pedro miguel oliveira soromenho de alvito -...

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

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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

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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


3.2.2 At the end of inter-breeding/beginning of breeding period (EIB/BB) ...................... 23

3.3 Wandering albatross ..................................................................................................... 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).

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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


( 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


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).


from Psychroteuthis glacialis) to -19.99‰ (Chiroteuthis veranyi; Fig. 10c), comprising 9


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.


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 )


( 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 )


( 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 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.


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


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


( 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).


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 )


( 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 )


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 )


( 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 )


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


( 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


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


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


Martialia hyadesi

(Large beaks)



Gonatus antarcticus


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


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 )


(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 )


( 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 )


(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 )


( 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


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


Gonatus antarcticus



Martialia hyadesi

(Large beaks)


(Large beaks)

Cephalopod Species

Appendix 7 – δ13

C and 15


least 6 lower beaks) found in gray-headed albatrosses during reproductive period. SD= standard deviation.

52

Appendix 8 – δ13

C and 15


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 )


(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 )


( 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 )


(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 )


( 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 )


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)


(Large beaks)

Taonius sp. B (Voss)

Gonatus antarcticus



Illex argentinus


Appendix 9 – δ13

C and 15


least 6 lower beaks) found in wandering albatrosses during reproductive period. SD= standard deviation.

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