonius sp. B (Voss); Fig. 11b).
Regarding the scavenging behaviour, a total of 60% of cephalopods was potentially
scavenged by black-browed albatrosses, corresponding to 97.7% of the total estimated
mass of cephalopods consumed.
17
Figure 7 – Number of lower beaks per consecutive and non-overlapping range of lower rostral length of the most important cephalopod species (i.e. frequency of occurrence or total number of lower beaks ≥ 20% or total estimated mass ≥ 5%; individualized) found in black-browed (BBA), gray-headed (GHA) and wandering albatrosses reproductive period and during the end of inter-breeding/beginning of breeding (EIBB/BB) period of BBA and GHA. “Others” include all cephalopod species that were not the principal squids in albatrosses diet.
18
Figure 8 – Number of lower beaks per consecutive and non-overlapping range of estimated mass of the most important cephalopod species (i.e. frequency of occurrence or total number of lower beaks ≥ 20% or total estimated mass ≥ 5%; individualized) found in black-browed (BBA), gray-headed (GHA) and wandering albatrosses reproductive period and during the end of inter-breeding/beginning of breeding (EIBB/BB) period of BBA and GHA. “Others” include all cephalopod species that were not the principal squids in albatrosses diet.
19
Figure 9 – Number of lower beaks per consecutive and non-overlapping range of estimated mantle length of the most important cephalopod species (i.e. frequency of occurrence or total number of lower beaks ≥ 20% or total estimated mass ≥ 5%; individualized) found in black-browed (BBA), gray-headed (GHA) and wandering albatrosses reproductive period and during the end of inter-breeding/beginning of breeding (EIBB/BB) period of BBA and GHA. “Others” include all cephalopod species that were not the principal squids in albatrosses diet.
20
Figure 10 - Stable carbon isotope values (δ13
C) of lower beaks from cephalopod species (with at least 6 lower beaks) found in: a) Black-browed albatrosses during reproductive period; b) Black-browed albatrosses during the end of inter-breeding/beginning of breeding (EIBB/BB) period; c) Gray-headed albatrosses during reproductive period; d) Gray-headed albatrosses during the EIBB/BB period; e) Wandering Albatross during reproductive period. Cephalopod species were deliberately placed according to their carbon signatures, and not in taxonomic order, to illustrate the water masses to which they belonged. Abbreviations: AZ, Antarctic Zone; PF, Polar Front; SAZ, Subantarctic Zone; STF, Subtropical Front; STZ, Subtropical Zone. Fronts carbon signatures were adopted following Jaeger et al. (2010) and are represented by dashed lines.
21
Figure 11 – Stable nitrogen isotope values (δ15
N) of lower beaks from cephalopod species (with at least 6 lower beaks) found in: a) Black-browed albatrosses during reproductive period; b) Black-browed albatrosses the end of inter-breeding/beginning of breeding (EIBB/BB) period; c) Gray-headed albatrosses during reproductive period; d) Gray-headed albatrosses during the EIBB/BB period; e) Wandering Albatross during reproductive period. Cephalopod species were deliberately placed in trophic sequence, and not in taxonomic order, according to their nitrogen signatures to illustrate the trophic structure of the community.
22
3.2 Grey-headed albatross
3.2.1 Reproductive period
Grey-headed albatrosses fed mainly, by solid mass, on cephalopods (51 ± 35.3%),
followed by fish (36 ± 32.5%), others contents (10 ± 22.9%) and crustaceans (4 ±
10.1%).
The cephalopod diversity found in stomach contents comprised 10 squid species
(based on fresh lower beaks identification; Table 1). The most important squid species
found were Kondakovia longimana (F=40%, N=8.9%, M=27.7%), Galiteuthis glacialis
(F=50%, N=50%, M=27.3%) and Martialia hyadesi (F=40%, N=20.3%, M=15%; Table
4).
Lower rostral lengths (LRL) ranged from 1.8 to 12.3 mm (Fig. 7c), estimated mass (M)
ranged from 35.5 to 1943 g (Fig. 8c) and estimated mantle lengths (ML) ranged from
72.2 to 492.6 mm (Fig. 9c). The mean LRL ranged between 3.4 ± 0.4mm (Histioteuthis
eltaninae) and 8.2 mm (Taonius sp. B (Voss); Table 4). Mean M ranged between 51.4
± 22.6 g (Chiroteuthis veranyi) and 620.3 ± 528.2 g (Kondakovia longimana; Table 4),
and mean ML ranged between 78.4 ± 10.7 mm (Histioteuthis eltaninae) and 491.4 mm
(Taonius sp. B (Voss); Table 4).
In terms of carbon signatures, squid lower beaks ranged from -25.36‰ (large beaks
from Psychroteuthis glacialis) to -19.99‰ (Chiroteuthis veranyi; Fig. 10c), comprising 9
species (out of total 8 cephalopod species presented in fresh lower beaks data and 1
species from non-fresh lower beaks data; beaks from the same specie with different
sizes were here counted only once). The number of squid species from “Antarctic” and
“sub-Antarctic” waters were 9 and 2, respectively (Fig. 10c), and the number of lower
beaks per water masses were 83% and 17% (Table 3), respectively.
In terms of nitrogen signatures, squid lower beaks ranged from 2.85‰ (Martialia
hyadesi) to 10.93‰ (Chiroteuthis veranyi; Fig. 11c).
In relation to scavenging, a total of 5.1% of cephalopods was potentially scavenged,
corresponding to 27% of the total estimated mass of cephalopods consumed.
23
Table 4 – Cephalopod component (lower beaks) in the diet of grey-headed albatrosses during the reproductive period and during the end of inter-breeding/beginning of breeding period (EIBB/BB). Abbreviations: frequency of occurrence (F); total number of lower beaks (N); estimated mass (M); estimated dorsal mantle length (ML) and lower rostral length (LRL). SD= standard deviation. Only those prey species that represented F or N ≥ 20%, M ≥ 5% or had extrema in the diets were included.
Cranchiidae 50,0 50,0 27,3 100,4 ± 12,8 446,8 ± 25,9 5,3 ± 0,3
( 71,1 – 124,3 ) ( 383,7 – 492,6 ) ( 4,5 – 5,8 )
3,3 0,6 0,8 220,1 491,4 8,2
Histioteuthidae 10,0 2,5 0,9 62,3 ± 27,7 78,4 ± 10,7 3,4 ± 0,4
( 46,9 – 103,7 ) ( 72,2 – 94,3 ) ( 3,1 – 4,0 )
Mastigoteuthidae 3,3 0,6 0,3 73,0 122,3 4,5
Ommastrephidae 40,0 20,3 15,0 156,1 ± 83,0 207,9 ± 29,3 3,6 ± 1,0
( 36,1 – 305,5 ) ( 155,0 – 255,2 ) ( 1,8 – 5,2 )
Onychoteuthidae 40,0 8,9 27,7 620,3 ± 528,2 277,3 ± 77,6 8,0 ± 2,1
( 172,0 – 1943,0 ) ( 190,4 – 436,7 ) ( 5,7 – 12,3 )
20,0 5,7 12,8 413,9 ± 263,5 267,8 ± 55,7 6,0 ± 0,9
( 201,7 – 964,4 ) ( 212,4 – 374,5 ) ( 5,1 – 7,7 )
Cranchiidae 3,1 28,6 4,6 257,8 ± 137,5 519,1 ± 134,7 8,7 ± 2,2
( 160,6 – 355,0 ) ( 423,9 – 614,3 ) ( 7,1 – 10,2 )
Onychoteuthidae 6,3 71,4 95,4 2135,0 ± 366,6 449,4 ± 26,2 12,6 ± 0,7
( 1704,8 – 2545,2 ) ( 418,0 – 477,7 ) ( 11,8 – 13,4 )
M (g)
%
N
(%)mean ± SD
(range)
M (g)
mean ± SD
(range)
ML (mm)
mean ± SD
(range)
F
(%)
LRL (mm)
mean ± SD
(range)
mean ± SD
(range)
Grey-headed albatrosses during reproductive period
F
(%)
N
(%)
LRL (mm)
mean ± SD
(range)
Grey-headed albatrosses during EIB/BB period
ML (mm)
Mastigoteuthis
psychrophila
Martialia
hyadesi
Kondakovia
longimana
Galiteuthis
glacialis
Taonius sp. B
(Voss)
Histioteuthis
eltaninae
Cephalopod
Species
Taonius sp. B
(Voss)
Kondakovia
longimana
Moroteuthis
knipovitchi
Family
Family Cephalopod
Species %
3.2.2 At the end of inter-breeding/beginning of breeding period
(EIB/BB)
During this period, the cephalopod diversity found in boluses comprised 2 squid
species (Table 1), and the most important one was Kondakovia longimana (F=6.3%,
N=71.4%, M=95.4%; Table 4).
Lower rostral lengths (LRL) ranged from 7.1 to 13.4 mm (Fig. 7d), estimated mass (M)
ranged from 160.6 to 2545.2 g (Fig. 8d) and estimated mantle lengths (ML) ranged
from 418 to 614.3 mm (Fig. 9d). The mean LRL ranged between 8.7 ± 2.2 mm
(Taonius sp. B (Voss)) and 12.6 ± 0.7 mm (Kondakovia longimana; Table 4). Mean M
ranged between 257.8 ± 137.5 g (Taonius sp. B (Voss)) and 2135 ± 366.6 g
(Kondakovia longimana; Table 4), and mean estimated mantle lengths ranged between
24
449.4 ± 26.2 mm (Kondakovia longimana) and 519.1 ± 134.7 mm (Taonius sp. B
(Voss); Table 4).
In terms of carbon signatures, squid lower beaks ranged from -23.84‰ (Batoteuthis
skolops) to -19.60‰ (Histioteuthis macrohista; Fig.10d), comprising 8 cephalopod
species (out of total 2 cephalopod species presented in fresh lower beaks data and 6
species from non-fresh lower beaks data). The amount of squid species that were from
“Antarctic” and “sub-Antarctic” waters were 3 and 5, respectively (Fig. 10d), and the
number of lower beaks per water masses were 36.6% and 63.4% (Table 3),
respectively.
In terms of nitrogen signatures, squid lower beaks ranged from 4.44‰ (Martialia
hyadesi) to 10.75‰ (Gonatus antarcticus; Fig. 11d).
In terms of scavenging, a total of 71.4% of cephalopods was potentially scavenged by
grey-headed albatrosses, corresponding to 95.4% of the total estimated mass of
cephalopods consumed.
3.3 Wandering albatross
3.3.1 Reproductive period
Wandering albatrosses fed mainly, by solid mass, on fish (37 ± 32.6%), cephalopods
(32 ± 34.6%) and others contents (31 ± 35.8%) followed by crustaceans (0 ± 0.2%).
The cephalopod diversity found in stomach contents comprised 15 squid species
based on fresh lower beaks identification (Table 1). The most important squid species
found were Kondakovia longimana (F=60%, N=28.5%, M=73.5%), Taonius sp. B
(Voss) (F=40%, N=24.6%, M=7.3%) and Galiteuthis glacialis (F=55%, N=18.5%
M=1.8%; Table 5).
25
Table 5 – Cephalopod component (lower beaks) in the diet of wandering albatrosses during the reproductive period. Abbreviations: frequency of occurrence (F); total number of lower beaks (N); estimated mass (M); estimated dorsal mantle length (ML) and lower rostral length (LRL). SD= standard deviation. Only those prey species that represented F or N ≥ 20%, M ≥ 5% or had extrema in the diets were included.
Brachioteuthidae 5,0 0,8 0,0 7,8 74,8 2,9
Cranchiidae 55,0 18,5 1,8 109,5 ± 15,4 464,4 ± 29,1 5,5 ± 0,3
( 78,3 – 144,0 ) ( 400,5 – 526,1 ) ( 4,7 – 6,2 )
40,0 24,6 7,3 331,7 ± 70,6 591,6 ± 61,2 9,8 ± 1,0
( 181,0 – 444,2 ) ( 448,4 – 681,9 ) ( 7,5 – 11,3 )
Histioteuthidae 5,0 0,8 0,0 57,0 77,1 3,3
Neoteuthidae 15,0 3,1 1,4 507,8 ± 159,8 185,5 ± 19,5 5,4 ± 0,6
( 367,9 – 735,4 ) ( 167,2 – 212,6 ) ( 4,9 – 6,2 )
Octopoteuthidae 10,0 2,3 6,9 3311,9 ± 1599,1 461,1 ± 167,7 13,5 ± 2,2
( 1520,5 – 4595,5 ) ( 270,5 – 586,4 ) ( 11,0 – 15,2 )
Ommastrephidae 5,0 0,8 0,2 305,5 255,2 5,2
Onychoteuthidae 60,0 28,5 73,5 2881,9 ± 1966,0 470,7 ± 116,1 13,2 ± 3,1
( 541,3 – 7524,8 ) ( 283,7 – 683,0 ) ( 8,2 – 18,9 )
25,0 6,9 2,8 456,2 ± 153,1 285,1 ± 32,9 6,3 ± 0,5
( 268,7 – 787,6 ) ( 237,3 – 349,6 ) ( 5,5 – 7,3 )
mean ± SD
(range)
M (g) ML (mm)
mean ± SD
(range)%
mean ± SD
(range)
F
(%)
N
(%)
Wandering albatrosses during reproductive period
LRL (mm)
Taonius sp. B
(Voss)
Kondakovia
longimana
Moroteuthis
knipovitchi
Cephalopod
Species
Histioteuthis
eltaninae
Alluroteuthis
antarcticus
Taningia
danae
Martialia
hyadesi
Slosarczykovia
circumantarctica
Galiteuthis
glacialis
Family
Lower rostral lengths (LRL) ranged from 2.9 to 18.9 mm (Fig. 7e), estimated mass (M)
ranged from 7.8 to 7524.8 g (Fig. 8e) and estimated mantle lengths (ML) ranged from
74.8 to 683 mm (Fig. 9e). The mean LRL ranged between 2.9 mm (Slosarczykovia
circumantarctica) and 13.5 ± 2.2 mm (Taningia danae; Table 5). The mean M ranged
between 7.8 g (Slosarczykovia circumantarctica) and 3311.9 ± 7779.7 g (Taningia
danae; Table 5), and the mean ML ranged between 74.8 mm (Slosarczykovia
circumantarctica) and 591.6 ± 61.2 mm (Taonius sp. B (Voss); Table 5).
In terms of carbon signatures, squid lower beaks ranged from -24.91‰ (large beaks
from Psychroteuthis glacialis) to -17.31‰ (Illex argentinus; Fig. 10e), comprising 9
cephalopod species (out of total 8 cephalopod species presented in fresh lower beaks
data and 1specie from non-fresh lower beaks data; beaks from the same specie with
different sizes were here counted only once). The number of squid species that were
from “Antarctic”, “sub-Antarctic” and “sub-Tropical” waters were 4, 6 and 1, respectively
(Fig. 10e), and the number of lower beaks per water masses were 32.7%, 59.4% and
7.9% (Table 3), respectively.
26
In terms of nitrogen signatures, squid lower beaks ranged from 6.19‰ (medium beaks
of Kondakovia longimana) to 12.18‰ (Taonius sp. B (Voss); Fig. 11e).
In terms of scavenging, a total of 35.4% of cephalopods was potentially scavenged by
wandering albatrosses, corresponding to 85.7% of the total estimated mass of
cephalopods consumed.
Only the wandering albatrosses showed interaction with fisheries by presenting a total
of 4 hooks and 8 lines (one of itch longline) in a total of 5 chicks stomach contests
(comprising all samples from August and one sample from July; which correspond to
25% of the total analyzed chick’s stomach contents from wandering albatross),
weighting this fishing gear a total of 30.2 g. Only one hook was associated to a fishing
line.
3.4 Characterization and comparison of the reproductive and
EIB/BB periods
Black-browed albatrosses during reproductive period fed mainly on fish (cephalopods
represented only 35 ± 35.1%), and showed the lowest cephalopod biodiversity of the
albatross species studied (with 6 species). Compared with previous studies, the year
2009 was similar to 1994, 1998 and 1999 where fish was the main diet component
(between 32 and 72.4%; Xavier et al, 2003b; Croxall et al. 1999).
Grey-headed albatrosses during reproductive period fed mostly on cephalopods (51 ±
35.3%), which could indicate that there were good oceanographic conditions around
and north of South Georgia and no needs to switch to alternative foraging grounds in
shelf and shelf-break waters around the Antarctic Peninsula. In fact, when conditions
are poor in the South Georgia region, breeding grey-headed albatrosses tend to switch
to alternative foraging grounds at the Antarctic Peninsula and this is accompanied by a
dietary shift towards increased consumption of krill, and less of the squid Martialia
hyadesi (Xavier et al. 2003b).
Wandering albatrosses during reproductive period fed mainly on fish and cephalopods
(fish and cephalopods represented 37 ± 32.6% and 32 ± 34.6%, respectively), like it
has been shown in previous studies (Rodhouse et al. 1987; Xavier et al, 2003c; Xavier
et al. 2004), and presented the highest cephalopod biodiversity (with 15 species) of the
three studied albatross species. Wandering albatrosses tended to feed on bigger
27
cephalopods than those recorded on other albatross species diets during their
reproductive period (see also Xavier and Croxall, 2007).
Compared to Xavier and Croxall (2007), wandering albatrosses during reproductive
period of 2009, showed similar scavenging percentages to those observed in 1989-
1999. On the other hand, black-browed albatrosses showed a higher percentage of
cephalopods scavenged in 2009 than in 2000 (almost reaching its double) but a similar
percentage of the total estimated mass of cephalopods consumed. Last, the grey-
headed albatrosses showed scavenging percentages lower in 2009 than those
recorded in 2000 (less than half 2000 percentages values). Summing up, these results
showed that, during the reproductive period of 2009, the wandering and black-browed
albatrosses mostly scavenge whereas grey-headed albatrosses feed more on live prey.
Moreover, during the end of interbreeding/beginning of breeding period, scavenging
could play an important role in the diet black-browed and grey-headed albatrosses, as
they showed higher than 60% of cephalopods potentially scavenged and more than
95% of the total estimated mass of cephalopods consumed. Black-browed and grey-
headed albatrosses tended to feed on squids of similar size to those found in
wandering albatross diet (Figs. 1, 2 and 3), and grey-headed squid prey were during
the reproductive period least heavier than those recorded on other albatrosses diets
and during its and black-browed albatross end of interbreeding/ beginning of breeding
period (Kruskal-Wallis, H = 94.2, P<0.01).
The number of cephalopod species found in grey-headed and black browed
albatrosses diets were higher during reproductive period than during the end of inter-
breeding period. The principal cephalopod species in albatrosses diet, chosen by their
importance by number and by mass, were K. longimana, G. glacialis, M. knipovitchi
and M. hyadesi during reproductive (Our results; Xavier et al, 2003b; Xavier et al,
2005) and K. longimana during the end of interbreeding/beginning of breeding period.
Only K. longimana, G.glacialis, G. antarcticus and T. sp.B (Voss) were recorded in both
sampled periods, which could suggest that those cephalopod species, specially
kondakovia longimana (the most important cephalopod species by mass in 2009), may
have an even greater role in marine ecosystems than previously thought, particularly in
the diet of albatrosses during the Antarctic winter.
28
According to Xavier et al (2011), to improve the assessment of the contribution of
different cephalopods to predator diets, lower and upper beaks should be studied at the
same time, because as the ratio of upper:lower beaks frequently differs from unity. This
was observed in the present study, specially during the end of inter-breeding/beginning
of breeding period for black-browed and grey-headed albatrosses. However, yet, it is
worth noting that there are fewer descriptions of upper beaks morphology and even
less allometric equations for estimating cephalopod mass based on upper beak
measurements.
3.5 Comparison between the main cephalopod species found in
albatross’ diets
The cephalopod beaks taken by the 3 studied albatross species during their
reproductive period were from species that had already been found in these
albatrosses diet, and were of similar size to those taken previously in other studies
(with species LRL means within ± 2 mm from the means recorded in the following
studies; Clarke et al. 1981; Rodhouse et al. 1987; Imber 1992; Xavier et al, 2003a,b
and c). The only cephalopod species that was outside these values was
Mesonychoteuthis hamiltoni in wandering albatrosses diet, due to one individual with a
LRL of 2.3mm which was outside the LRL range recorded in Xavier et al, 2003a.
The diversity of cephalopods recorded in this study, for all albatross species studied,
was lower than that recorded in previous years. There were no octopods found in their
diets during both periods. It could suggest that the studied albatross species spent
most of their time foraging over oceanic waters and less over neritic waters (where
octopods dominate the cephalopod fauna) and that the availability / abundance of less
common prey may have been lower during the sampled period and / or winds may
have changed, not allowing access to certain feeding sites where those species are
more probably found.
The four main cephalopod species found in the albatrosses diets were Kondakovia
longimana, Martialia hyadesi, Moroteuthis knipovitchi and Galiteuthis glacialis during
the reproductive period and K. longimana during the EIB/BB period. They were chosen
because of their importance by number and by mass, representing 54.6 - 91.5% of the
total fresh lower beaks found in the three albatrosses diets and 78.4 - 98.7% of the
total estimated mass found per albatross species.
29
3.5.1 Kondakovia longimana
The maximum estimated mass mean (3343.2 g) was found in black-browed
albatrosses at the end of inter-breeding/beginning of breeding period. Because it had
less than 5 individuals it was not compared with other albatross species and periods.
Squids found in wandering albatrosses diet in spite of presenting an estimated mass
mean of 2881.9 g had a large SD (1966.0) which includes the heaviest estimated
individual (with 7524.8 g). Because of that it was statistically different from other
breeders (Kruskal-Wallis, H = 36.5, P < 0.01). Squids found in grey-headed albatrosses
diet were heavier during the end of inter-breeding/beginning of breeding period than
those recorded during the reproductive period (Kruskal-Wallis, H = 36.5, P < 0.01).
Lower beaks number ranged from 3 in black-browed albatrosses (at the end of inter-
breeding/beginning of breeding period) to 37 in wandering albatrosses. Mean number
of squids per sample was only significantly different between grey-headed albatrosses
during reproductive period (1 squid per sample) and other breeders (3 squids per
sample, Kruskal-Wallis, H = 10.4, P =0.04).
3.5.2 Galiteuthis glacialis
The maximum estimated mass mean (109.5 g) was found in wandering albatrosses
and was statistically different from the minimum estimated mass (100.4 g) registered in
grey-headed albatrosses during reproductive period (ANOVA, F=4.4, P =0.01).
Because the data from black-browed albatrosses at the end of Inter-breeding/beginning
of breeding period had less than 5 samples with squids it was not compared with other
albatross species and periods.
Lower beaks number ranged from 1 in black-browed albatrosses (at the end of inter-
breeding/beginning of breeding period) to 79 lower beaks in grey-headed albatrosses
during reproductive period. Mean number of squids per sample ranged from 2 to 5
squids per sample with no differences among albatrosses (Kruskal-Wallis, H = 4.9, P
=0.18).
30
3.5.3 Moroteuthis knipovitchi
Its mean estimated mass ranged from 413.9 g in grey-headed albatrosses to 456.2 g in
wandering albatrosses, both during reproductive period, with no differences among
albatrosses (Kruskal-Wallis, H = 2.7, P =0.26).
Lower beaks number ranged from 9 in grey-headed and wandering albatrosses to 28
lower beaks in black-browed albatrosses, all during reproductive period. Mean number
of squids per sample ranged from 2 to 3 squids per sample with no differences among
albatrosses ( Kruskal-Wallis, H = 0.2, P =0.91).
3.5.4 Martialia hyadesi
Its mean estimated mass ranged from 156.1 g in grey-headed albatrosses to 305.5 g in
wandering albatrosses.
Lower beaks number ranged from 1 in wandering albatrosses to 32 lower beaks in
grey-headed albatrosses, all during reproductive period. There were not used in
comparisons the data from wandering albatrosses because it presented only one squid
sampled.
3.6 Cephalopods habitats and trophic levels
According to Cherel et Hobson (2007), there is a strong negative correlation between
latitude and 13C values, unlike 15N, which is strongly affected by predators’ feeding
ecology, with fish-eaters having higher 15N values than crustacean eaters. Yet, carbon
isotopic signatures of cephalopod beaks found in albatrosses diet only provides us
information about the water masses where cephalopods spent most of their time
foraging and eating but not from where they were caught by albatrosses. To know that,
satellite tracking devices and data loggers in albatrosses were needed, and a better
understanding of cephalopods migration patterns would be essential.
Since there is no study referring the isotopic values of ocean fronts near South
Georgia, especially from squid beaks data, the isotopic position of the ocean fronts
presented here was based on Jaeger et al (2010) for Crozet island, which may not
correspond exactly to South Georgia. In fact, South Georgia is surrounded by Atlantic
Ocean and not by Indic Ocean as Crozet, and its own geomorphology and ocean
31
currents may culminate in different habitats and trophic levels to cephalopods and its
preys.
3.6.1 Prey habitats
Based on the carbon signatures (13C) from cephalopod lower beaks in all albatross
species and periods studied, there were: i) four species that showed signatures from
Antarctic and Sub-Antarctic waters (A. antarcticus, K. longimana, G. antarcticus and G.
glacialis; see similar findings in Anderson et al, 2009; Cherel and Hobson, 2005; Cherel
et al, 2011; Stowasser et al, 2012); ii) two species that showed only signatures from
Antarctic waters (B. skolops, P. glacialis; see similar findings in Cherel and Hobson,
2005; Anderson et al, 2009); iii) four species that showed only signatures from Sub-
Antarctic waters (T. sp B (Voss), H. macrohista, H. atlantica, C. veranyi; see also
similar results in Cherel and Hobson, 2005; Cherel et al, 2011); iv) one species that
showed only signatures from subtropical waters (I. argentinus; Our results); and v)
three species known to be from Sub-Antarctic waters (Cherel and Hobson, 2005;
Cherel et al, 2011; Anderson et al, 2009) that also showed Antarctic signatures (M.
hyadesi, H. eltaninae, M. knipovitchi). The species Illex argentinus could had been
caught near the Patagonian shelf (South America, its geographical range) or near
South Georgia, because it is a common bait used by longliners (Catard et al. 2000).
Some species presented statistical differences on the carbon signatures among
albatrosses and periods. Small beaks of Psychroteuthis glacialis found in wandering
albatrosses diet had a carbon signature near polar front (-22.28‰) and were different
from other Psychroteuthis glacialis small and larger beaks, with more negative
signatures. Small beaks of Psychroteuthis glacialis found in grey-headed albatrosses
diet had a carbon signature of -24.11‰ and were different from the more negative
signatures showed by the large beaks of Psychroteuthis glacialis found in grey-headed
and black-browed albatrosses diet,(ANOVA, F=12.7, P < 0.01).Taonius sp. B (Voss)
presented no differences among albatrosses (ANOVA, F=2.3, P= 0.13). The Antarctic
and Sub-Antarctic waters signatures were significant different in Histioteuthis eltaninae
(ANOVA, F=9.5, P < 0.01), Gonatus antarcticus (only between wandering and grey-
headed albatrosses during reproductive period, ANOVA, F=3.4, P =0.018), Martialia
hyadesi (only between grey-headed albatrosses sampled periods, Kruskal-Wallis, H =
8.7, P =0.01), Galiteuthis glacialis (only among wandering albatrosses and other
albatrosses and periods, except for black-browed albatrosses at the end of inter-
breeding/beginning of breeding period, and between grey-headed albatrosses sampled
32
periods, ANOVA, F=7.62, P < 0.001) and Alluroteuthis antarcticus (Kruskal-Wallis, H =
19.5, P < 0.01).
3.6.2 Prey trophic levels
Based on the nitrogen signatures (15N) from cephalopod lower beaks in all albatross
species and periods studied, they could be grouped in four trophic levels. The only
squid species with nitrogen signatures ranging from 2.45 to 4.4‰ was Martialia
hyadesi. The only squid species with nitrogen signatures ranging from 6.19 to 6.63‰
was Kondakovia longimana (medium beaks), and no differences among albatross
species were observed (ANOVA, F=0.8, P=0.45). Squid species with nitrogen
signatures ranging from 7.15 to 8.83 ‰ were Histioteuthis eltaninae, Moroteuthis
knipovitchi, Kondakovia longimana (large beaks), Galiteuthis glacialis, Alluroteuthis
antarcticus and Psychroteuthis glacialis (both sizes). These signatures were significant
different in H. eltaninae (only between black-browed and grey-headed albatrosses
reproductive period, having the last a lower trophic level ,Kruskal-Wallis, H = 8.3, P =
0.02), G. glacialis (only among wandering albatrosses and the other two albatross
species during the reproductive period, showing the G. glacialis specimens found in
wandering albatrosses diet a higher trophic level than those recorded in the other two
albatross species diet, Kruskal-Wallis, H = 19, P < 0.01) and P. glacialis, which did not
change with size (only among small beaks of Psychroteuthis glacialis found in grey-
headed albatrosses diet and its and black-browed albatrosses large beaks, having the
last a higher trophic level, ANOVA, F=3.6, P = 0.01). Squid species with nitrogen
signatures from 9.02 to 12.18 ‰ were Gonatus antarcticus, Chiroteuthis veranyi, Illex
argentinus, Taonius sp. B (Voss), Histioteuthis macrohista, Histioteuthis atlantica and
Batoteuthis skolops. These signatures were significant different in Gonatus antarcticus
(only between wandering and grey-headed albatrosses reproductive periods, having
the last a lower trophic level, Kruskal-Wallis, H = 12.2, P = 0.01) and Taonius sp. B
(Voss) (only among grey-headed albatrosses at the end of inter-breeding/beginning of
breeding period and other albatrosses, having the lasts a higher trophic level, ANOVA,
F=10.6, P = 0.01).
The nitrogen signature values obtained for black-browed albatrosses during
reproductive period were significant lower than those obtained for grey-headed
albatrosses at the end of inter-breeding/beginning of breeding period (ANOVA, F=5.1,
P = 0.01).
33
In K. longimana there was enrichment in N15 with increasing beak size (medium beaks
of K. longimana found in wandering albatrosses diet had a nitrogen signature (6.19‰)
statistically different from the nitrogen signatures of the large beaks of K. longimana
found in wandering (7.63‰), grey-headed (during reproductive period; 7.66‰) and
black-browed (during EIB/BB period; 8‰) albatrosses; large beaks of K. longimana
found in black-browed albatross diet during EIB/BB period were also statistically
different from the medium beaks found in black-browed albatrosses diet during
reproductive period; 6.63‰; ANOVA, F=4.7, P < 0.01).
Regarding the nitrogen signatures (15N) from cephalopod lower beaks in all albatross
species and periods studied, it strongly suggests that cephalopods spread out in a
continuum between crustacean (such as M. hyadesi) and fish-eating species (such as
G. antarcticus; Cherel et al, 2011; Collins and Rodhouse, 2006). Indeed, the medium
δ15N value of G. antarcticus is higher (5.3‰) than that of M. hyadesi (2.45-4.4‰),
which had the lowest δ15N values of the community. However, nitrogen signatures from
2009 were lower to those recorded in 2001/2002 (Anderson et al, 2009), which could
indicated the presence of alternative trophic pathways (Stowasser et al, 2012). Due to
the possibly scarcity of krill in 2009, the well-known diatoms–krill–top predator food
chain could had shifted to a longer phytoplankton copepod-myctophid-higher predator
food chain (Tarling et al, 2012). Thus, cephalopods presented nitrogen signatures
lower than those usually recorded, because they fed on prey that normally occupy
lower trophic levels, and therefore, presented lower nitrogen signatures.
South Georgia community showed higher trophic levels than cephalopods community
of Kerguelen (more than 2 ‰ of difference for H. eltaninae, M. knipovitchi, K.
longimana, G. antarcticus and C. veranyi; Cherel et Hobson, 2005; Cherel et al, 2011),
which may be related to its strongest seasonal carbon uptake in the ice-free zone
(Jones et al, 2012).
3.7. Main threats and suggested measures to reinforce these
albatrosses conservation
The main threats faced by wandering albatross during the studied period were the
negative consequences that could had arising out of its proven interaction with fisheries
(fishing gear were found in its chicks stomach contents), possibly with patagonian
toothfish longlining (as one longline was found in its chicks stomach contents; and
34
patagonian toothfish individuals were found in its diet; unpublished data). The main
treaths found to black-browed albatross were a possible lower availability of krill in
South Georgia region, which could had stated an unsuccessful breeding year to this
albatross species (known to fed mainly on krill; and the negative consequences that
could had arising out of its possible interaction with icefish trawl fisheries (as icefish
individuals were found in its diet; unpublished data)). The main threat found to grey-
headed albatross was the almost absent of M. hyadesi in its diet, which could had
stated an unsuccessful breeding year to this albatross species.
The main cause of the decline of most albatross species is the fisheries-related by-
catch, especially in longline and trawling fisheries (Croxall et al., 1990; Nel et al. 2000;
Weimerskirch et al., 1997; Schiavini et al., 1998; Sullivan et al., 2003). As cephalopod
and fish components in the diet of the three studied albatross species were always
more important than the crustaceans component, it could indicate that in 2009, just like
suggested to the year of 1994, South Georgia region had lower availability of krill and
increased interspecific competition among krill predators (Croxall et al. 1999). Although
the three studied albatross species, which are krill predators (specially black-browed
albatross), do not normally compete against each other’s for krill due to their different
foraging areas, they seem to compete instead with other predators, such as gentoo
and macaroni penguins and Antarctic fur seals (Xavier et al, 2003b, Croxall et al.
1999). As black-browed albatrosses do not seem to change their main foraging area
(Antarctic waters) in years of low Antarctic prey availability (Xavier et al, 2003b), its
chick breeding success and adult survival could had been low in 2009 (Xavier et al,
2003b; Croxall et al. 1999). As M. hyadesi was almost absent in grey-headed albatross
diet (N=20.3%), and knowing that M. hyadesi consumption and grey-headed albatross
breeding success are correlated (Xavier et al, 2003b), its breeding success and
fledging success could had been low in 2009, as was observed in 1998 (N=14%;
Xavier et al, 2003b). The absence of known correlations between wandering
albatrosses diet and its chicks breeding success (Xavier et al, 2003a; Xavier et al,
2004) prevents to conclude anything about this subject.
So, the implementation of mitigation measures to reduce seabirds by-catch and an
effective combat to illegal, unreported and unregulated (IUU) fishing are crucial to
prevent these threats to albatrosses. Which allied with a better knowledge of southern
ocean cephalopods distributions and population trends could enables us to protect
them more efficiently as far as knowing and protecting albatrosses potentially feeding
35
zones during breeding and non-breeding periods. Other way passes by an ongoing
severe control of the rapidly krill fishery expansion while continue studying the
unfavorable climate conditions and its consequences in an increasing competition
environment for krill in the Southern Ocean.
4. Concluding Remarks
During the reproductive period, black-browed albatross fed mainly on fish, the grey-
headed albatross on cephalopods, and the wandering albatross on both preys. The
four main cephalopod species found in the albatrosses diets were Kondakovia
longimana, Martialia hyadesi, Moroteuthis knipovitchi and Galiteuthis glacialis during
the reproductive period. The highest cephalopod biodiversity was found in wandering
albatrosses diet during reproductive period, including larger prey than other albatross
species, mostly scavenged. Black-browed albatross during reproductive period was
also mainly scavenger, whereas grey-headed albatross fed more on live prey. For the
first time, black-browed and grey-headed albatrosses diets during the EIB/BB period
were analyzed. It was found that scavenging could play an important role in
albatrosses diet since their diets included cephalopods with weight and dimensions
characteristics of this type of food strategy. K. longimana was reported as the main
cephalopod species during the EIB/BB period. As only K. longimana, G.glacialis, G.
antarcticus and Taonius sp.B (Voss) were recorded in both sampled periods, it could
be suggested that those cephalopod species, especially K. longimana, may have an
even greater role in marine ecosystems than previously thought.
Regarding the ratio of δ13C (13C/12C) from cephalopod lower beaks, the main
cephalopod species found in the albatrosses diets presented signatures from Antarctic
and subantarctic waters. The species associated to the Antarctic waters were
Batoteuthis skolops and Psychroteuthis glacialis, associated to Subantarctic waters
were Chiroteuthis veranyi, Histioteuthis macrohista, Histioteuthis atlantica and Taonius
sp. B (Voss). Beyond these species, other cephalopods presented isotopic signatures
related to Antarctic and Subantarctic waters, which included Histioteuthis eltaninae,
Moroteuthis knipovitchi, Kondakovia longimana, Gonatus antarcticus, Martialia hyadesi,
Galiteuthis glacialis and Alluroteuthis antarcticus. Finally, the species Illex argentinus
presented a nitrogen signature related to subtropical waters although it is known to
occur in Patagonian shelf subantarctic waters.
36
Regarding the ratio of δ15N (15N / 14N) from cephalopod lower beaks, it was found that
the cephalopod species could be grouped into four different trophic levels. The squid
species with nitrogen signatures ranging from 2.45 to 4.4‰ was Martialia hyadesi. The
squid species with nitrogen signatures ranging from 6.19 to 6.63‰ was Kondakovia
longimana (medium beaks). The squid species with nitrogen signatures ranging from
7.15 to 8.83 ‰ were Histioteuthis eltaninae, Moroteuthis knipovitchi, Kondakovia
longimana (large beaks), Galiteuthis glacialis, Alluroteuthis antarcticus and
Psychroteuthis glacialis (both sizes). The squid species with nitrogen signatures from
9.02 to 12.18 ‰ were Gonatus antarcticus, Chiroteuthis veranyi, Illex argentinus,
Taonius sp. B (Voss), Histioteuthis macrohista, Histioteuthis atlantica and Batoteuthis
skolops. These nitrogen signatures strongly suggests that cephalopods spread out in a
continuum between cephalopods from lower trophic levels that feed on crustaceans (as
M. hyadesi) to higher trophic levels that feed on fish (as G. antarcticus). Cephalopod
lower beaks signatures were lower than those usually reported, which may indicate that
they fed on preys that usually occupy lower trophic levels.
The main threats to the albatross species were identified based on their diets and
included: i) the interaction with fisheries, ii) the possible low availability of krill at South
Georgia during the reproductive period of albatrosses, which affected mainly black-
browed albatrosses and iii) the absence of M. hyadesi in grey-headed albatrosses diet.
The main cause of the decline of most albatross species is the fisheries-related by-
catch, especially in longline and trawling fisheries. Wandering albatrosses diets
presented hooks and fishing lines, including a longline. The diets of wandering and
black-browed albatrosses included some target commercial fish species. The black-
browed albatrosses did not alter their hunting areas during periods of low prey
availability. A low availability of krill in these periods could induce a low reproductive
success, contributing to a population decline of these species. Data from grey-headed
albatrosses diet suggested that they might have faced a low reproductive success in
the studied period due to the almost absence of M. hyadesi.
Considering these threats, measures could be sugested to reinforce the conservation
of these albatrosses. Some actions are related to the ongoing actions such as: i)
implementation of mitigation measures to reduce the incidental catch of seabirds in
fishing fleets, ii ) combat of illegal, unreported and unregulated (IUU) fisheries, and iii)
control of the expansion of the industrial fishing of krill. Other actions concerns new
measures such as the protection of potential feeding areas for the albatrosses during
37
the reproductive and non-reproductive periods. The knowledge of the distribution and
population trends of the main cephalopod species caught by the three albatross
species will contribute to the identification of albatrosses potential feeding areas.
Future work should be focused on: i) increasing the knowledge of black-browed and
grey-headed albatrosses diet during the non-breeding period, to reinforce the remarks
of this study, ii) sampling wandering albatrosses diet during the non-breeding period to
compare with black-browed and grey-headed albatrosses; and iii) comparing the diet
with telemetry data and monitoring the chicks welfare to confirm the adults foraging
areas and its reproductive success.
38
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Appendices
Appendix 1 – Allometric equations from squids lower rostral length (LRL), to estimate its dorsal
mantle length (ML, mm) and the original wet body mass (M, g) published by Xavier and Cherel
(2009). References for each allometric equation are inside brackets.
Family Cephalopod Species
Batoteuthidae
Brachioteuthidae
Chiroteuthidae
Cranchiidae
Gonatidae
Histioteuthidae
Mastigoteuthidae
Neoteuthidae
Octopoteuthidae
Onychoteuthidae
Psychroteuthidae
* used Mastigoteuthis psychrophila because it had no specific equations and both species belong to the same family.
ML=94.424+6.203LRL ; log M=0.701+1.779logLRL
ML= 102.0+29.47LRL ; ln M=2.405+2.012 ln LRL (Rodhouse & Yeatman 1990)
ML=-556.9+75.22LRL; ln M=-0.874+3.42ln LRL (Clarke 1986)
ML=-4.301+34.99LRL ; ln M=1.229+2.944ln LRL (Piatkowski et al. 2001)
(British Antarctic Survey, unpublished data)
Males: ML= 98.59+24.40LRL; females: ML=-27.84+44.63LRL
equations for males and females (Jackson 1995):
It is provided the mean value between estimates obtained using
ML=-22.348+37.318LRL ; M=0.713LRL3.152
(Brown & Klages 1987)
ML=-12.3+61.43LRL (Rodhouse et al. 1990);
ML=6.676+83.785LRL; log M= 0.415+2.20 log LRL (Lu & Williams 1994)
based on Chiroteuthis spp. formulas
ML=11.4+24.46LRL ; ln M=-0.241+2.7 ln LRL (Clarke 1986),
ln M = 0.3422+2.1380lnLRL+0.2214lnLRL3 (Gröger et al. 2000)
ML= 50.6895LRL-8.6008LRL2+1.0823LRL
3-8.7019;
ML=-105.707+62.369LRL; ln M=-0.881+3.798lnLRL (Cherel, unpublished data)
Males: logM= 1.22+1.80logLRL; females: logM= 0.15+3.25logLRL
ML=11.4+24.46LRL; ln M=-0.241+2.7ln LRL (Clarke 1986),
(British Antarctic Survey, unpublished data)
ML=94.424+6.203LRL ; log M=0.701+1.779logLRL
ML=-3.65+24.48LRL; ln M= 0.33+3.11lnLRL (Lu & Ickeringill 2002)
based on Gonatus spp. formulas
ML=-43.4+42.87LRL ; ln M=-0.655+3.33ln LRL (Clarke 1986),
based on Taonius spp. formulas
ML=-12.3+61.43LRL ; ln M=0.786+2.19 ln LRL (Rodhouse et al. 1990),
M=ln 3.24 + 2.80ln LRL (Clarke 1962b)
Moroteuthis ingens
Psychroteuthis glacialis
Allometric Equations
for the species of the family Brachioteuthidae
ML= 16.31+20.18LRL ; ln M=0.55+1.41ln LRL (Clarke 1986),
based on Chiroteuthis spp. formulas
Martialia hyadesi
Kondakovia longimana
Moroteuthis knipovitchi
Gonatus antarcticus
Histioteuthis eltaninae
?Mastigoteuthis A
(Clarke)*
Mastigoteuthis
psychrophila
Alluroteuthis antarcticus
Taningia danae
Batoteuthis skolops
Slosarczykovia
circumantarctica
Chiroteuthis veranyi
Galiteuthis glacialis
Mesonychoteuthis
hamiltoni
Taonius sp. B (Voss)
46
Batoteuthidae 3,3 1,2 0,1 35,5 172,7 4,1
Cranchiidae 26,7 30,5 7,1 100,7 ± 13,1 447,4 ± 26,2 5,3 ± 0,3
( 74,7 – 129,1 ) ( 392,1 – 501,0 ) ( 4,6 – 5,9 )
Gonatidae 3,3 1,2 1,2 426,1 278,1 7,5
Neoteuthidae 10,0 6,1 6,5 460,7 ± 366,2 167,8 ± 55,6 4,9 ± 1,6
( 95,6 – 965,3 ) ( 104,2 – 233,6 ) ( 3,1 – 6,8 )
Onychoteuthidae 26,7 26,8 51,7 836,0 ± 783,6 305,9 ± 84,9 8,8 ± 2,3
( 153,7 – 3193,4 ) ( 182,9 – 515,0 ) ( 5,5 – 14,4 )
36,7 34,1 33,5 425,2 ± 114,1 278,8 ± 27,4 6,2 ± 0,4
( 268,7 – 671,5 ) ( 237,3 – 330,9 ) ( 5,5 – 7,0 )
Black-browed albatrosses during reproductive period
Family
Kondakovia
longimana
Moroteuthis
knipovitchi
Alluroteuthis
antarcticus
Gonatus
antarcticus
Cephalopod
Speciesmean ± SD
(range)
mean ± SD
(range)
Galiteuthis
glacialis
Batoteuthis
skolops
F
(%)
N
(%)
M (g) ML (mm) LRL (mm)
%mean ± SD
(range)
Appendix 2 – Cephalopod component (lower beaks) in the diet of black-browed albatrosses
during the reproductive period. Abbreviations: frequency of occurrence (F); total number of
lower beaks (N); estimated mass (M); estimated dorsal mantle length (ML) and lower rostral
length (LRL). SD= standard deviation.
47
Chiroteuthidae 6,7 1,3 0,4 51,4 ± 22,6 125,1 ± 19,0 4,7 ± 0,8
( 35,5 – 67,4 ) ( 111,7 – 138,6 ) ( 4,1 – 5,2 )
Cranchiidae 50,0 50,0 27,3 100,4 ± 12,8 446,8 ± 25,9 5,3 ± 0,3
( 71,1 – 124,3 ) ( 383,7 – 492,6 ) ( 4,5 – 5,8 )
3,3 0,6 0,8 220,1 491,4 8,2
Gonatidae 20,0 5,7 8,1 260,3 ± 120,6 228,1 ± 39,5 6,3 ± 0,9
( 103,3 – 445,3 ) ( 166,7 – 282,4 ) ( 4,9 – 7,6 )
Histioteuthidae 10,0 2,5 0,9 62,3 ± 27,7 78,4 ± 10,7 3,4 ± 0,4
( 46,9 – 103,7 ) ( 72,2 – 94,3 ) ( 3,1 – 4,0 )
Mastigoteuthidae 3,3 0,6 0,3 73,0 122,3 4,5
Ommastrephidae 40,0 20,3 15,0 156,1 ± 83,0 207,9 ± 29,3 3,6 ± 1,0
( 36,1 – 305,5 ) ( 155,0 – 255,2 ) ( 1,8 – 5,2 )
Onychoteuthidae 40,0 8,9 27,7 620,3 ± 528,2 277,3 ± 77,6 8,0 ± 2,1
( 172,0 – 1943,0 ) ( 190,4 – 436,7 ) ( 5,7 – 12,3 )
20,0 5,7 12,8 413,9 ± 263,5 267,8 ± 55,7 6,0 ± 0,9
( 201,7 – 964,4 ) ( 212,4 – 374,5 ) ( 5,1 – 7,7 )
Psychroteuthidae 13,3 4,4 6,8 283,2 ± 166,5 268,4 ± 110,7 6,4 ± 1,6
( 101,3 – 461,3 ) ( 147,8 – 388,6 ) ( 4,6 – 7,9 )
Grey-headed albatrosses during reproductive period
Martialia
hyadesi
Kondakovia
longimana
Moroteuthis
knipovitchi
Psychroteuthis
glacialis
Taonius sp. B
(Voss)
Gonatus
antarcticus
Family Cephalopod
Speciesmean ± SD
(range)
mean ± SD
(range)
ML (mm) LRL (mm)
%
N
(%)
M (g)F
(%) mean ± SD
(range)
Histioteuthis
eltaninae
Mastigoteuthis
psychrophila
Chiroteuthis
veranyi
Galiteuthis
glacialis
Appendix 3 – Cephalopod component (lower beaks) in the diet of gray-headed albatrosses
during the reproductive period. Abbreviations: frequency of occurrence (F); total number of
lower beaks (N); estimated mass (M); estimated dorsal mantle length (ML) and lower rostral
length (LRL). SD= standard deviation.
48
Brachioteuthidae 5,0 0,8 0,0 7,8 74,8 2,9
Chiroteuthidae 5,0 0,8 0,0 60,6 133,7 5,0
Cranchiidae 55,0 18,5 1,8 109,5 ± 15,4 464,4 ± 29,1 5,5 ± 0,3
( 78,3 – 144,0 ) ( 400,5 – 526,1 ) ( 4,7 – 6,2 )
10,0 1,5 2,5 1800,4 ± 2498,9 433,1 ± 430,0 7,3 ± 7,0
( 33,4 – 3567,4 ) ( 129,0 – 737,1 ) ( 2,3 – 12,2 )
40,0 24,6 7,3 331,7 ± 70,6 591,6 ± 61,2 9,8 ± 1,0
( 181,0 – 444,2 ) ( 448,4 – 681,9 ) ( 7,5 – 11,3 )
Gonatidae 40,0 8,5 2,2 287,6 ± 111,1 238,4 ± 32,5 6,6 ± 0,8
( 170,8 – 485,5 ) ( 201,0 – 291,0 ) ( 5,7 – 7,8 )
Histioteuthidae 5,0 0,8 0,0 57,0 77,1 3,3
Mastigoteuthidae 10,0 1,5 0,2 140,9 ± 27,2 134,7 ± 4,4 6,5 ± 0,7
( 121,7 – 160,1 ) ( 131,6 – 137,8 ) ( 6,0 – 7,0 )
Neoteuthidae 15,0 3,1 1,4 507,8 ± 159,8 185,5 ± 19,5 5,4 ± 0,6
( 367,9 – 735,4 ) ( 167,2 – 212,6 ) ( 4,9 – 6,2 )
Octopoteuthidae 10,0 2,3 6,9 3311,9 ± 1599,1 461,1 ± 167,7 13,5 ± 2,2
( 1520,5 – 4595,5 ) ( 270,5 – 586,4 ) ( 11,0 – 15,2 )
Ommastrephidae 5,0 0,8 0,2 305,5 255,2 5,2
Onychoteuthidae 60,0 28,5 73,5 2881,9 ± 1966,0 470,7 ± 116,1 13,2 ± 3,1
( 541,3 – 7524,8 ) ( 283,7 – 683,0 ) ( 8,2 – 18,9 )
5,0 0,8 1,0 1495,5 359,8 9,4
25,0 6,9 2,8 456,2 ± 153,1 285,1 ± 32,9 6,3 ± 0,5
( 268,7 – 787,6 ) ( 237,3 – 349,6 ) ( 5,5 – 7,3 )
Psychroteuthidae 5,0 0,8 0,1 107,6 151,9 4,7
Kondakovia
longimana
Moroteuthis
ingens
Moroteuthis
knipovitchi
Psychroteuthis
glacialis
Wandering albatrosses during reproductive period
Martialia
hyadesi
?Mastigoteuthis A
(Clarke)
Alluroteuthis
antarcticus
Taningia
danae
Galiteuthis
glacialis
Mesonychoteuthis
hamiltoni
Taonius sp. B
(Voss)
Gonatus
antarcticus
Histioteuthis
eltaninae
Chiroteuthis
veranyi
Family Cephalopod
Species
Slosarczykovia
circumantarctica
mean ± SD
(range)
mean ± SD
(range)
ML (mm) LRL (mm)F
(%)
N
(%) %
M (g)
mean ± SD
(range)
Appendix 4 – Cephalopod component (lower beaks) in the diet of wandering albatrosses during
the reproductive period. Abbreviations: frequency of occurrence (F); total number of lower
beaks (N); estimated mass (M); estimated dorsal mantle length (ML) and lower rostral length
(LRL). SD= standard deviation.
49
Cranchiidae 10 4,94 ± 0,30 46,38 ± 2,02 13,59 ± 0,84 -23,76 ± 0,99 8,02 ± 1,05
( 4,50 – 5,50 ) ( 42,64 – 48,09 ) ( 11,82 – 14,64 ) ( -25,15 – -21,96 ) ( 6,29 – 9,92 )
Gonatidae 10 6,31 ± 0,72 46,32 ± 2,43 14,26 ± 0,85 -22,43 ± 1,64 10,44 ± 0,53
( 5,00 – 7,00 ) ( 41,43 – 48,53 ) ( 12,62 – 15,19 ) ( -24,26 – -19,05 ) ( 9,62 – 11,32 )
Histioteuthidae 10 3,44 ± 0,30 47,05 ± 1,71 14,37 ± 0,65 -20,97 ± 1,14 8,69 ± 1,07
( 3,20 – 4,20 ) ( 43,42 – 48,40 ) ( 13,05 – 15,02 ) ( -23,12 – -19,09 ) ( 7,61 – 10,47 )
Neoteuthidae 10 5,84 ± 0,53 47,33 ± 0,89 14,23 ± 0,40 -24,55 ± 1,00 8,39 ± 0,53
( 4,80 – 6,70 ) ( 46,05 – 48,38 ) ( 13,42 – 14,72 ) ( -25,93 – -23,00 ) ( 7,63 – 9,54 )
10 4,33 ± 0,79 49,44 ± 1,11 14,05 ± 0,44 -23,14 ± 0,40 2,45 ± 1,06
( 3,00 – 5,80 ) ( 47,36 – 50,65 ) ( 13,39 – 14,61 ) ( -23,90 – -22,54 ) ( 0,14 – 3,62 )
Onychoteuthidae Kondakovia longimana 10 8,20 ± 1,77 50,16 ± 0,90 15,37 ± 0,52 -21,87 ± 1,68 6,63 ± 0,79
(Medium beaks) ( 5,60 – 12,30 ) ( 48,30 – 51,42 ) ( 14,37 – 16,11 ) ( -24,78 – -19,42 ) ( 4,69 – 7,73 )
10 12,10 ± 1,21 50,19 ± 0,69 15,23 ± 0,23 -23,28 ± 1,15 7,25 ± 0,70
( 10,40 – 14,30 ) ( 49,22 – 51,83 ) ( 14,70 – 15,53 ) ( -25,24 – -21,55 ) ( 6,03 – 8,31 )
10 5,98 ± 0,30 50,41 ± 1,07 15,39 ± 0,49 -21,12 ± 0,98 8,70 ± 0,44
( 5,60 – 6,40 ) ( 47,91 – 52,17 ) ( 14,68 – 16,26 ) ( -22,82 – -20,03 ) ( 7,77 – 9,32 )
Psychroteuthidae Psychroteuthis glacialis 9 4,42 ± 0,16 50,55 ± 0,81 14,33 ± 0,29 -24,58 ± 1,32 8,30 ± 0,51
( Small beaks)( 4,10 – 4,70 ) ( 49,12 – 51,68 ) ( 13,78 – 14,74 ) ( -25,96 – -21,70 ) ( 7,25 – 8,93 )
10 7,18 ± 0,61 50,02 ± 0,76 14,36 ± 0,30 -25,44 ± 0,80 8,46 ± 0,54
( 6,40 – 8,30 ) ( 48,68 – 51,23 ) ( 13,90 – 14,83 ) ( -26,33 – -23,96 ) ( 7,41 – 9,30 )
Family
Black-browed albatrosses during reproductive period
n
LRL (mm) % C %N δ13 C (‰ ) δ15N (‰ )
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
(Large beaks)
Cephalopod Species
Galiteuthis glacialis
Martialia hyadesi
(Large beaks)
Moroteuthis knipovitchi
Alluroteuthis antarcticus
Gonatus antarcticus
Histioteuthis eltaninae
Appendix 5 – δ13
C and 15
N signatures, lower rostral length (LRL), carbon (C) and nitrogen (N) percentages of lower beaks from cephalopod species (with at
least 6 lower beaks) found in black-browed albatrosses during reproductive period. SD= standard deviation.
50
Appendix 6 – δ13
C and 15
N signatures, lower rostral length (LRL), carbon (C) and nitrogen (N) percentages of lower beaks from cephalopod species (with at
least 6 lower beaks) found in black-browed albatrosses during the end of inter-breeding/beginning of breeding period (EIB/BB). SD= standard deviation.
Cranchiidae Galiteuthis glacialis 10 5,21 ± 0,37 46,10 ± 1,65 13,95 ± 0,68 -23,73 ± 1,50 8,36 ± 0,92
( 4,60 – 5,80 ) ( 42,66 – 47,25 ) ( 12,72 – 14,61 ) ( -26,62 – -21,94 ) ( 6,59 – 9,94 )
Taonius sp. B (Voss) 6 8,33 ± 1,08 46,84 ± 1,97 14,32 ± 0,67 -21,39 ± 0,90 11,48 ± 0,61
( 7,30 – 10,20 ) ( 42,86 – 47,86 ) ( 13,08 – 15,09 ) ( -22,68 – -20,39 ) ( 10,84 – 12,32 )
Gonatidae Gonatus antarcticus 6 6,42 ± 0,69 47,73 ± 0,31 14,78 ± 0,34 -21,42 ± 2,76 11,09 ± 1,14
( 5,20 – 7,00 ) ( 47,23 – 48,10 ) ( 14,28 – 15,21 ) ( -24,67 – -18,33 ) ( 9,53 – 12,10 )
Onychoteuthidae Kondakovia longimana 10 13,61 ± 2,31 48,35 ± 0,69 15,17 ± 0,34 -21,85 ± 1,53 8,00 ± 0,82
(Large beaks) ( 11,40 – 19,00 ) ( 46,71 – 48,84 ) ( 14,67 – 15,63 ) ( -24,83 – -19,60 ) ( 6,53 – 9,16 )
Moroteuthis knipovitchi 10 5,81 ± 0,26 51,17 ± 8,96 15,09 ± 3,00 -21,24 ± 1,04 8,82 ± 0,76
( 5,30 – 6,20 ) ( 42,12 – 75,44 ) ( 12,02 – 23,32 ) ( -23,03 – -19,82 ) ( 7,76 – 9,97 )
mean ± SD
(range)
n
Black-browed albatrosses during EIB/BB period
Family Cephalopod Species mean ± SD
(range)
LRL (mm) % C %N δ13 C (‰ ) δ15N (‰ )
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
51
Chiroteuthidae 7 4,59 ± 0,56 47,66 ± 0,21 14,68 ± 0,11 -19,99 ± 0,54 10,93 ± 0,40
( 4,00 – 5,30 ) ( 47,46 – 48,06 ) ( 47,46 – 14,79 ) ( -20,82 – -19,10 ) ( 10,28 – 11,40 )
Cranchiidae 10 4,89 ± 0,39 46,95 ± 0,93 13,80 ± 0,93 -24,45 ± 1,11 7,52 ± 0,65
( 4,30 – 5,50 ) ( 44,94 – 48,04 ) ( 12,10 – 14,90 ) ( -26,13 – -22,96 ) ( 6,52 – 8,56 )
Gonatidae 10 6,00 ± 0,76 47,96 ± 0,57 14,93 ± 0,36 -23,44 ± 1,36 10,07 ± 0,47
( 5,10 – 7,00 ) ( 46,62 – 48,55 ) ( 14,35 – 15,50 ) ( -25,15 – -21,43 ) ( 9,32 – 10,91 )
Histioteuthidae 10 3,18 ± 0,45 47,75 ± 0,69 14,80 ± 0,30 -22,88 ± 1,22 7,54 ± 0,45
( 2,40 – 3,90 ) ( 46,66 – 48,62 ) ( 14,30 – 15,08 ) ( -24,38 – -20,40 ) ( 6,87 – 8,19 )
Neoteuthidae 10 5,65 ± 0,62 47,71 ± 1,49 14,32 ± 0,42 -24,94 ± 0,90 7,83 ± 0,81
( 4,50 – 6,60 ) ( 44,27 – 49,01 ) ( 13,40 – 14,78 ) ( -26,10 – -22,92 ) ( 6,50 – 9,27 )
Ommastrephidae 10 4,14 ± 1,12 50,63 ± 0,53 13,59 ± 0,75 -22,67 ± 1,75 2,85 ± 2,04
( 2,30 – 5,60 ) ( 49,56 – 51,31 ) ( 12,38 – 14,67 ) ( -23,84 – -19,29 ) ( 0,86 – 7,03 )
Onychoteuthidae Kondakovia longimana 8 7,98 ± 1,56 50,63 ± 0,64 15,22 ± 0,46 -22,41 ± 1,65 6,73 ± 0,94
(Medium beaks) ( 5,10 – 10,10 ) ( 49,42 – 51,50 ) ( 14,20 – 15,66 ) ( -24,93 – -20,32 ) ( 4,82 – 8,07 )
10 11,42 ± 0,78 50,37 ± 0,46 15,26 ± 0,29 -22,77 ± 0,94 7,66 ± 0,77
( 10,50 – 13,10 ) ( 49,76 – 51,07 ) ( 14,80 – 15,80 ) ( -24,60 – -20,96 ) ( 6,67 – 8,71 )
10 5,84 ± 0,79 50,06 ± 1,41 14,68 ± 0,72 -21,70 ± 0,69 8,62 ± 0,43
( 5,00 – 7,50 ) ( 47,95 – 53,10 ) ( 13,16 – 15,92 ) ( -22,62 – -20,74 ) ( 7,83 – 9,16 )
Psychroteuthidae Psychroteuthis glacialis 10 4,50 ± 0,19 51,05 ± 0,74 14,50 ± 0,22 -24,11 ± 0,74 7,89 ± 0,52
( Small beaks)( 4,20 – 4,80 ) ( 49,98 – 52,31 ) ( 14,02 – 14,88 ) ( -25,00 – -22,51 ) ( 7,33 – 8,98 )
10 7,59 ± 0,31 50,14 ± 1,16 14,63 ± 0,26 -25,36 ± 0,71 8,64 ± 0,42
( 7,20 – 8,30 ) ( 47,36 – 51,58 ) ( 14,14 – 14,91 ) ( -26,41 – -24,56 ) ( 7,84 – 9,25 )
Family
Grey-headed albatrosses during reproductive period
n
LRL (mm) % C %N δ13 C (‰ ) δ15N (‰ )
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
Chiroteuthis veranyi
Galiteuthis glacialis
Gonatus antarcticus
Histioteuthis eltaninae
Alluroteuthis antarcticus
Martialia hyadesi
(Large beaks)
Moroteuthis knipovitchi
(Large beaks)
Cephalopod Species
Appendix 7 – δ13
C and 15
N signatures, lower rostral length (LRL), carbon (C) and nitrogen (N) percentages of lower beaks from cephalopod species (with at
least 6 lower beaks) found in gray-headed albatrosses during reproductive period. SD= standard deviation.
52
Appendix 8 – δ13
C and 15
N signatures, lower rostral length (LRL), carbon (C) and nitrogen (N) percentages of lower beaks from cephalopod species (with at
least 6 lower beaks) found in grey-headed albatrosses during the end of inter-breeding/beginning of breeding period (EIB/BB). SD= standard deviation.
Batoteuthidae Batoteuthis skolops 10 3,98 ± 0,23 47,95 ± 0,35 14,45 ± 0,21 -23,84 ± 0,43 9,02 ± 0,63
( 3,70 – 4,40 ) ( 47,39 – 48,37 ) ( 14,10 – 14,81 ) ( -24,63 – -23,14 ) ( 7,84 – 10,01 )
Cranchiidae Galiteuthis glacialis 6 5,15 ± 0,28 47,62 ± 0,27 14,78 ± 0,33 -22,06 ± 1,78 7,78 ± 1,51
( 4,60 – 5,30 ) ( 47,22 – 47,91 ) ( 14,36 – 15,35 ) ( -24,63 – -19,86 ) ( 6,44 – 10,29 )
Taonius sp. B (Voss) 4 8,43 ± 1,41 47,43 ± 0,49 14,31 ± 0,51 -21,89 ± 1,52 9,89 ± 1,02
( 7,20 – 10,20 ) ( 46,93 – 48,11 ) ( 13,89 – 15,04 ) ( -23,62 – -19,92 ) ( 8,88 – 11,30 )
Gonatidae Gonatus antarcticus 10 6,56 ± 0,58 51,72 ± 12,53 16,45 ± 4,07 -21,65 ± 1,68 10,75 ± 0,70
( 5,40 – 7,20 ) ( 44,04 – 87,14 ) ( 14,06 – 27,96 ) ( -24,15 – -19,71 ) ( 9,74 – 11,60 )
Histioteuthidae Histioteuthis atlantica 10 3,31 ± 0,51 48,10 ± 0,72 14,83 ± 0,40 -20,09 ± 0,43 9,33 ± 1,16
( 2,90 – 4,70 ) ( 46,66 – 48,78 ) ( 14,25 – 15,36 ) ( -21,10 – -19,59 ) ( 7,23 – 10,55 )
Histioteuthis macrohista 9 3,64 ± 0,25 48,19 ± 0,35 14,96 ± 0,33 -19,60 ± 0,31 10,24 ± 0,76
( 3,30 – 4,00 ) ( 47,47 – 48,63 ) ( 14,28 – 15,33 ) ( -20,14 – -19,13 ) ( 9,16 – 11,29 )
Ommastrephidae Martialia hyadesi 10 2,73 ± 0,37 48,15 ± 0,37 14,03 ± 0,19 -20,70 ± 1,06 4,44 ± 1,11
( 2,20 – 3,30 ) ( 47,27 – 48,57 ) ( 13,82 – 14,49 ) ( -23,61 – -19,70 ) ( 2,48 – 5,89 )
Onychoteuthidae Kondakovia longimana 10 11,29 ± 0,71 48,01 ± 0,23 15,11 ± 0,20 -22,82 ± 1,46 7,15 ± 0,90
(Large beaks) ( 10,20 – 12,10 ) ( 47,57 – 48,30 ) ( 14,74 – 15,41 ) ( -24,26 – -20,51 ) ( 6,08 – 8,61 )
Family Cephalopod Species
δ15N (‰ )
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
n
LRL (mm) % C %N δ13 C (‰ )
Grey-headed albatrosses during EIB/BB period
53
Cranchiidae 10 5,24 ± 0,37 48,33 ± 0,96 12,94 ± 0,57 -21,51 ± 1,56 8,13 ± 1,32
( 4,60 – 5,90 ) ( 46,93 – 50,05 ) ( 11,62 – 13,54 ) ( -23,88 – -19,31 ) ( 6,37 – 9,94 )
10 9,81 ± 0,82 45,38 ± 0,88 14,01 ± 0,21 -20,63 ± 0,96 12,18 ± 0,88
( 8,30 – 10,80 ) ( 44,05 – 46,60 ) ( 13,82 – 14,57 ) ( -21,75 – -19,09 ) ( 10,70 – 13,76 )
Gonatidae 10 6,88 ± 0,68 47,44 ± 2,58 14,29 ± 0,87 -20,50 ± 2,14 11,39 ± 1,01
( 5,50 – 7,80 ) ( 40,97 – 49,70 ) ( 12,23 – 15,33 ) ( -25,03 – -18,13 ) ( 9,29 – 12,78 )
Histioteuthidae 10 3,55 ± 0,22 57,31 ± 28,18 16,63 ± 8,40 -21,46 ± 0,58 7,89 ± 0,33
( 3,20 – 3,80 ) ( 47,71 – 137,50 ) ( 13,49 – 40,53 ) ( -22,51 – -20,59 ) ( 7,32 – 8,40 )
Neoteuthidae 10 5,24 ± 0,34 48,30 ± 1,34 13,75 ± 0,48 -20,95 ± 1,59 8,01 ± 1,02
( 4,70 – 5,70 ) ( 44,77 – 49,40 ) ( 12,93 – 14,26 ) ( -22,95 – -18,61 ) ( 6,95 – 9,42 )
Ommastrephidae 8 4,23 ± 0,76 49,77 ± 0,35 14,85 ± 0,38 -17,31 ± 0,58 10,10 ± 0,37
( 3,50 – 5,80 ) ( 49,23 – 50,31 ) ( 14,30 – 15,29 ) ( -18,18 – -16,36 ) ( 9,63 – 10,63 )
Onychoteuthidae Kondakovia longimana 8 8,79 ± 0,67 50,07 ± 0,63 15,14 ± 0,45 -22,88 ± 1,60 6,19 ± 1,00
(Medium beaks)( 8,10 – 10,00 ) ( 49,15 – 50,91 ) ( 14,24 – 15,82 ) ( -24,02 – -19,43 ) ( 5,27 – 8,16 )
10 13,07 ± 1,67 49,00 ± 1,10 14,79 ± 0,46 -21,71 ± 1,62 7,63 ± 0,86
( 11,30 – 17,10 ) ( 47,33 – 50,69 ) ( 13,89 – 15,44 ) ( -23,67 – -19,04 ) ( 6,14 – 8,84 )
10 6,02 ± 0,38 49,53 ± 1,29 14,95 ± 0,47 -22,32 ± 1,50 8,42 ± 0,60
( 5,20 – 6,50 ) ( 46,01 – 50,44 ) ( 13,77 – 15,43 ) ( -23,78 – -19,32 ) ( 7,89 – 9,85 )
Psychroteuthidae Psychroteuthis glacialis 7 4,59 ± 0,34 49,69 ± 0,54 13,95 ± 0,52 -22,28 ± 1,17 8,41 ± 0,53
( Small beaks)( 4,30 – 5,10 ) ( 49,20 – 50,50 ) ( 13,09 – 14,65 ) ( -23,94 – -21,04 ) ( 7,81 – 9,31 )
8 7,33 ± 0,35 49,57 ± 0,44 13,85 ± 0,22 -24,91 ± 0,68 8,83 ± 0,57
( 6,80 – 7,80 ) ( 48,88 – 50,23 ) ( 13,56 – 14,16 ) ( -25,89 – -24,19 ) ( 7,82 – 9,75 )
Wandering albatrosses during reproductive period
n
LRL (mm) % C %N δ13 C (‰ ) δ15N (‰ )
Family Cephalopod Species mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
mean ± SD
(range)
(Large beaks)
Moroteuthis knipovitchi
(Large beaks)
Taonius sp. B (Voss)
Gonatus antarcticus
Histioteuthis eltaninae
Alluroteuthis antarcticus
Illex argentinus
Galiteuthis glacialis
Appendix 9 – δ13
C and 15
N signatures, lower rostral length (LRL), carbon (C) and nitrogen (N) percentages of lower beaks from cephalopod species (with at
least 6 lower beaks) found in wandering albatrosses during reproductive period. SD= standard deviation.