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Universidade de Lisboa

Faculdade de Ciências

Departamento de Biologia Animal

“Cephalopod Fauna in the Southern Ocean using the diet of wandering

albatrosses Diomedea exulans: a stable isotopes approach”

Miguel Fernandes Guerreiro

Dissertação

Mestrado em Ecologia Marinha

2012

1

Universidade de Lisboa

Faculdade de Ciências

Departamento de Biologia Animal

“Cephalopod Fauna in the Southern Ocean using the diet of wandering

albatrosses Diomedea exulans: a stable isotopes approach”

Miguel Fernandes Guerreiro

Dissertação Orientada pelo Prof. Doutor Rui Rosa da Faculdade de Ciências da Universidade de

Lisboa e Doutor José Xavier do Instituto do Mar em Coimbra e do British Antarctic Survey

Mestrado em Ecologia Marinha

2012

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Á memória de Josefa Esteves Afonso (17/03/1933 - 23/09/2011),

carinhosamente chamada por avó.

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AGRADECIMENTOS

Quero agradecer ao meu orientador externo Dr. José Xavier pela oportunidade em fazer uma tese

desta escala, e focada na Antártida. Foi um excelente orientador, já que me guio em todo o

processo do desenvolvimento de uma dissertação cientifica e todo o processo por detrás desta, e

levou-me aos melhores locais da Europa (e senão do Mundo) para se fazer ciência Polar e

apresentou-me os maiores especialistas na matéria. Para rematar, e citando o mesmo, foi um

orientador “Brutal” (Xavier, 2007).

Ao meu orientador interno Dr. Rui Rosa, que puxou por mim, e me “puxou pelas orelhas”

quando foi preciso.

Ao Dr. Yves Cherel, pelos seus comentários, perspectivas e conhecimentos que me passou

fundamentais para a minha dissertação.

Ao Dr. Filipe Ceia, pela sua paciência e compreensão no laboratório de Coimbra (IMAR). Se não

fosse ele, provávelmente os meus resultados estariam todos contaminados devido á minha

inexperiência.

Á Dr. Alexandra e á Dr. Gabriela (IMAR), por correr as análises de isótopos estáveis e “tomar

contar” da minha equipa de trabalho respectivamente.

Á minha equipa de trabalho (Pedro Alvito e José Seco), pela a ajuda no processamento de

mandíbulas de cefalópodes em Coimbra.

Á minha irmã pela ajuda na formatação do texto da tese.

Á minha Familia, e ao meu grupo de amigos, ambos por me ouvirem um bilião de vezes a falar

de isótopos, e responderem-me de volta, e claro, pela afeição que nutrem por mim.

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ABSTRACT

The Southern Ocean is a key component in the climatic and ecological global system.

Cephalopods play an important task in this ecosystem. However, they are difficult to collect and

therefore the basic knowledge regarding their ecology is scarce. The wandering albatross,

Diomedea exulans, is a cephalopod predator. Here I characterize the cephalopod component of

D. exulans diet by collecting boluses and regurgitates of chicks from around the ocean, in South

Georgia, Crozet and Kerguelen Islands. By using stable isotopes analyses of Nitrogen and

Carbon on the squids found on the diet, I can determine the distribution and trophic level of

them, an approach that may provide important information about the threats of D. exulans.

D. exulans fed predominantly in Onychoteuthid and Histioteuthid squids and secondarily on

cranchiids and giant squids. Kerguelen diet differs from the others due to the influence of these

large bodied squids, further proving the idea that much of the diet of these seabirds comes from

scavenging.

Cephalopods of the Southern Ocean were distributed within three water masses (Subtropical,

Subantarctic and Antarctic), except for South Georgia (Antarctic and Subantarctic). Much of the

previous biogeographic distributions of these squids in the Indian sector were confirmed or

expanded north, for the subantarctic region. Cephalopods on the Southern Ocean occupy a great

trophic span, from Martialia hyadesi (3.52±0.25 TL) to Taningia danae (6.01±0.15 TL).Thus,

squids play a key role in the trophic ecology of D. exulans, that feeds mainly of Antarctic and

Subantarctic and secondarily of Subtropical squids.

Based on these findings, we may argue that D. exulans have different threats within the Southern

Ocean: in the Atlantic, Longliners operating in the nearby shelves are the main threat; In the

Indian sector, there is different contributions from Subtropical Tuna fishing and longliners in the

shelves, at the two studied islands.

Key-Words: Cephalopods, Southern Ocean, Stable Isotopes, Diomedea exulans.

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RESUMO

O Oceano Antártico, também conhecido como Oceano Austral e Oceano Glacial Antártico, é

constituído por uma série de bacias abissais oceânicas, interrompidas pelas cristas oceânicas de

Scotia e Macquarie e pela plataforma continental de Kerguelen.

Este oceano representa um importante componente tanto do Clima e Oceano global, como

também da Bioesfera. É aqui que se inicia a corrente termohalina profunda, fundamental para a

vida submarina planetária devido ao abastecimento de oxigénio às camadas mais profundas do

oceano, e para a vida à superfície, visto que transporta nutrientes das profundezas para os

produtores primários pelágicos. Também é nesta região que se encontra a corrente circumpolar

antártica, acompanhada pelas vagas e ventos de oeste que aumentam a profundidade da camada

homogénea superficial (conceito fundamental em produção primária). Para a existência destes

fenómenos fundamentais e para a manutenção da calote glacial é essencial que as temperaturas

registadas na Antártida permaneçam abaixo de zero.

Deste Oceano dependem vários animais para se reproduzirem e alimentarem, nomeadamente a

ave com maior envergadura de asas do nosso planeta, o Albatroz-Errante (Diomedea exulans).

Esta espécie está, segundo a União Internacional para a Conservação da Natureza (I.U.C.N),

vulnerável à extinção, em muito devido à mortalidade que advém da interação desta ave com

barcos de pesca que operam nas suas áreas de alimentação. Os aparelhos atualmente utilizados

para seguir estes animais quando partem para o mar em busca de alimento apenas nos fornecem

dados de localização e massa do alimento, mas nada acerca de intensidade ou frequência de itens

ingeridos, nem a categoria taxonómica a que esses itens pertencem.

Uma dessas categorias taxonómicas, a teutofauna, é composta pelos cefalópodes (lulas e polvos),

que, no oceano Austral apresentam um alto grau de endemismo, e muitas divisões taxonómicas

não se encontram aqui presentes, como é o caso dos chocos e lulas Myopsidas. Teoriza-se que a

teutofauna seja responsável por uma cadeia trófica alternativa ao Krill (Euphausia superba) e

que substitua o nicho alimentar dos grandes peixes epipelágicos. Estes moluscos são muito

esquivos, conseguindo evadir-se muito eficazmente à captura por métodos tradicionais tanto

pelos cruzeiros científicos, como por barcos de pesca, daí a informação atualmente disponível

relativamente a estes animais nesta região ser reduzida.

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Nos últimos anos têm sido desenvolvidas técnicas e metodologias com isótopos estáveis de

Carbono e Azoto que pemitem averiguar a partir das assinaturas destes elementos (razão entre a

concentração do isótopo mais pesado sobre a do mais leve) nas mandibulas inferiores das lulas, a

distribuição latitudinal e posição trófica (respetivamente) destes animais. A assinatura de

Carbono é caracteristico de cada latitude neste Oceano, logo informa onde as lulas se

alimentaram, e como a assinatura de Azoto enriquece de uma forma mais ou menos linear de

nível trófico em nível trófico, é possivel calcular níveis tróficos com esta assinatura.

Assim, este estudo pretende averiguar a intensidade de captura de cefalópodes pelo D. exulans ao

longo do oceano em estudo, através da caracterização da dieta em cefalópodes deste e averiguar

a distribuição geográfica (e trófica) destes cefalópodes, e finalmente, inferir a partir desta

informação consequências conservacionistas para o D. exulans.

Para tal, obtiveram-se regurgitações induzidas e boluses de crias de D. exulans nas ilhas da

Geórgia do sul, Crozet e Kerguelen, donde se recolheram as mandíbulas dos cefalópodes usadas

neste estudo. Através da identificação de cada mandíbula e uso de equações alométricas para

estrapolar o peso da lula a partir do tamanho da mandíbula, foi possível obter valores da

abundância numérica e em massa das várias espécies, e assim caracterizar a dieta.

Para averiguar a distribuição latitudinal das lulas, foram consideradas as assinaturas de Carbono

superiores a -19,5‰ e inferiores a -22,3‰ como subtropicais e antárticas, respetivamente, e as

que se encontravam entre estes limites, como subantárticas. Enquanto que para o cálculo do nível

trófico, foi usada uma função linear que transforma a assinatura de Azoto da mandíbula em nível

trófico.

Com os dados obtidos nas alíneas anteriores, foi possível obter a latitude média em que os

cefalópodes da dieta vivem, através do cálculo da média da assinatura de Carbono das lulas

encontradas na dieta, ponderando-a com o peso (neste caso a percentagem de indivíduos) que as

espécies têm na dieta.

A dieta na Geórgia do sul e Crozet foi dominada em número pelas lulas Kondakovia longimana

(24,2% e 33,7%), Taonius sp B (Voss) (23,7% na Geórgia do sul), Galiteuthis glacialis (8,8%

em Crozet) e Histioteuthis eltaninae (10,6% e 25,3%).

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Em Kerguelen, a ordem de importância do contributo em número é o inverso da observada nas

outras ilhas, com Histioteuthis atlantica (29,9%) a dominar, seguida por G. glacialis (12,2%) e

finalmente K. longimana (10,0%).

Em todas as ilhas, K. longimana destacou-se como a principal espécie a contribuir para a massa

encontrada na dieta (75.5%, 76.0% e 31.0% na Geórgia da sul, Crozet e Kerguelen

respetivamente), mas em Kerguelen verificou-se que lulas gigantes (Architeuthis dux e Taningia

danae) também contribuem com alguma importância para a massa total da dieta (15,0% e

13,2%). A espécie Histioteuthis atlantica, devido ao grande número de individuos encontrado

em Kerguelen , acabou por ter um grande contributo por massa (12,9%).

As diferenças verificadas nas dietas sustentam que no setor atlântico deste Oceano, os albatrozes

dependem mais de Taonius sp. B (Voss), Gonatus antarcticus e Mastigoteuthis sp. A (Clarke)

que no setor Indico, pois neste último setor os albatrozes têm disponível uma maior variedade de

lulas devido à proximidade aos subtrópicos. Foram verificados indícios de necrofagia, pois várias

lulas encontradas pesavam várias vezes mais que um albatroz adulto (aproximadamente 45 Kg e

12 Kg respetivamente).

As lulas analisadas neste estudo apresentam distribuição desde a zona Subtropical á Antártica.

As espécies identificadas como subtropicais foram a H. atlantica, Cycloteuthis akimushkini e

Taonius sp. (Clarke), e como espécies antárticas foram identificadas a Batoteuthis skolops e

Gonatus antarcticus. K. longimana e Moroteuthis knipovitchi também se encontraram em águas

antárticas, mas em alguns locais da amostragem mostraram distribuição subantártica devido ao

efeito que a proximidade à costa tem sobre a assinatura isotópica de Carbono, e também ao facto

de já terem sido observadas a norte da frente polar antártica. Todas as espécies apresentaram a

mesma distribuição que a previamente observada, exceto G. antarcticus que foi observada no

Antártico e Galiteuthis glacialis com a Alluroteuthis antarcticus no subantártico perto da frente

subtropical.

As lulas analisadas distribuem-se por 3 níveis tróficos diferentes, desde o final do terceiro até ao

início do sexto, com a Martialia hyadesi a representar o terceiro nível (alimentando-se

potencialmente de copépodes e krill), seguida no quarto pela K. longimana e Moroteuthis ingens

(alimentando-se potencialmente de mictófideos e outros peixes mesopelágicos). No início do

quinto nível estavam presentes várias espécies que são características do meio mesopelágico

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como H. eltaninae e Haliphron atlanticus e a meio deste nível encontra-se B. skolops e M. sp. A

(Clarke), duas espécies muito similares, e que provavelmente têm a mesma estratégia alimentar

que outros Mastigoteuthideos, ou seja, alimentam-se de zooplânton bentopelágico. Nos níveis

tróficos mais elevados, encontra-se G. antarcticus, T. sp. B (Voss) e Taningia danae, que se

alimentam de presas com assinaturas de Azoto elevadas devido a encontrarem-se em cadeias

tróficas muito inefecientes ou a serem predadores de topo. Não foi possível a determinação de

níveis tróficos na zona subtropical, mas C. akimushkini apresenta a assinatura de Azoto mais

alta, e H. atlantica mais baixa. A espécie H. atlantica revela um crescimento da assinatura de

Azoto com o aumento do tamanho do animal.

A média ponderada da assinatura de Carbono das dietas dos albatrozes em lulas e a assinatura de

Carbono das principais lulas da dieta mostrou que na Georgia do sul os albatrozes se alimentam

em média na zona da frente polar, limitando-se mais a água subantárticas e proximas das

plataformas continentais desta região, onde ocorre a pesca do Bacalhau da Patagónia

(Dissostichus eleginoides), enquanto que no setor indico, alimentam-se mais a norte na zona

subantártica, perto da plataforma continental das ilhas Kerguelen (onde opera a pesca ao D.

eleginoides), ou no mar aberto entre estas e as Crozet.

Em Kerguelen, se os dados da dieta estiverem certos acerca da importância da H. atlantica, estas

aves alimentam-se principalmente na zona subtropical onde ocorre a pesca ao atum Thunnus

maccoyii e secundariamente na plataforma continental da ilha onde são residentes (onde opera a

pesca ao D. eleginoides), se H .atlantica afinal não for tão importante, a principal zona de

alimentação será mesmo a plataforma continental, com os seus respetivos perigos.

Assim, K. longimana domina a dieta de D. exulans, com diferentes contribuições das outras

familias de lulas nas várias ilhas. As lulas presentes na dieta vêm desde a zona subtropical até á

Antártida com exceção na Geórgia do sul, onde não se registaram lulas dos subtrópicos. A

importância na cadeia trófica destes animais foi confirmada, encontrando-se animais de vários

níveis tróficos. A principal ameaça ao D. exulans é a pesca dos palangreiros nas plataformas

continentais desta região, e em Kerguelen, a pesca ao Atum Thunnus maccoyii.

Palavras-Chave: Cefalópodes, Antártico, Isótopos estáveis, Diomedea exulans.

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TABLE OF CONTENTS

1. Introduction ........................................................................................................................... 15

1.1 Southern Ocean oceanography and climate.................................................................... 15

1.2 Southern Ocean cephalopods.......................................................................................... 17

1.3 Wandering albatrosses as a sampling predator of cephalopods ..................................... 18

1.4 Using stable isotopic signatures of cephalopods beaks .................................................. 19

1.5 Objectives ....................................................................................................................... 20

2. Material and Methods............................................................................................................ 21

2.1 Study Area and sampling ................................................................................................ 21

2.2 Characterization of cephalopod component in the albatross’ diet .................................. 21

2.3 Stable isotopes analysis .................................................................................................. 23

2.3.1 Isotope Modeling..................................................................................................... 24

2.4 Statistical Analyses ......................................................................................................... 24

3. Results ................................................................................................................................... 26

3.1 Overall ............................................................................................................................ 26

3.1.1 Diet .......................................................................................................................... 26

3.1.2 Stable isotopes ......................................................................................................... 26

3.2 South Georgia ................................................................................................................. 27

3.2.1 Diet .......................................................................................................................... 27

3.2.2 Stable isotopes ......................................................................................................... 33

3.3 Crozet ............................................................................................................................. 36

3.3.1 Diet .......................................................................................................................... 36

3.3.2 Stable Isotopes......................................................................................................... 37

3.4 Kerguelen........................................................................................................................ 40

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3.4.1 Diet .......................................................................................................................... 40

3.4.2 Stable Isotopes......................................................................................................... 41

3.5 Comparison between islands .......................................................................................... 44

3.5.1 Diet indexes ............................................................................................................. 44

3.5.2 Diversity and cumulative curves ............................................................................. 44

3.5.3 Spatial differences of cephalopod species parameters and signatures .................... 46

3.5.4 Overall trophic level assessment ............................................................................. 49

3.5.5 Isotope modeling of wandering albatrosses foraging waters .................................. 50

4. Discussion ............................................................................................................................. 51

4.1 Methodological limitations ............................................................................................. 51

4.2 Spatial differences in the cephalopod diet of wandering albatrosses ............................. 53

4.3 Cephalopod habitats in the Southern Ocean and adjacent waters .................................. 55

4.4 Cephalopod trophic position in the Southern Ocean and adjacent waters ..................... 57

4.5 Implications on the conservation of wandering albatrosses ........................................... 60

5. Final considerations............................................................................................................... 62

6. Bibliography .......................................................................................................................... 63

7. annexs .................................................................................................................................... 71

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LIST OF FIGURES

Figure 1.1 - The Southern Ocean. Emerged areas are green coloured. Parallels are spaced 10º and

meridians 20º. The geographical position of the breeding islands of D.exulans South Georgia,

Prince Edward, Crozet, Kerguelen, Heard & Macdonald and Macquarie on the Southern Ocean.

The main surface water circulation in the Southern ocean is also represented (Orange arrows –

warmer waters; Blue arrows – colder waters of the Circumpolar Current) with the 1000 m

isobath. Main Oceanic fronts are present in the map on the left. Legend: PF-Antarctic Polar

Front; SAF- Sub-Antarctic Front; STF-Sub-Tropical Front. (Source: Orsi et al., 1995) .............. 15

Figure 3.1 - Lower Rostral Length (LRL) distribution of the squids found on the diet of

Wandering Albatross in South Georgia, Crozet and Kerguelen. .................................................. 26

Figure 3.2 – Lower Rostral Length (LRL) distribution of the squids found on the diet of

Wandering Albatross in South Georgia. ....................................................................................... 28

Figure 3.3 - Distribution of the stable isotopes signatures of the squids of South Georgia. Top

panel shows the Carbon signature(Red line and Blue line correspond to Subtropical and Polar

fronts respectively from ( Cherel & Hobson, 2007)) and in the Bottom panel the Nitrogen

signature. "L" and "S" in front of Histioteuthis atlantica stand for large and small specimens

respectively.................................................................................................................................... 35


Wandering Albatross in Crozet. .................................................................................................... 36

Figure 3.5 - Distribution of the stable isotopes signatures of the squids of Crozet. Top panel

shows the Carbon signature (Red line and Blue line correspond to Subtropical and Polar fronts

respectively from ( Cherel & Hobson, 2007)) and in the Bottom panel the Nitrogen signature. . 39


Wandering Albatross in Kerguelen. .............................................................................................. 40

Figure 3.7 - Distribution of the stable isotopes signatures of the squids of Kerguelen. Top panel

shows the Carbon signature (Red line and Blue line correspond to Subtropical and Polar fronts

respectively from ( Cherel & Hobson, 2007)) and in the Bottom panel the Nitrogen signature.

"L" and "S" in front of Histioteuthis atlantica stand for large and small specimens respectively.

....................................................................................................................................................... 43

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Figure 3.8 - Coleman Curves of the squid diversity in South Georgia, Crozet and Kerguelen. ... 45

13

LIST OF TABLES

Table 3.1 - Lower Rostral Length (LRL), Mantle Length (ML) and Weight (W) of the main

species found on the diet of Wandering Albatrosses of South Georgia, Crozet islands and

Kerguelen. (Continued next page) ................................................................................................ 29

Table 3.2 - Frequency of occurrence (F%), number of beaks (N%) and estimated mass(W%) of

the main species contributing to the diet of Wandering Albatross in South Georgia, Crozet and

Kerguelen. All species in Table 7.3 in annex. ............................................................................... 33

Table 3.3 - Lower Rostral Length (LRL), Nitrogen and Carbon stable isotopes signatures of the

main species found on the diet of Wandering Albatrosses of South Georgia. .............................. 34

Table 3.4 - Lower Rostral Length(LRL), Nitrogen and Carbon stable isotopes signatures of the

main species found on the diet of Wandering Albatrosses of Crozet. .......................................... 38

Table 3.5 - Lower Rostral Length(LRL), Nitrogen and Carbon stable isotopes signatures of the

main species found on the diet of Wandering Albatrosses of Kerguelen. .................................... 42

Table 3.7 - Tests results of the Nitrogen stable isotopes signatures of the squid species analysed.

Legend: A – Anova; T – T-test; T(EXP) – T-test, to exponentially transformed data. ................ 47

Table 3.8 - Tests results of the Carbon stable isotopes signatures of the squid species analysed.

Legend: A – Anova; T – T-test. .................................................................................................... 48

Table 3.9 - Trophic level of the main Antarctic and Sub-Antarctic species found on the diet of

Wandering Albatrosses of South Georgia, Crozet and Kerguelen. ............................................... 49

Table 3.10 - Mean Stable isotopes signatures of carbon and Nitrogen of the cephalopod

component of the diet of Wandering Albatrosses of South Georgia, Crozet and Kerguelen. ...... 50

Table 7.1 – Alometric equations chosen from Xavier & Cherel (2009). Legend: a- Chiroteuthid

family formula; b- Brachioteuthid family formula; c- Cranchiid family formula; d- Taonius spp.

formula; e- Gonatus spp. Formula; f- Cycloteuthis akimushkini formulas; g- Galiteuthis glacialis

formula. ......................................................................................................................................... 72

Table 7.2 – Distribution of mantle length (ML), weight (W) and LRL from all squids found on

D. exulans diet in the South Georgia, Crozet and Kerguelen islands. .......................................... 75

14

Table 7.3 – All squid items found on the D. exulans diet throughout the three studied isands, and

their respective contributions to the diet in terms of frequency, numeric and mass indexes. ....... 84

Table 7.4 – Chi-squared results on the diet indexes (Frequency of occurrence (F%), numeric

(N%) and mass (W%) indexes). .................................................................................................... 88

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1. INTRODUCTION

1.1 Southern Ocean oceanography and climate

The Southern ocean consists of a system of deep-sea basins separated by the Scotia Ridge (South

of the Falklands), the Kerguelen plateau (in the Indian section) and the Macquarie Ridge (South

of New Zealand) (Carmack, 1990) and is limited in the South by the Antarctic continent (Figure

1.1).

Figure 1.1 - The Southern Ocean. Emerged areas are green coloured. Parallels are spaced 10º and meridians

20º. The geographical position of the breeding islands of D.exulans South Georgia, Prince Edward, Crozet,

Kerguelen, Heard & Macdonald and Macquarie on the Southern Ocean. The main surface water circulation

in the Southern ocean is also represented (Orange arrows – warmer waters; Blue arrows – colder waters of

the Circumpolar Current) with the 1000 m isobath. Main Oceanic fronts are present in the map on the left.

Legend: PF-Antarctic Polar Front; SAF- Sub-Antarctic Front; STF-Sub-Tropical Front. (Source: Orsi et al.,

1995)

16

The northern part is surrounded by the relatively warmer waters of the Antarctic Polar Frontal

Zone (APFZ), beginning at the Antarctic convergence or Antarctic Polar Front (APF), which

varies temporally and spatially between the 47ºS and 63ºS latitudes and it is characterized by a

horizontal thermocline of 2-3ºC and other oceanic clines (Carmack, 1990; Orsi et al., 1995;

Moore et al. 1997; Trathan et al. 1997; Moore et al., 1999). The main surface current is the

Antartic Circumpolar Current (ACC) that runs eastwards around the continent.

Other important oceanic features in this ocean are the Sub-Antarctic Front (SAF; it sets the end

of the APFZ waters and the beginning of the Sub-Antarctic waters), formed by the mixture of

southern waters brought by the ACC and Northern tropical waters, and the Subtropical

convergence or Subtropical Front (STF) (near the 40ºS latitude) (Deacon, 1982). The ACC with

the APF, constitute a biological barrier, making this ocean virtually closed to all outside species

(Collins & Rodhouse, 2006).

The fronts mentioned above are delineated by wind and oceanic features. Most of the Southern

ocean is characterized by strong West winds, except for the area near the continent, where East

winds predominate. The area of transition of this two wind regimes near the continent, it is called

the Antarctic divergence, and it is characterized by low pressures and upwelling. The APF or

Antarctic convergence, is the region where the Westerlies and Ekman drift are stronger (Deacon,

1982). The STF or Subtropical convergence occurs where the Westerlies meet the Trade winds,

and the Antarctic waters sink to unusual depths, suggesting strong downwelling (Deacon, 1982).

Southern Ocean is a key component of the climate system in our planet. The deep thermo-haline

current (THC) starts in this region, fueled by a density shift in the waters due to the low

temperatures, and increase in salinity due to the formation of oceanic ice (Sarmiento et al.,

2004). Also, the low temperatures in this area (great thermal shift) in comparison to surrounding

regions, allows the formation of strong winds, which maintain a strongly deep mixed layer on the

surface of this ocean with high concentrations of nutrients.

This region is therefore, particularly sensitive to climate change as all of its currents and physical

oceanographic and atmospheric processes are deeply dependent of below zero temperatures in

the system, to fuel the THC and winds, and to maintain the Antarctic Ice Cap. The latter, if

melted, would interrupt the THC, and increase global sea-levels by approximately 60 meters

(Church & Gregory, 2001 ).Thus, if any changes in the temperature of this ocean are verified in

17

the future, they will have great repercussions not only in this area and their inhabitants, as for the

global ocean and planet.

Besides playing a key role in the replenishment of dissolved oxygen in the deep sea, this region

also brings nutrients that are deposited in the sea bottom (or in deep waters) back to the surface

(Sarmiento et al., 2004).

Last but not the least, the Southern Ocean is the habitat for numerous seabirds and marine

mammal species, which depend on this ocean productivity and remoteness for foraging and

breeding, respectively.

1.2 Southern Ocean cephalopods

Cephalopods play an important role in the marine food web of the Southern Ocean, since some

of them occupy the niche of epipelagic top predators, normally occupied by sharks and large

fish, and constitute part of an alternate food chain to krill (Rodhouse & White, 1995). These

factors make cephalopods target of predation by many top marine predators (e.g. toothed whales,

seals, penguins and Procellariform birds), and enable them to sustain large populations in the

region (Xavier & Cherel, 2009). In fact, it has been estimated that top marine predators consume

around 34 million tonnes of cephalopods per annum (Clarke, 1983).

Despite their important bio-ecological role in the Southern ocean, the basic knowledge of the

ecology of cephalopods is poorly known (Xavier et al., 1999). One of the main reasons for that is

the fact that the Southern Ocean cephalopods have not awakened the interest of fishery industry,

due to: i) the low number of exploitable species ii) the unpredictability of such stocks, iii) Lack

of knowledge of the abundance and distribution of relevant species and iv) our inability to catch

them ( Cherel et al., 2004; Collins & Rodhouse, 2006; Rodhouse 1998).

Also, the scientific cruises carried out in this area are unable to capture these animals due to the

low speeds they practice, and as well for the orthodox sampling methods used (Rodhouse 1990,

Rodhouse et al. 1996, Clarke 1977, Xavier et al., 2007).

It is worth noting that the cephalopod fauna of the Southern ocean deeply differs from the

cephalopod fauna of the rest of the world. It consists of endemic species of octopods (cirrate and

incirrate) and oegopsid squids, with a total absence of cuttlefish. Also myopsids are absent, and

normally abundant families are rare or nonexistent. Only here we can find the Psychroteuthidae

18

and Batoteuthidae squid families, and the genera Mesonychoteuthis, Psychroteuthis, Kondakovia,

Alluroteuthis, Slosarczykovia and Batoteuthis.

The oegopsid squids in this ocean are exclusively pelagic or benthopelagic and most have

circum-Antarctic patterns of distribution. The cephalopod fauna can be divided into species

entirely Antarctic, and those that span the APF. These last ones either are migratory species or

are deep-sea animals, to which the APF has no biological meaning.

The main squid families found in this ocean are the: i) Onychoteuthids (e.g. including the

Kondakovia and Moroteuthis genera), ii) Ommastrephids (mainly Martialia hyadesi), iii)

Gonatids (e.g. Gonatus antarcticus), iv) Cranchids (including the colossal squid

Mesonychoteuthis hamiltoni), v) Neoteuthids (mainly Alluroteuthis antarcticus), vi) Batoteuthids

(with only Batoteuthis skolops), vii) Mastigoteuthids (e.g. Mastigoteuthis psychrophila and M.

sp. A (Clarke)), and viii) Histioteuthids.

1.3 Wandering albatrosses as a sampling predator of cephalopods

As an alternative to the more conventional methods used to study the biology of cephalopods

from the Southern Ocean, a different approach has been recently applied, namely the use of

seabird predators to sample cephalopods (Xavier et al. 2003a).

In this study, it was used the wandering albatross (D. exulans), the seabird with the largest wing

span (with over 3 meters) that allows them to practice of long distance flights with low energetic

requirements (Weimerskirch et al., 2000), for instance, during its annual circum-antarctic

migration. In general, albatrosses are an excellent tool for this kind of studies, because: i) they

feed on a great amount and diversity of cephalopods (Rodhouse et al., 1987; Tickell 2000), ii)

their populations gather around every year in high density colonies, iii) they do not fear the

human presence, iv) cover large foraging areas to feed their chicks, which in turn v) maintain

undigested parts of their prey in the stomachs for long periods of time (e.g. cephalopod statoliths

and beaks).

D. exulans is thought to explore vast areas of the ocean seeking for large blotches of dying post-

spawning cephalopods that float up to the surface after death or near death (Lipinski & Jackson

1989),or for regurgitated stomach contents of sperm whales (Clarke et al., 1981). These

assumptions are supported by the fact that their diet includes many deep sea cephalopods, i.e.,

19

animals that are usually found in depths out of the albatross reach (note: the maximum depth

reach of the D. exulans is normally the length of its neck).

The main nesting colonies of D. exulans are found in islands and archipelagos of the sub/peri-

antarctic regions of South Georgia, Prince Edward, Crozet, Kerguelen and Macquarie (Figure

1.1). It is a biannual reproducing species, starting its mating season in the beginning of the

austral summer (late November) and ending in the summer of the following year (December)

(Tickell, 2000). By that time, the chicks regurgitate boluses with all the undigested parts of the

meals that the parents gave to them up to that point, and leave the colony, for the first time, into

the ocean.

During this period, breeding D. exulans make foraging trips to the surrounding ocean, which

change in both length and time spent according to the state of development of the chick. Females

go further North than males (Nel et al., 2002 ;Xavier et al., 2004), and it is by far, during

incubation, that the parents perform the longest foraging trips. When chicks are born, parents

limit their trips, becoming shorter and closer to the colonies continental platform (Weimerskirch

et al., 1993; Nel et al., 2002).

According to the International Union for Conservation of Nature (IUCN), D.exulans is presently

in a vulnerable state of conservation, due to several causes, one of them is due to being a by-

catch of the long liners operating in foraging areas (Gales 1993, Gales 1998, Prince et al., 98).

The reason behind the common visits to these fishing vessels is the hope to get an easy meal.

Although the foraging areas of wandering albatrosses are well known, the foraging effort in such

areas has not been quantified yet, as the information of the devices used in foraging behavior

studies can only give us the information about the feeding location and the mass of their food

intake, with no taxonomic or categorical information.

1.4 Using stable isotopic signatures of cephalopods beaks

In the last couple of decades, stable isotopes analysis has been used to study trophic web

ecology, namely by using the isotopes of Carbon (of atomic weights 12 and 13) and Nitrogen (of

atomic weights 14 and 15), to gather information of geographic position and trophic level of

biological samples, respectively (DeNiro & Epstein, 1978; DeNiro & Epstein, 1981).

20

The stable isotope signature of Carbon is influenced by limitations occurring during the

photosynthesis of the autotrophs (the bottom of the food web), mainly by the activity of the

Rubisco or by the concentration of the substrate (CO2) that limits the fixation of Carbon. This

translates into an impoverishment or enrichment in heavy isotopes of Carbon 13, respectively.

As the activity of Rubisco is gradually more limited in the upper latitudes of the ocean due to the

decline of sea surface temperatures (SST) (Sackett et al., 1973), and at the same time, the

increase in CO2 available for the photosynthesis, a latitudinal gradient can be verified from the

equator to the poles (Cherel & Hobson, 2007; Jaeger et al., 2010). This signature is then passed

up throw the food chain with very low variability (DeNiro & Epstein, 1987).

The stable isotope signature of Nitrogen is useful to calculate the trophic level of a sample, as the

heavier isotope of Nitrogen 15 accumulates from trophic level to trophic level in a linear way

(Minagawa & Wada, 1984), and integrates the Nitrogen signatures of the different items of the

diets.

Cherel & Hobson (2005) were the first to adapt and calibrate the stable isotopes methodology for

the cephalopod beaks found on the diet of several of their predators, and by using the respective

signatures, they confirmed the geographic position and trophic levels of reference species, and

extrapolated to the rest of the species in that study. The present study intends to apply this

methodology to the beaks found on the: i) boluses regurgitated by the wanderers’ chicks and ii)

induced regurgitations of the chicks after being feed by their parents.

1.5 Objectives

Under this content, the main objectives of this study are to:

• Characterize the cephalopod diet of wandering albatrosses from the Atlantic sector (South

Georgia), Indian Sector (Crozet and Kerguelen islands) of the Southern Ocean;

• Define the habitat and trophic level of cephalopods in the Southern Ocean and adjacent

waters, using stable isotope analyses;

• Evaluate the implications of such findings on the conservation of wandering albatrosses.

21

2. MATERIAL AND METHODS

2.1 Study Area and sampling

The study area is focused on the Diomedea exulans’ breeding islands (Figure 1.1) off South

Georgia (54ºS, 38ºW; South of the APF) and French archipelagos of Kerguelen (49ºS,69ºE; on

the APF) (Moore et al., 1999; Koubbi et al. 1991) and Crozet (46ºS,51ºE; North of the APF)

(Park et al., 1991; Belkin & Gordon, 1996; Park et al., 1997).

The cephalopod beaks were collected by two methods – boluses and induced regurgitations –

both involving the sampling of stomach contents of albatrosses.

All samples were collected in the same year of 1998 (on the months of September, October and

December).

The boluses were collected in South Georgia, where albatross chicks voluntarily regurgitate prior

to the departure from the colony (fledgling) (Xavier et al., 2003a). Boluses comprise indigestible

items, including beaks of cephalopods given by both parents to the chick, during the winter prior

to its departure, from April/May until October/December (Prince & Morgan, 1987; Xavier et al.,

2003b; Xavier & Croxall, 2007; Xavier et al., 2005).

The second sampling method – induced regurgitations (the animal is held upside down, and its

chest is massaged until the stomach contents are vomited) – was used in the archipelagos of

Crozet and Kerguelen. They were obtained immediately after the chicks being fed by one of its

parents (Cherel & Weimerskirch, 1999; Weimerskirch et al., 2005).

2.2 Characterization of cephalopod component in the albatross’ diet

After sampling in 1998, samples were frozen at -20ºC, until laboratory treatment. Samples from

Crozet and Kerguelen were analyzed in the Centre E´tudes Biologiques de Chizé in France,

while the ones from South Georgia were analyzed at the British Antarctic Survey headquarters,

Cambridge (UK).

The sample treatment was performed according to the procedures described in Table 2.1. The

identification of lower beaks was done according to Xavier & Cherel (2009). Beak identification

22

was confirmed against the collections present in the British Antarctic Survey and in the Centre

E´tudes Biologiques de Chizé.

Table 2.1 – Laboratory procedures adopted on the treatment of the different structures.

Structure Procedure

Beak

Clean and separation in upper and lower beaks (Xavier et al.

2003a).

Upper beak

Counted

Lower beak

Counted, measurement of lower rostral length (LRL) with

callipers with a precision of a tenth of a millimeter and

identification to the species level when possible (Xavier et al.,

2003a; Xavier & Cherel, 2009).

To characterize the cephalopod component in the wandering albatross diet, the following indices

were determined for each island:

i. Weight index value (%W): indicates the percentage of weight that each prey species has

in the diet. For that, it was used allometric equations that relate the wet mass (M, in

grams) and Mantle Length (ML, in mm) with the Lower Rostral Length (LRL) of the

squids, and the Lower Hood Length (LHL) in the octopuses (Xavier &Cherel, 2009). The

total weight contribution of a certain species is then calculated by multiplying the mean

weight of the individuals sampled and measured (LRL), with the total number of Lower

beaks counted for that same species in the samples. Allometric equations from Xavier &

Cherel 2009 were used (Table 7.1,in annex). No equation was available for the ML of

Haliphron atlanticus;

ii. Numeric index value (%N): it is the number of prey of a certain species divided by the

total number of prey in the samples. The number of prey was estimated by the number of

lower beaks found on the samples;

iii. Frequency index value (%F): percentage of samples with lower beaks of each prey.

Biological diversity of each sample was calculated using the Shannon-Wienner index:

;

23

For comparison of diet diversity, there were plotted individual-based rarefaction curves of each

island and by confidence intervals, it was deliberated if the samples are equal or not. In this case,

it was used a mathematically distinct but computationally much faster way, the “random

placement” curve of Coleman (Coleman, 1981; Coleman et al., 1982), which has been shown to

very closely approximate the hypergeometric rarefaction curve (Brewer & Williamson 1994;

Colwell & Coddington 1994). Confidence Intervals of 95% were calculated by adding and

subtracting to the curve the double of standard deviation registered in each point of the curve.

2.3 Stable isotopes analysis

After the characterization of the cephalopod component in the diet of wandering albatrosses off

South Georgia, Crozet, and Kerguelen, only the cephalopod species that had at least 30

individuals present in one of the islands diets were used in the stable isotope study, ie., the

species choice was done according to their importance by number and mass in the diets.

After that, 10 lower beaks for each species were randomly chosen following Cherel & Hobson

(2005) procedure.

In IMAR-CMA laboratory, the beaks were dried at 60ºC and grinded into a fine powder; 0.30 to

0.55 mg of each beak sample were placed in a tin capsule, and the stable isotope signatures were

measured using a Flash EA 1112 Series elemental analyser coupled on line via Finningan conflo

II interface to a Thermo delta V S mass spectrometer. Replicate measurements of internal

laboratory standards (acetanilide) indicate measurement errors < 0.1 % both for Carbon and for

Nitrogen.

The Carbon and Nitrogen isotope signatures are expressed in delta (δ) notation, defined as the

parts per thousand (‰) deviation from a standard material (PDB limestone for δ 13C and

atmospheric Nitrogen for δ 15N);

δ 13C or δ 15N , where R = 13C/12C or 15N/14N.

After this procedure, it was subtracted 0.75‰ and added 4.8‰ to the Carbon and Nitrogen

signature, respectively, to obtain the mean soft tissues signature of the cephalopods (Cherel &

Hobson, 2006).

24

2.3.1 Isotope Modeling

Samples with δ 13C signatures above -19.5‰ and below -22.3‰ were considered of Subtropical

and Antarctic origin respectively (Cherel & Hobson, 2007). Those that did not enter in these two

groups, were Subantarctic.

Trophic levels (TL) of the samples were calculated according to Minagawa & Wada (1984)

equation:

,

using the δ 15N baseline as Salpa thompsoni with δ15N=3.0‰ (South Georgia average of Su7

and Su8 of (Stowasser et al., 2012)) and 3.4‰ (Crozet island and Kerguelen (Cherel et al,

2008)), both at TL=2 to compare later in this study with other top predators of the ocean.

Subtropical species (with a δ 13C signatures above -19.5‰) were not included in this

calculations, as they have a different d15N baseline of the other 2 oceanic areas (Subantarctic

and Antarctic, I.e. below δ 13C=-19.5‰).

To estimate mean foraging latitude of D. exulans in each island, the means and standard

deviation of the stable isotopes signatures of all cephalopod sampled were calculated.

Afterwards, the Weighted mean Carbon and Nitrogen signature of the cephalopod component of

the Wandering Albatross diet was calculated by weighting the mean signature of each species,

with the number of individuals of each cephalopod found on the diet of D. exulans, for each

island. Representation of the diet (total individuals of the sampled species for SI analysis on the

diet/total individuals on the diet) is presented in %.

2.4 Statistical Analyses

In order to compare the three diet indexes, there were used chi-squared tests. For that, individual

categories were created for each common species to the three islands and all the others species

that only occurred in one or two islands were merged in a category called “others”. This was due

to the high sensibility of the chi-squared test to null entries, skewing the test results to statistical

significance.

25

For the frequency index analysis only the common species to the three islands categories were

considered, because otherwise it would skew the final results.

Histioteuthis B is a group of species (H. atlantica and H. eltaninae) merged into this division, on

the moment of identification and measurement of LRL by the British Antarctic Survey in 1998

(South Georgia sample). However, this 2 species were separated a posteriori, by determining H.

eltaninae highest LRL value (4.2 mm inclusive), and higher values being of H. atlantica LRL,

by the observation of LRL distribution of both these species in the other studied islands . This

means, H. atlantica lower LRL values are included in the H. eltaninae sample.

The mean, standard deviation (presented in mean ± standard deviation) and range (minimum-

maximum) were calculated for LRL, stable isotopes signatures data and the mantle length and

weight values of the species (note: the latter were calculated with LRL allometric equations). It

was only used the LRL and Stable isotopes signatures to test for differences between

cephalopods in different diets, due to the inherent error that the allometric equations used to

calculate weight and length have.

Test for difference on previous parameters between two different islands was made by the use of

T-Test if assumptions are followed; If not, it was used the Mann-Whitney test or Kruskall-

Wallis.

When comparing multiple islands (k>3) analysis was carried using an ANOVA (previously,

normality and homogeneity of variances were verified) or Kruskall-Wallis. If significant

differences were demonstrated somewhere among the groups with the ANOVA or Kruskall-

Wallis tests, the Tukey or Dunn Tests were used, respectively, to find out where those

differences were.

All statistical analyses were performed for a significance level of 0.05, using Statistica 10.0.

EstimateS Win 8.20 software was used to calculate the values for the Coleman curves.

26

3. RESULTS

3.1 Overall

3.1.1 Diet

A total of 15,583 beaks were analyzed from the diet of 82 wandering albatrosses. Of those, 7677

were upper and 7906 were lower beaks, all comprising 53 different cephalopod species

belonging to 22 families. The overall distribution of LRL of the beaks revealed three

conspicuous peaks (2 to 3, 5 to 6 and 12 to 13 mm), and a forth minor one around 9-10 mm

(Figure 3.1).

Figure 3.1 - Lower Rostral Length (LRL) distribution of the squids found on the diet of Wandering

Albatross in South Georgia, Crozet and Kerguelen.

3.1.2 Stable isotopes

A total of 384 samples were collected from the 3 islands. The selected species for stable isotopes

analysis (both Histioteuthis miranda and Teuthowenia pellucida were not included as they

contributed poorly to the diets, whereas Haliphron atlanticus that had only 14 beaks entered the

sampled species due to its cosmopolitan distribution, and interest for future studies) were

responsible for a total of 94.1% of the beaks in Crozet (93.1% of the mass), 86.6% in Kerguelen

27

(71.9% in of the mass) and 94.9% in South Georgia (96.6% of the mass) (Table 3.10). The δN

values varied between 7.21‰ (Martialia hyadesi from Crozet) to 18.11‰ (Gonatus antarcticus

from South Georgia), and δ13C from -26.50‰ (Kondakovia longimana of South Georgia) to -

18.62‰ (Histioteuthis atlantica from Kerguelen). Squid with less than -19.5‰ feed along a

continuum of about 1 trophic level (4.77‰) from K. longimana (11.97±0.38‰ to 12.59±0.75‰)

to T. sp. B (Voss) (15.75±0.80‰ to 16.74±0.64‰). This continuum was preceded by a drop of

2.71‰ (almost 1 trophic level) to M. hyadesi (8.4±0.84‰ and 9.26±0.45‰). All this are

followed by a second feed continuum consisting of subtropical species that span less than 1

trophic level (1.93‰), beginning at H. atlantica small (15.07±0.97‰), and ending at C.

akimushkini (17±0.52‰).

3.2 South Georgia

3.2.1 Diet

A total of 1421 upper and 1329 lower beaks were found in the samples (n= 19) from South

Georgia. The distribution of LRL of the beaks is shown in Figure 3.2 and Table 3.1. Four peaks

were observed, namely:

i. 3 to 4 mm, due to the great amount of Histioteuthis eltaninae beaks;

ii. 5 to 6 mm, the largest peak, which was composed by Alluroteuthis antarcticus, G.

antarticus and H. atlantica;

iii. 9 to 10 mm, due to the presence of Taonius sp. B (Voss);

iv. 14 to 15 mm, due to the presence of K. longimana.

A total of 28 cephalopod species were identified, of which 3 were only found in this island. The

Shannon-Wienner value was H=0.998. The most numerous preys found were (by number) K.

longimana (24.2%), T. sp. B (Voss) (23.7%), H.eltaninae (10.6%), A. antarcticus (7.9%), G.

antarcticus (6.8%) and H.atlantica (5.7%) (Table 3.2). In terms of mass, K. longimana (75.5%)

and T. sp. B (Voss) (7.9%) were the most important (Table 3.2). The distribution of the mantle

length and weigth of each species is shown in Table 3.1 & Table 7.2 , in annex. Mantle length

ranged from 47.2 mm (in Histioteuthis macrohista) up to 706.8 mm (in Taningia danae), while

the weight values showed that the lightest prey came from from Brachioteuthis ?picta and

Batoteuthis skolops (7.8 g ) and the heaviest was again, T. danae (6471.2 g ).

28

Figure 3.2 – Lower Rostral Length (LRL) distribution of the squids found on the diet of Wandering Albatross

in South Georgia.

29

Table 3.1 - Lower Rostral Length (LRL), Mantle Length (ML) and Weight (W) of the main species found on

the diet of Wandering Albatrosses of South Georgia, Crozet islands and Kerguelen. (Continued next page)

South Georgia

LRL (mm)

ML (mm)

W (g)

mean ± sd

mean ± sd

mean ± sd

(Range)

(Range)

(Range)

Alloposidae Haliphron

atlanticus

12.51 ± 2.92

-

482.63 ± 165.14

7.90 - 18.60

-

243.95 - 844.36

Architeuthidae

Architeuthis

dux

-

-

-

Batoteuthidae Batoteuthis

skolops

4.17 ± 0.71

113.37 ± 17.36

39.59 ± 20.77

3.00 - 6.30

84.78 - 165.50

15.26 - 113.12

Cranchidae

Galiteuthis

glacialis

5.30 ± 0.48

450.60 ± 40.48

102.98 ± 20.45

4.00 - 6.40

341.82 - 542.90

54.89 - 154.38

Taonius

sp.(Clarke)

-

-

-

Taonius sp.B

(Voss)

9.24 ± 1.08

555.30 ± 66.31

290.90 ± 69.66

5.40 - 11.30

319.42 - 681.86

88.17 - 444.22

Cycloteuthidae

Cycloteuthis

akimushkini

-

-

-

Gonatidae Gonatus

antarcticus

6.05 ± 0.96

215.94 ± 41.25

228.12 ± 112.49

3.40 - 8.20

102.36 - 308.13

30.57 - 573.51

Histioteuthidae

Histioteuthis

atlantica

5.51 ± 0.55

130.95 ± 14.07

295.28 ± 70.41

4.30 - 6.70

99.92 - 161.50

158.16 - 468.79

Histioteuthis

eltaninae

3.46 ± 0.29

81.01 ± 7.06

67.44 ± 17.25

2.30 - 4.20

52.65 - 99.17

18.55 - 120.68

Histioteuthis

miranda

5.63 ± 0.63

134.13 ± 16.09

468.77 ± 157.70

4.70 - 6.50

110.18 - 156.37

261.02 - 699.44

Mastigoteuthidae

Mastigoteuthis

sp.A (Clarke)

6.93 ± 0.82

181.02 ± 20.16

151.27 ± 49.49

5.00 - 9.60

133.70 - 246.22

60.61 - 352.75

Neoteuthidae

Alluroteuthis

antarcticus

5.16 ± 0.48

176.10 ± 16.88

437.86 ± 120.04

3.40 - 6.70

114.67 - 230.13

125.44 - 924.09

Ommastrephidae

Martialia

hyadesi

4.40 ± 0.46

231.67 ± 13.50

219.93 ± 46.52

4.00 - 4.90

219.88 - 246.40

180.23 - 271.11

30

Onychoteuthidae

Kondakovia

longimana

13.45 ± 1.72

479.46 ± 64.04

2709.54 ± 978.52

5.30 - 17.50

175.44 - 630.72

136.78 - 5903.99

Moroteuthis

ingens 9.90 377.07 1729.76

Moroteuthis

knipovitchi

6.87 ± 0.96

322.81 ± 60.09

695.41 ± 424.50

5.40 - 9.40

231.09 - 480.56

250.62 - 2057.44

Moroteuthis

robsoni

7.87 ± 0.31

535.19 ± 46.14

1852.95 ± 595.67

7.60 - 8.20

494.92 - 585.54

1362.61 - 2515.84

Octopoteuthidae Taningia

danae

14.70 ± 3.21

548.83 ± 241.76

4609.20 ± 2693.68

11.00 - 16.80

270.52 - 706.80

1520.51 - 6471.19

Crozet

LRL (mm)

ML (mm)

W (g)

mean ± sd

mean ± sd

mean ± sd

(Range)

(Range)

(Range)


atlanticus

-

-

-

Architeuthidae

Architeuthis

dux 8.53 450.31

3050.94


skolops

4.02 ± 0.45

109.82 ± 11.02

34.66 ± 10.12

3.01 - 4.96

85.02 - 132.72

15.40 - 59.31

Cranchidae

Galiteuthis

glacialis

5.38 ± 0.35

457.83 ± 29.49

106.17 ± 14.93

4.01 - 6.26

342.65 - 531.17

55.20 - 147.05

Taonius

sp.(Clarke)

5.12 ± 0.29

302.21 ± 17.55

78.76 ± 9.56

4.52 - 5.69

265.36 - 337.24

59.72 - 98.87

Taonius sp.B

(Voss)

8.65 ± 1.20

518.86 ± 73.76

253.30 ± 77.59

5.74 - 11.60

340.31 - 700.29

100.78 - 470.46

Cycloteuthidae

Cycloteuthis

akimushkini

12.76 ± 2.55

395.42 ± 78.90

982.31 ± 350.48

6.39 - 17.56

198.09 - 544.36

246.34 - 1768.64

Gonatidae

Gonatus

antarcticus

6.05 ± 0.64

215.75 ± 27.40

217.17 ± 87.61

5.05 - 7.89

173.09 - 294.84

114.16 - 504.43

Histioteuthidae

Histioteuthis

atlantica

5.64 ± 0.84

134.36 ± 21.44

319.44 ± 107.39

3.20 - 7.20

71.69 - 174.33

76.69 - 559.20

Histioteuthis

eltaninae

3.46 ± 0.32

80.98 ± 7.90

67.73 ± 19.15

2.30 - 5.03

52.65 - 119.48

18.55 - 211.44

Histioteuthis

miranda

6.84 ± 0.40

207.56 ± 13.77

825.91 ± 146.34

5.91 - 7.71

175.67 - 237.25

523.74 - 1175.27

Mastigoteuthidae Mastigoteuthis 6.62 ± 0.62

194.26 ± 18.06

284.07 ± 72.31

31

sp.A (Clarke) 5.26 - 7.79

154.76 - 228.33

143.33 - 444.16

Neoteuthidae

Alluroteuthis

antarcticus

5.46 ± 0.38

186.70 ± 13.23

512.31 ± 100.55

4.22 - 6.23

143.36 - 213.69

236.96 - 745.97

Ommastrephidae

Martialia

hyadesi

6.81 ± 0.83

302.57 ± 23.31

532.83 ± 128.64

5.17 - 9.00

254.36 - 367.23

302.01 - 921.33

Onychoteuthidae

Kondakovia

longimana

12.58 ± 1.37

447.30 ± 51.13

2174.27 ± 796.43

6.20 - 18.66

209.02 - 674.01

224.24 - 7227.75

Moroteuthis

ingens

8.70 ± 1.04

343.04 ± 47.65

1397.23 ± 683.18

5.82 - 11.67

236.25 - 492.99

413.88 - 4149.35

Moroteuthis

knipovitchi

7.30 ± 0.84

349.35 ± 52.26

840.84 ± 354.75

5.75 - 9.07

252.91 - 459.98

318.13 - 1796.30

Moroteuthis

robsoni

8.86 ± 0.39

685.22 ± 59.50

4883.08 ± 1823.92

8.54 - 9.30

636.89 - 751.67

3491.97 - 6948.05

Octopoteuthidae Taningia

danae

15.07 ± 1.72

576.67 ± 129.49

4659.38 ± 1699.85

12.21 - 17.41

361.54 - 752.68

2172.67 - 7310.69

Kerguelen

LRL (mm)

ML (mm)

W (g)

mean ± sd

mean ± sd

mean ± sd

(Range)

(Range)

(Range)


atlanticus

-

-

-

Architeuthidae Architeuthis

dux

11.16 ± 2.85

606.10 ± 168.75

15815.86 ± 16350.63

7.67 - 15.41

399.31 - 858.37

1877.20 - 45525.42

Batoteuthidae

Batoteuthis

skolops

4.71 ± 0.57

126.62 ± 13.82

53.24 ± 16.51

3.67 - 5.57

101.17 - 147.64

26.30 - 81.12

Cranchidae

Galiteuthis

glacialis

5.45 ± 0.33

463.27 ± 27.39

108.90 ± 13.91

3.84 - 6.29

328.41 - 533.68

50.18 - 148.60

Taonius

sp.(Clarke)

4.98 ± 0.22

293.70 ± 13.59

74.07 ± 7.17

4.56 - 5.40

267.82 - 319.42

60.88 - 88.17

Taonius sp.B

(Voss)

9.62 ± 1.09

578.55 ± 66.83

317.28 ± 74.70

6.64 - 11.73

395.60 - 708.27

138.64 - 482.08

Cycloteuthidae

Cycloteuthis

akimushkini

12.78 ± 2.31

396.29 ± 71.57

980.75 ± 322.37

6.90 - 17.98

213.90 - 557.38

286.14 - 1852.07

Gonatidae

Gonatus

antarcticus

6.37 ± 0.73

229.64 ± 31.28

259.97 ± 105.19

5.37 - 7.98

186.81 - 298.70

140.07 - 523.85

Histioteuthidae

Histioteuthis

atlantica

6.05 ± 0.75

144.71 ± 19.10

374.03 ± 101.80

2.54 - 7.79

54.76 - 189.47

43.55 - 678.21

32

Histioteuthis

eltaninae

3.22 ± 0.29

75.23 ± 7.07

54.33 ± 15.60

2.51 - 4.05

57.79 - 95.49

24.34 - 107.77

Histioteuthis

miranda

6.41 ± 1.03

192.63 ± 35.11

715.27 ± 252.18

2.85 - 7.80

70.99 - 240.33

57.05 - 1217.48

Mastigoteuthidae

Mastigoteuthis

sp.A (Clarke)

6.84 ± 0.95

200.60 ± 27.66

319.01 ± 113.27

4.76 - 8.08

140.22 - 236.77

107.50 - 493.46

Neoteuthidae

Alluroteuthis

antarcticus

5.41 ± 0.40

184.93 ± 14.05

499.36 ± 102.55

4.17 - 6.10

141.61 - 209.14

228.79 - 701.07

Ommastrephidae

Martialia

hyadesi

5.97 ± 0.81

278.05 ± 23.77

411.22 ± 111.97

4.36 - 7.68

230.49 - 328.33

214.35 - 669.61

Onychoteuthidae

Kondakovia

longimana

13.44 ± 1.52

479.37 ± 56.57

2685.82 ± 1034.12

10.26 - 19.04

360.53 - 688.19

1097.05 - 7701.93

Moroteuthis

ingens

10.49 ± 0.85

440.15 ± 38.11

2986.58 ± 741.94

9.21 - 11.33

383.20 - 477.82

1922.40 - 3769.18

Moroteuthis

knipovitchi

6.94 ± 0.75

327.06 ± 46.80

691.11 ± 303.82

5.80 - 8.79

256.03 - 442.52

328.77 - 1594.62

Moroteuthis

robsoni

9.17 ± 0.58

731.55 ± 88.04

6883.91 ± 3446.28

8.32 - 10.12

603.66 - 875.51

2828.79 - 13740.81

Octopoteuthidae

Taningia

danae

17.36 ± 2.17

748.56 ± 163.14

7656.06 ± 2669.42

11.62 - 20.62

317.16 - 994.14

1834.14 - 13040.49

33

Table 3.2 - Frequency of occurrence (F%), number of beaks (N%) and estimated mass(W%) of the main

species contributing to the diet of Wandering Albatross in South Georgia, Crozet and Kerguelen. All species

in Table 7.3 in annex.

South Georgia

Crozet

Kerguelen

Family Species F% N% W%

F% N% W%

F% N% W%

Alloposidae Haliphron atlanticus 52.6 1.1 0.6

- - -

- - -

Architeuthidae Architeuthis dux - - -

12.1 0.1 0.3

63.3 0.8 15.0

Batoteuthidae Batoteuthis skolops 57.9 2.2 0.1

84.8 2.8 0.1

66.7 1.3 0.1

Cranchidae

Galiteuthis glacialis 84.2 4.5 0.5

97.0 8.8 1.0

96.7 12.2 1.5

Taonius sp.(Clarke) - - -

48.5 1.0 0.1

60 2.1 0.2

Taonius sp. B (Voss) 100.0 23.7 7.9

57.6 1.6 0.4

53.3 6.8 2.5

Cycloteuthidae Cycloteuthis akimushkini - - -

57.6 1.0 1.0

86.7 3.2 3.6

Gonatidae Gonatus antarcticus 89.5 6.8 1.8

60.6 1.5 0.3

73.3 1.7 0.5

Histioteuthidae

Histioteuthis atlantica 89.5 5.8 2.0

84.8 3.3 1.1

96.7 29.9 12.9

Histioteuthis eltaninae 100.0 10.6 0.8

100.0 25.3 1.8

86.7 7.9 0.5

Histioteuthis miranda 42.1 0.9 0.5

54.5 0.9 0.7

60.0 1.4 1.2

Mastigoteuthidae Mastigoteuthis sp.A (Clarke) 78.9 3.9 0.7

54.5 0.8 0.2

23.3 0.4 0.2

Neoteuthidae Alluroteuthis antarcticus 94.7 8.0 4.0

87.9 2.5 1.3

90.0 3.2 1.9

Ommastrephidae Martialia hyadesi 10.5 0.2 0.1

84.8 4.3 2.4

86.7 3.7 1.8

Onychoteuthidae

Kondakovia longimana 94.7 24.2 75.5

100.0 33.7 76.0

86.7 10.0 31.0

Moroteuthis ingens 5.3 0.1 0.1

93.9 4.1 5.9

20.0 0.3 0.9

Moroteuthis knipovitchi 68.4 3.2 2.6

93.9 3.4 3.0

83.3 2.5 2.0

Moroteuthis robsoni 10.5 0.2 0.5

9.1 0.1 0.4

46.7 0.9 6.8

Octopoteuthidae Taningia danae 10.5 0.2 1.2

18.2 0.2 0.7

46.7 1.5 13.2

3.2.2 Stable isotopes

119 beaks from South Georgia were used for stable isotopes analysis. The δN values ranged

from 11.25‰ (K. longimana) to 18.11‰ (G. antarcticus), and δ13C from -26.50‰ (K.

longimana) to -19.20‰ (H. atlantica small)

The distribution of the δ15N and δ13C signatures by species is showed in the Table 3.3 and

Figure 3.3. There were three δ15N signatures groups: i) K. longimana was the squid with by far

the lowest signature (11.97±0.38‰) followed by ii) the second group, consisting of a continuum

of squids beginning at G. glacialis (13.39±1.10‰) and finishing at B. skolops (14.45±0.28‰),

iii) and finally, a second continuum of squids, starting with H. atlantica small (15.89±0.58‰),

and ending at H. atlantica large(16.75±0.72‰). The highest standard deviations were found in

G. glacialis (1.10‰) and A. antarcticus (0.98‰).

34

Subtropical signatures (mean δ13C higher than -19.5‰) were not found, but H. atlantica showed

the closest values as it had the highest values for δ13C (-19.9±0.48‰ and -20.39±0.61‰ for

small and large specimens respectively).Antarctic signatures (below -22.3‰) were found in H.

eltaninae (-22.66±1.20‰), G. antarcticus (-23.28±2.33‰), M. knipovitchi (-23.85±1.00‰), K.

longimana (-24.37±1.59‰) and B. skolops (-25.14±0.54‰). The species showing high standard

deviations in their δ13C signatures were G. antarcticus (2.33‰), A. antarcticus (1.46‰), K.

longimana (1.59‰), H. eltaninae (1.20‰) and M. knipovitchi (1‰).

Table 3.3 - Lower Rostral Length (LRL), Nitrogen and Carbon stable isotopes signatures of the main species

found on the diet of Wandering Albatrosses of South Georgia.

South Georgia

Family Species LRL(mm)

Nitrogen (‰)

Carbon (‰)

mean ± sd

mean ± sd

mean ± sd

Alloposidae Haliphron atlanticus 12.51 ± 2.92

13.80 ± 0.41

-20.91 ± 0.30

Batoteuthidae Batoteuthis skolops 4.17 ± 0.71

14.45 ± 0.28

-25.14 ± 0.54

Cranchidae

Galiteuthis glacialis 5.30 ± 0.48

13.39 ± 1.10

-22.27 ± 0.82

Taonius sp. (Clarke) -

-

-

-

-

-

Taonius sp. B (Voss) 9.24 ± 1.08

16.74 ± 0.64

-21.94 ± 0.82

Cycloteuthidae Cycloteuthis akimushkini -

-

-

-

-

-

Gonatidae Gonatus antarcticus 6.05 ± 0.96

16.46 ± 0.73

-23.28 ± 2.33

Histioteuthidae

Histioteuthis atlantica 5.51 ± 0.55

16.34 ± 0.78

-20.17 ± 0.59

Histioteuthis atlantica

small -

-

15.89 ± 0.58

-19.92 ± 0.48


Large -

-

16.75 ± 0.72

-20.39 ± 0.61

Histioteuthis eltaninae 3.46 ± 0.29

14.28 ± 0.76

-22.66 ± 1.20

Histioteuthis miranda -

-

-

-

-

-

Mastigoteuthidae Mastigoteuthis sp. A

(Clarke) 6.93 ± 0.82

15.95 ± 0.46

-21.26 ± 0.75

Neoteuthidae Alluroteuthis antarcticus 5.16 ± 0.48

13.52 ± 0.98

-21.67 ± 1.46

Ommastrephidae Martialia hyadesi -

-

-

-

-

-

Onychoteuthidae

Kondakovia longimana 13.45 ± 1.72

11.97 ± 0.38

-24.37 ± 1.59

Moroteuthis ingens -

-

-

-

-

-

Moroteuthis knipovitchi 6.87 ± 0.96

13.88 ± 0.63

-23.85 ± 1.00

Octopoteuthidae Taningia danae -

-

-

-

-

-

35

Mean

Mean±SD

Mean±2*SD

Histioteuthis atlantica S

Histioteuthis atlantica L

Haliphron atlanticus

?Mastigoteuthis A (Clarke)

Alluroteuthis antarcticus

Taonius sp.B (Voss)

Galiteuthis glacialis

Histioteuthis eltaninae

Gonatus antarcticus

Moroteuthis knipovitchi

Kondakovia longimana

Batoteuthis skolops

-30

-28

-26

-24

-22

-20

-18

δ 1

3C

‰

-22.3

-19.5

Mean

Mean±SD

Mean±2*SD


Taonius sp.B (Voss)

Gonatus antarcticus



Batoteuthis skolops



Haliphron atlanticus




10

11

12

13

14

15

16

17

18

19

δ 1

5N

‰

Figure 3.3 - Distribution of the stable isotopes signatures of the squids of South Georgia. Top panel shows the

Carbon signature(Red line and Blue line correspond to Subtropical and Polar fronts respectively from (

Cherel & Hobson, 2007)) and in the Bottom panel the Nitrogen signature. "L" and "S" in front of

Histioteuthis atlantica stand for large and small specimens respectively.

36

3.3 Crozet

3.3.1 Diet

A total of 3719 upper and 3905 lower beaks were analyzed in Crozet (n = 33 samples).

Moreover, a total of 3904 individuals were identified, with a total estimated mass of 3508.7 Kg.

Regarding cephalopod diversity, 45 species were identified in Crozet; 8 of them were exclusively

found here. The Shannon-Wienner value was H=0.958 (lowest value on this study). The

distribution of LRL of the beaks found in this island is shown in Figure 3.4. Two large peaks

were detected at 3 to 4 and 5 to 6 mm, which were dominated by H. eltaninae and Galiteuthis

glacialis, respectively. A third peak was found from 12 to 13 mm, which was dominated by K.

longimana.

Figure 3.4 - Lower Rostral Length (LRL) distribution of the squids found on the diet of Wandering Albatross

in Crozet.

The main species occurring by number (Table 3.2) were K. longimana (33.7%), H. eltaninae

(25.3%) and G. glacialis (8.8%); regarding mass, the species that dominated were K. longimana

(76%) and Moroteuthis ingens (5.9%) (Table 3.2).

37

Distribution of the mantle length and weight by species found in the diet of the samples of this

study is showed in the Table 3.1 & Table 7.2,in annex. Mantle length ranged from 5.4 mm

(Notonikya africanae) to the colossal squid (Mesonychoteuthis hamiltoni) with 927.6 mm..

Lightest prey was a 5.5 g Slosarczykovia circumantarctica, and heaviest was a 9205.7 g

Lepidoteuthis grimaldii.

3.3.2 Stable Isotopes

130 beaks from Crozet were used for stable isotopes analysis. The δ15N values ranged from

7.21‰ (M .hyadesi) to 17.31‰ (T. sp. B (Voss)), and δ13C from -25.07‰ (Moroteuthis.

knipovitchi) to -19.04‰ (H. atlantica).

The distribution of the δ15N and δ13C signatures by species is showed in the Table 3.4 and

Figure 3.5. Again, three δ15N signatures groups were found: i) M. hyadesi stands out with the

lowest signature (8.40±0.84‰), followed by ii) the second group, consisting of a continuum of

squids beginning at K. longimana (12.22±0.40‰) and finishing at H. eltaninae (13.81±0.32‰),

iii) and finally, a second continuum of squids, starting with B. skolops (15.15±0.69‰), and

ending at T. sp. B (Voss) (15.75±0.80‰). Highest standard deviations were found in

M.hyadesi(0.84‰) and T. sp. B (Voss) (0.80‰).

Subtropical δ13C signatures were found in H. atlantica (-19.34±0.20‰) and T. sp. (Clarke) (-

19.41±0.30)‰ (Both this species presented some of the highest δ15N in the sample); Antarctic

signatures were found in M. hyadesi (-22.57±0.42‰), K. longimana (-22.60±0.65‰), B. skolops

(-23.62±0.50‰) and G. antarcticus (-23.94±1.18‰). The species showing higher standard

deviations in their δ13C signatures were M. knipovitchi (1.47‰), A. antarcticus (1.38‰), G.

antarcticus (1.18‰) and T. sp. B (Voss) (1.05‰).

38

Table 3.4 - Lower Rostral Length(LRL), Nitrogen and Carbon stable isotopes signatures of the main species

found on the diet of Wandering Albatrosses of Crozet.

Crozet


Nitrogen (‰)

Carbon (‰)

mean ± sd

mean ± sd

mean ± sd

Alloposidae Haliphron atlanticus - -

- -

- -


15.15 ± 0.69

-23.62 ± 0.50

Cranchidae


13.67 ± 0.55

-21.29 ± 0.53

Taonius sp. (Clarke) 5.12 ± 0.29

15.62 ± 0.42

-19.41 ± 0.30


15.75 ± 0.80

-21.38 ± 1.05

Cycloteuthidae Cycloteuthis akimushkini 12.76 ± 2.55

- -

- -


15.58 ± 0.61

-23.94 ± 1.18

Histioteuthidae

Histioteuthis atlantica 5.64 ± 0.84 15.63 ± 0.65 -19.34 ± 0.20


small -

-

-

-

-

-


Large -

-

-

-

-

-


13.81 ± 0.32

-21.42 ± 0.56

Histioteuthis miranda 6.84 ± 0.40

- -

- -


(Clarke) 6.62 ± 0.62

13.73 ± 0.70

-21.42 ± 0.51


13.01 ± 0.23

-21.29 ± 1.38

Ommastrephidae Martialia hyadesi 6.81 ± 0.83

8.4 ± 0.84

-22.57 ± 0.42

Onychoteuthidae


12.22 ± 0.40

-22.60 ± 0.65

Moroteuthis ingens 8.70 ± 1.04

12.69 ± 0.20

-21.79 ± 0.35


12.81 ± 0.45

-22.09 ± 1.47

Octopoteuthidae Taningia danae - -

- -

- -

39

Mean

Mean±SD

Mean±2*SD


Taonius sp.(Clarke)



Taonius sp.B (Voss)



Moroteuthis ingens


Martialia hyadesi


Batoteuthis skolops

Gonatus antarcticus

-27

-26

-25

-24

-23

-22

-21

-20

-19

-18δ

13

C‰

-22.3

-19.5

Mean

Mean±SD

Mean±2*SD

Taonius sp.B (Voss)


Taonius sp.(Clarke)

Gonatus antarcticus

Batoteuthis skolops






Moroteuthis ingens


Martialia hyadesi6

8

10

12

14

16

18

δ 1

5N

‰

Figure 3.5 - Distribution of the stable isotopes signatures of the squids of Crozet. Top panel shows the Carbon

signature (Red line and Blue line correspond to Subtropical and Polar fronts respectively from ( Cherel &

Hobson, 2007)) and in the Bottom panel the Nitrogen signature.

40

3.4 Kerguelen

3.4.1 Diet

A total of 2537 upper and 2672 lower beaks were analyzed from Kerguelen (n= 30 samples).

Regarding cephalopod diversity, a total of 41 species were found, of which 4 were endemic.

From the 2672 individuals identified, a total estimated mass of 2264.3 Kg was recorded. The

Shannon-Wienner value was H=1.143 (highest value recorded on this study). The distribution of

LRL of the beaks is shown in Figure 3.6. The distribution was dominated by a large peak of H.

eltaninae, H. atlantica and G. glacialis (5 to 6 mm). Beyond 10 mm, the LRL readings were

dominated first by T. sp. B (Voss) and then by K. longimana.

Figure 3.6 - Lower Rostral Length (LRL) distribution of the squids found on the diet of Wandering Albatross

in Kerguelen.

The main species in Kerguelen (Table 3.2) were, by number: H. atlantica (29.9%), G. glacialis

(12.2%), K. longimana (10%), H. eltaninae (7.9%) and T.sp.B (Voss) (6.8%). According to

mass, the main species were K. longimana (31%), Architeuthis dux (15%), Taningia danae

(13.2%), H. atlantica (12.9%) and Moroteuthis robsoni (6.8%).

41

The distribution of the mantle length and weight is shown in the Table 3.1 and Table 7.2,in

annex. H. atlantica was the smallest prey found (minimum 54.76 mm). On the other hand, the

largest prey was T. danae (maximum 994.14 mm). The lightest species was H. eltaninae

(minimum 24.34 g) while the heaviest was the giant squid A. dux (maximum 45525.42 g). It is

worth noting that T. danae and Moroteuthis robsoni presented some of the heaviest individuals,

over 13 Kg (13040.49 g and 13740.81 g respectively).

3.4.2 Stable Isotopes

135 beaks from Kerguelen were used for stable isotopes analysis. The δ15N values ranged from

8.40‰ (M. hyadesi) to 17.7‰ (H. atlantica large), and δ 13C from -25.46‰ (K. longimana) to -

18.63‰ (H. atlantica small).

Distribution of the δ15N and δ13C signatures by species is shown in the Table 3.5 and Figure

3.7.

In here, there were four δ15N signatures groups found: i) M. hyadesi stands out with the lowest

signature (9.26±0.45‰), followed by ii) the second group, consisting of a continuum of squids

beginning at K. longimana (12.59±0.75‰) and finishing at H. eltaninae (13.51±0.47‰), iii) a

second continuum of squids, starting with G. antarcticus (15.04±0.51‰), and ending at B.

skolops (15.10±0.41‰) and finally iv) the highest continuum, with H. atlantica large

(16.42±0.69‰) to C. akimushkini (17.00±0.52‰). Highest standard deviations were found in H.

atlantica small (0.97‰) and K. longimana (0.75‰).

Subtropical δ13C signatures were found in T. sp. (Clarke) (-19.28±0.22‰), C. akimushkini (-

19.32±0.32‰) and H. atlantica (-19.36±0.40‰ and 19.46±0.66‰ for small and large

respectively); Antarctic signatures were found in B. skolops (-23.69±0.73‰) and M. knipovitchi

(-23.71±0.95‰). Species showing high standard deviations in their δ13C signatures were K.

longimana (1.84‰), G. antarcticus (1.80‰), H. eltaninae (1.11‰), T. danae (1.04‰) and M.

knipovitchi (0.95‰).

42

Table 3.5 - Lower Rostral Length(LRL), Nitrogen and Carbon stable isotopes signatures of the main species

found on the diet of Wandering Albatrosses of Kerguelen.

Kerguelen


Nitrogen (‰)

Carbon (‰)

mean ± sd

mean ± sd

mean ± sd

Alloposidae Haliphron atlanticus -

-

-

-

-

-


15.1 ± 0.41

-23.69 ± 0.73

Cranchidae


13.26 ± 0.71

-21.07 ± 0.59

Taonius sp. (Clarke) 4.98 ± 0.22

16.28 ± 0.70

-19.28 ± 0.22


16.61 ± 0.48

-21.85 ± 0.84

Cycloteuthidae Cycloteuthis akimushkini 12.78 ± 2.31

17 ± 0.52

-19.32 ± 0.32


15.04 ± 0.51

-22.48 ± 1.80

Histioteuthidae

Histioteuthis atlantica 6.05 ± 0.75

15.74 ± 1.08

-19.41 ± 0.54


small -

-

15.07 ± 0.97

-19.36 ± 0.40


Large -

-

16.42 ± 0.69

-19.46 ± 0.66


13.51 ± 0.47

-21.50 ± 1.11

Histioteuthis miranda 6.41 ± 1.03

-

-

-

-


(Clarke) 6.84 ± 0.95

-

-

-

-


13.2 ± 0.36

-20.70 ± 0.90


9.26 ± 0.45

-21.75 ± 0.79

Onychoteuthidae


12.59 ± 0.75

-22.34 ± 1.84

Moroteuthis ingens -

-

-

-

-

-


13.44 ± 0.41

-23.71 ± 0.95

Octopoteuthidae Taningia danae 17.36 ± 2.17

16.64 ± 0.50

-20.68 ± 1.04

43

Figure 8. Distribution of the stable isotopes signatures of the squids of Kerguelen. Top panel

shows the Carbon signature(Red line and Blue line correspond to Subtropical and Polar fronts

Mean

Mean±SD

Mean±2*SD

Taonius sp.(Clarke)

Cycloteuthis akimushkini



Taningia danae




Martialia hyadesi

Taonius sp.B (Voss)


Gonatus antarcticus

Batoteuthis skolops

Moroteuthis knipovitchi-27

-26

-25

-24

-23

-22

-21

-20

-19

-18

-17

δ 1

3C

‰

-22.3

-19.5

Mean

Mean±SD

Mean±2*SD Cycloteuthis akimushkini

Taningia danae

Taonius sp.B (Voss)


Taonius sp.(Clarke)

Batoteuthis skolops


Gonatus antarcticus






Martialia hyadesi6

8

10

12

14

16

18

20

δ 1

5N

‰

Figure 3.7 - Distribution of the stable isotopes signatures of the squids of Kerguelen. Top panel shows the

Carbon signature (Red line and Blue line correspond to Subtropical and Polar fronts respectively from (

Cherel & Hobson, 2007)) and in the Bottom panel the Nitrogen signature. "L" and "S" in front of

Histioteuthis atlantica stand for large and small specimens respectively.

44

3.5 Comparison between islands

3.5.1 Diet indexes

There were no significant spatial differences between the frequency of occurrence of cephalopod

species in the diet of wandering albatrosses from South Georgia, Crozet and Kerguelen islands

(χ2=13.261; p = 0.99). Similar findings were observed for the numeric and weight index values

(χ2=39.68; p =0.66 and χ2=57.57; p =0.055, respectively). Yet, it is worth noting that there were

great deviations from the predicted values, namely in the numeric index for South Georgia, and

also in the weight index for South Georgia and Kerguelen (Table 7.4,in annex). The species that

differed the most by number of individuals were the T. sp. B (Voss), Mastigoteuthis sp.A(Clarke)

and G. antarcticus from South Georgia; By weight, they were the T. sp. B (Voss) and G.

antarcticus from South Georgia, M. robsoni, T. danae and H. atlantica from Kerguelen (Table

7.4,in annex). The most numerous species found were K. longimana, H. eltaninae and H.

atlantica (especially on Kerguelen). Top species contributing to the overall weight found were K.

longimana, H. atlantica and T. danae (both this last 2 species from Kerguelen).

3.5.2 Diversity and cumulative curves

Shannon-Wiener Index was higher in Kerguelen, and lowest in South Georgia, while rarefaction

curves are shown in Figure 3.8 and indicated that: i) South Georgia has less cephalopod diversity

than the French islands, and ii) Crozet appears to have higher diversity, although there is no

statistical significance between the archipelagos of Crozet and Kerguelen (as most part of both

curves are inside each other confidence intervals of 95%).

45

Figure 3.8 - Coleman Curves of the squid diversity in South Georgia, Crozet and Kerguelen.

46

3.5.3 Spatial differences of cephalopod species parameters and signatures

Significant spatial differences between same species from different islands were observed for

LRL, δ15N and δ13C (Table 3.6, Table 3.7 and Table 3.8). Briefly, the biggest specimens (LRL)

of B. skolops, G. glacialis and H. atlantica, and the smallest H. eltaninae, A. antarcticus were

observed in Kerguelen. The biggest T. sp. (Clarke), M. hyadesi and M. knipovitchi, and the

smallest K. longimana were found in Crozet. Additionally, T. sp. B (Voss) from South Georgia

was smaller than the ones from Kerguelen, and bigger than the ones from Crozet (Table 3.6).

Table 3.6 - Tests results of the Lower Rostral Length (LRL) of the squid species analyzed. Legend: K-W -

Kruskall-Wallis.

Family Species LRL (mm)

South Georgia

Crozet

Kerguelen

Test

P-Value


atlanticus 12.51 ± 2.92

- - -

- - -

-

-


skolops 4.17 ± 0.71

4.02 ± 0.45

4.71 ± 0.57

K-W

<0.01

Cranchidae

Galiteuthis

glacialis 5.30 ± 0.48

5.38 ± 0.35

5.45 ± 0.33

K-W

<0.01

Taonius sp.

(Clarke) - - -

5.12 ± 0.29

4.98 ± 0.22

K-W

0.021

Taonius sp. B

(Voss) 9.24 ± 1.08

8.65 ± 1.20

9.62 ± 1.09

K-W

<0.01

Cycloteuthidae Cycloteuthis

akimushkini - - -

12.76 ± 2.55

12.78 ± 2.31

K-W

0.997

Gonatidae Gonatus

antarcticus 6.05 ± 0.96

6.05 ± 0.64

6.37 ± 0.73

K-W

0.111

Histioteuthidae

Histioteuthis

atlantica 5.51 ± 0.55

5.64 ± 0.84

6.05 ± 0.75

K-W

<0.01

Histioteuthis

eltaninae 3.46 ± 0.29

3.46 ± 0.32

3.22 ± 0.29

K-W

<0.01

Histioteuthis

miranda - - -

6.84 ± 0.40

6.41 ± 1.03

K-W

0.056

Mastigoteuthidae Mastigoteuthis

sp. A (Clarke) 6.93 ± 0.82

6.62 ± 0.62

6.84 ± 0.95

K-W

0.201

Neoteuthidae Alluroteuthis


5.46 ± 0.38

5.41 ± 0.40

K-W

<0.01

Ommastrephidae Martialia

hyadesi - - -

6.81 ± 0.83

5.97 ± 0.81

K-W

<0.01

Onychoteuthidae

Kondakovia

longimana 13.45 ± 1.72

12.58 ± 1.37

13.44 ± 1.52

K-W

<0.01

Moroteuthis

ingens - - -

8.70 ± 1.04

- - -

-

-

47

Moroteuthis

knipovitchi 6.87 ± 0.96

7.30 ± 0.84

6.94 ± 0.75

K-W

<0.01

Octopoteuthidae Taningia danae - - -

- - -

17.36 ± 2.17

-

-

Regarding the δ15N signature, it was in South Georgia that significantly higher values for G.

antarcticus and H. atlantica (small), and the lowest for B. skolops were observed. Kerguelen was

where it was found the higher values for T. sp. (Clarke) and M. hyadesi. The lowest value for T.

sp. B (Voss) was registered in Crozet. Moreoever, H. eltaninae values were higher in South

Georgia then in Kerguelen, and K. longimana values from Kerguelen were higher than in South

Georgia. M. sp. A (Clarke) and M. knipovitchi values from South Georgia were higher than the

ones found in Crozet (Table 3.7).

Table 3.7 - Tests results of the Nitrogen stable isotopes signatures of the squid species analysed. Legend: A –

Anova; T – T-test; T(EXP) – T-test, to exponentially transformed data.

Family Species Nitrogen (‰)

South Georgia

Crozet

Kerguelen

Test

P-Value


atlanticus 13.80 ± 0.41

- - -

- - -

-

-


skolops 14.45 ± 0.28

15.15 ± 0.69

15.1 ± 0.41

A

<0.01

Cranchidae

Galiteuthis

glacialis 13.39 ± 1.10

13.67 ± 0.55

13.26 ± 0.71

A

0.53

Taonius sp.

(Clarke) - - -

15.62 ± 0.42

16.28 ± 0.70

T

0.02

Taonius sp. B

(Voss) 16.74 ± 0.64

15.75 ± 0.80

16.61 ± 0.48

A

<0.01


akimushkini - - -

- - -

17 ± 0.52

-

-

Gonatidae Gonatus


15.58 ± 0.61

15.04 ± 0.51

A

<0.01

Histioteuthidae

Histioteuthis

atlantica 16.34 ± 0.78 15.63 ± 0.65 15.74 ± 1.08 A

0.06

Histioteuthis

atlantica small 15.89 ± 0.58

- - -

15.07 ± 0.97

T

0.04

Histioteuthis

atlantica Large 16.75 ± 0.72

- - -

16.42 ± 0.69

T

0.31

Histioteuthis

eltaninae 14.28 ± 0.76

13.81 ± 0.32

13.51 ± 0.47

A

0.01

Histioteuthis

miranda - - -

- - -

- - -

-

-


sp. A (Clarke) 15.95 ± 0.46

13.73 ± 0.70

- - -

T

<0.01

48



13.01 ± 0.23

13.2 ± 0.36

A

0.20


hyadesi - - -

8.4 ± 0.84

9.26 ± 0.45

T(EXP)

0.02

Onychoteuthidae

Kondakovia

longimana 11.97 ± 0.38

12.22 ± 0.40

12.59 ± 0.75

A

0.05

Moroteuthis

ingens - - -

12.69 ± 0.20

- - -

-

-

Moroteuthis

knipovitchi 13.88 ± 0.63

12.81 ± 0.45

13.44 ± 0.41

A

<0.01


- - -

16.64 ± 0.50

-

-

In relation to the δ13C signature, significantly lower values of B. skolops, G. glacialis, H.

eltaninae and K. longimana were found in South Georgia The highest values for H. atlantica

(large) and M. hyadesi were found in Kerguelen and the M. knipovitchi values from Crozet were

significantly higher than those observed in Kerguelen (Table 3.8).

Table 3.8 - Tests results of the Carbon stable isotopes signatures of the squid species analysed. Legend: A –

Anova; T – T-test.

Family Species Carbon (‰)

South Georgia

Crozet

Kerguelen

Test

P-Value


atlanticus -20.91 ± 0.30

- - -

- - -

-

-


skolops -25.14 ± 0.54

-23.62 ± 0.50

-23.69 ± 0.73

A

<0.01

Cranchidae

Galiteuthis

glacialis -22.27 ± 0.82

-21.29 ± 0.53

-21.07 ± 0.59

A

<0.01

Taonius sp.

(Clarke) - - -

-19.41 ± 0.30

-19.28 ± 0.22

T

0.26

Taonius sp. B

(Voss) -21.94 ± 0.82

-21.38 ± 1.05

-21.85 ± 0.84

A

0.36


akimushkini - - -

- - -

-19.32 ± 0.32

-

-

Gonatidae Gonatus

antarcticus -23.28 ± 2.33

-23.94 ± 1.18

-22.48 ± 1.80

A

0.22

Histioteuthidae

Histioteuthis

atlantica -20.17 ± 0.59

-19.34 ± 0.20

-19.41 ± 0.54

A

<0.01

Histioteuthis

atlantica small -19.92 ± 0.48

- - -

-19.36 ± 0.40

T

0.11

Histioteuthis

atlantica Large -20.39 ± 0.61

- - -

-19.46 ± 0.66

T

<0.01

Histioteuthis

eltaninae -22.66 ± 1.20

-21.42 ± 0.56

-21.50 ± 1.11

A

0.02

Histioteuthis

miranda - - -

- - -

- - -

-

-

49


sp. A (Clarke) -21.26 ± 0.75

-21.42 ± 0.51

- - -

T

0.59


antarcticus -21.67 ± 1.46

-21.29 ± 1.38

-20.70 ± 0.90

A

0.24


hyadesi - - -

-22.57 ± 0.42

-21.75 ± 0.79

T

<0.01

Onychoteuthidae

Kondakovia

longimana -24.37 ± 1.59

-22.60 ± 0.65

-22.34 ± 1.84

A

<0.01

Moroteuthis

ingens - - -

-21.79 ± 0.35

- - -

-

-

Moroteuthis

knipovitchi -23.85 ± 1.00

-22.09 ± 1.47

-23.71 ± 0.95

A

0.04


- - -

-20.68 ± 1.04

-

-

3.5.4 Overall trophic level assessment

Average Trophic Levels (TL) of the sampled cephalopods (Table 3.9) ranged from M. hyadesi of

Crozet (3.52±0.25 TL, and a minimum of 3.15 TL) to a G. antarcticus in South Georgia (with a

maximum 6.58 TL). M. hyadesi is isolated at the third trophic level and K. longimana and M.

ingens present the only values in the fourth level. A. antarcticus, M. knipovitchi, G. glacialis, H.

eltaninae and H. atlanticus were in the fifth level; At this level, but showing some omnivory

(feeding in species of different trophic levels) there were B. skolops and M. sp. A (Clarke). In the

sixth TL, there were G. antarcticus, T. sp. B (Voss) and T. danae. The trophic distribution for

each island is represented in Figure 3.3, Figure 3.5 and Figure 3.7.

Table 3.9 - Trophic level of the main Antarctic and Sub-Antarctic species found on the diet of Wandering

Albatrosses of South Georgia, Crozet and Kerguelen.

Trophic Level (TL)

Family Species

South Georgia

Crozet

Kerguelen

mean ± sd

mean ± sd

mean ± sd

Range

Range

Range

Alloposidae Haliphron atlanticus 5.27 ± 0.13

5.09 - 5.52


5.56 ± 0.21

5,54 ± 0,12

5.29 - 5.60

5.38 - 6.09

5.31 - 5.67

Cranchidae


5.11 ± 0.17

4.99 ± 0.21

4.69 - 5.87

4.82 - 5.40

4.63 - 5.30


5.74 ± 0.24

6.00 ± 0.15

5.76 - 6.38

5.30 - 6.21

5.79 - 6.18

50


5.69 ± 0.18

5.53 ± 0.15

5.87 - 6.58

5.30 - 5.90

5.27 - 5.72

Histioteuthidae Histioteuthis eltaninae 5.42 ± 0.23

5.15 ± 0.10

5.06 ± 0.14

5.02 - 5.86

4.98 - 5.29

4.83 - 5.27


(Clarke)

5.92 ± 0.14

5.13 ± 0.21

5.72 - 6.14

4.87 - 5.39


4.91 ± 0.07

4.97 ± 0.11

4.80 - 5.63

4.82 - 5.04

4.82 - 5.17


3.78 ± 0.14

3.15 - 3.87

3.52 - 3.98

Onychoteuthidae


4.67 ± 0.12

4.79 ± 0.23

4.50 - 4.88

4.54 - 4.87

4.35 - 5.07

Moroteuthis ingens 4.82 ± 0.06

4.72 - 4.94


4.85 ± 0.14

5.04 ± 0.12

4.83 - 6.00

4.54 - 5.01

4.89 - 5.22

Octopoteuthidae Taningia danae 6.01 ± 0.15

5.88 - 6.26

3.5.5 Isotope modeling of wandering albatrosses foraging waters

The values of the δ15N and δ13C signatures for each island (taking account the number of

individuals captured by Diomedea.exulans) are presented in Table 3.10. South Georgia was the

most impoverished in C13 (-23.48±1.30‰), and Kerguelen the least impoverished (-21.54±

1.30‰). For the 15 Nitrogen isotopes, Crozet was the least enriched (17.85± 1.46‰) and South

Georgia the most enriched (19.33± 1.91‰).

Table 3.10 - Mean Stable isotopes signatures of carbon and Nitrogen of the cephalopod component of the diet

of Wandering Albatrosses of South Georgia, Crozet and Kerguelen.

Island (samples) % of diet covered

δN (‰)

δC (‰)

South Georgia (N=1250) 94.9%

19.33 ± 1.91

-23.48 ± 1.3

Crozet (N=3637) 94.1%

17.85 ± 1.46

-22.69 ± 0.87

Kerguelen (N=2302) 86.6%

19.3 ± 1.86

-21.54 ± 1.3

51

4. DISCUSSION

4.1 Methodological limitations

There are several limitations related to the stable isotopes methodology that was used in this

study, and several other potential biases that could be important to the results here obtained.

In this study, we only characterize the component of cephalopods in the diet of wandering

albatrosses. Yet, the diet of wandering albatrosses is also known to comprise fish in fairly similar

proportions to those of cephalopods (Croxall & Prince 1994; Xavier et al. 2004), and smaller

amounts of carrion and crustaceans (mostly Krill) ( Xavier et al. 2003b). Therefore, this study

focuses only on less than half of the diet, and any conclusions about the overall albatross dietary

ecology, or feeding behaviour is limited, despite not being on the aims of the study. Also,

albatross diet is a biased estimation of the amount and diversity of cephalopods found in the

Southern ocean, due to how cephalopods might be available to albatrosses. Cephalopods that

sink after death (sinking species) might be underestimated in the diet when compared to species

that float after dying. This is because D. exulans only feeds on food available at the sea surface

and probably these sinking squid species come from rare sperm whale vomit scavenging (Clarke

et al., 1981), although the origin of this squids are still under debate (Croxall & Prince 1994;

Rodhouse & Boyle 2010 in press; Xavier et al., 2012 in press). But apart from that, D. exulans

proved to be an efficient sampling tool for cephalopods.

Secondly, incorrect estimation of cephalopod consumption could result from equations used to

estimate squid mass, as this are normally based on: i) low number of individuals covering a

restricted size range (Xavier et al. 2003a), ii) estimations made only with the lower beaks, and it

was observed differences in the number of lower and upper beaks, or iii) conserved individuals,

in which, the conservation process could have altered the original weight of the specimens. The

same limitation is applied to the mantle length estimations. Therefore, further work as to be done

in order to obtain more accurate equations for both upper and lower beaks (Xavier et al.2007;

Xavier et al., 2011).

Thirdly, the Carbon isotopes apart from giving us latitudinal positioning of our sample

(according to water mass), it also can give us information about the position/distance of the

52

biological sample to the coast (Coastal vs. Oceanic) and to the bottom (Benthic vs. Pelagic)

(Cherel& Hobson 2005), meaning that there can be a synergetic effect of this three gradients

(one latitudinal and two longitudinal (coast to open ocean and benthos to pelagic areas)) in the

Carbon signature adding noise and error to the latitude prediction. Therefore, the species of this

study are all considered and picked for being entirely oceanic, and never feeding in coastal or

benthic waters. This problem could have been solved by using stable isotopes of Oxygen – which

give us the information of the temperature (and therefore in the Southern ocean, latitude) where

the animals lived in – but there are currently no studies that calibrate SI signatures of Oxygen of

cephalopods beaks and their muscles, and furthermore, the number of samples that we could run

would be significantly lower due to the costs associated to the measurement of these isotopes.

Further work with Oxygen stable isotopes in this squids should be done, to complement the

Carbon signature in this Ocean.

Forthly, the Nitrogen signature has a major problem: when comparing same trophic level

specimens from different areas or habitats (in this case water masses), Nitrogen signatures do not

match, because, there are different baseline Nitrogen signatures on these environments (i.e.

different background levels of the Nitrogen isotopes (Cherel et al., 2000)). Therefore, it is with

precaution that it is studied the trophic distribution of the samples, when they are in different

water masses that are known to have different baseline Nitrogen signature levels, in this case,

Subtropical waters versus Antarctic and Subantarctic waters. The best solution to this problem

would be by assessing the Nitrogen signature of a cosmopolitan species that has throughout its

distribution, the same trophic level, being the best candidate a phytoplankton or even better, an

herbivor (or a low level omnivor) that lives more than a year, so it can integrate a year round

Nitrogen signal, I.e.Krill (E. superba). Unfortunately, in this study it was used S. thompsoni

sampled in another study (Stowasser et al. 2012), as the representative species for our food web

baseline in South Georgia. S. thompsoni feeds mainly on flagellates and cyanobacteria

(Sutherland et al., 2010; von Harbou et al., 2011), both being isotopically depleted when

compared to other forms of phytoplankton (Fry and Wainwright, 1991; del Giorgio and France,

1996; Fawcett et al., 2010), thus making S. thompsoni also isotopically depleted then expected

for an herbivor (it presented a lower Nitrogen signature then particulate organic matter (POM)

(Stowasser et al.2012)). In consequence, it was used only the average of the 2 highest samples

(Su7 and Su8) as the Nitrogen baseline signature, but even so, trophic levels of the squids in this

53

study may be overestimated in comparison to reality. Furthermore, there are still processes that

change the Nitrogen signature of these (and other) animals that are not yet fully understood, that

can give the wrong idea about their trophic level. Hence, complementary methods should be used

when trying to estimate trophic distribution in animals, as for example, concentration of heavy

metals in their tissues (Anderson et al., 2009).

Fifthly, cephalopods carry out ontogenetic and annual migrations throughout their lives, and by

so, their stable isotopes signatures might be different from the place where they were captured by

albatrosses. So, conclusions about the foraging behavior of albatrosses are limited, but in terms

of prey water mass origin, valuable information can be provided.

4.2 Spatial differences in the cephalopod diet of wandering albatrosses

In other studies done at South Georgia, the onychoteuthid family (and more specifically K.

longimana) also dominated the diets of Wandering Albatross (Clarke et al.1981; Rodhouse et al.

1987; Imber 1992 ; Xavier et al, 2003a), followed by the family Cranchiidae (particularly the

cranchid species Taonius sp. ( Clarke et al. 1981; Rodhouse et al. 1987; Xavier et al. 2003a)) and

by the family Histioteuthidae.

At Crozet, Ridoux (1994), Cherel & Weimerskirch (1999) also found K. longimana to be the

most important item of the diet of Albatross. However, in Cherel & Weimerskirch (1999), M.

ingens is the overall second most numerous species, while in this study, H. eltaninae and G.

glacialis were the second and third most numerous species, as according to Ridoux (1994).

However, M. ingens was the second most important in mass, while in the Cherel &

Weimerskirch (1999), M. ingens in a rare year (1992) was the most important cephalopod in

mass, contributing to 56.8% of the fresh remains on the diet.

At Kerguelen, to our knowledge, there are no dietary studies of the wandering albatross.

According to the results obtained in the present study, H. atlantica is by far the most relatively

abundant species by number, followed by G. glacialis, K. longimana, H. eltaninae and Taonius

sp. B (Voss). By mass, the most important species were K. longimana, A. dux, T. danae, H.

atlantica and M. robsoni, which are all big size species, except for the H. atlantica which is a

small squid (Table 3.1), but due to the high number of individuals found in the diet its

contribution to the total diet mass was significant. The high relative abundance of H. atlantica in

54

Kerguelen waters in 1998 was also registered one year later on the diet of Dissostichus

eleginoides during the 1999 summer fishing season in a 3 years study (1998, 1999 and 2000) (

Cherel et al., 2004).

It is interesting the importance of these giant squids on the diet of the albatrosses from

Kerguelen, mainly A. dux, since on the other islands these species do not have such relevancy.

The radical difference in teuthofauna found in this place can be explained by the great difference

of the nearby Ocean basin. Unlike the other two places studied that consist in Oceanic ridges,

Kerguelen has an enormous continental shelf, which might gather the right conditions to support

this squids.

Diet of D.exulans from Crozet, in this and other studies (Cherel & Weimerskirch, 1999; Ridoux,

1994), shows dominance of the Onychoteuthid family and also the presence of H. eltaninae and

G. glacialis, showing similarities with Kerguelen; in Crozet however, giant species do not appear

to be as important as in Kerguelen.

At Marion island (Cooper et al., 1992) the most abundant species by number were H. eltaninae,

K. longimana, G. glacialis and A. antarcticus (this one is not significant in the Kerguelen diet),

and by weight the Onychoteuthids , while in Prince Edward (Imber, 1992), species dominating

by weight were the Onychoteuthids followed by the Octopoteuthid T. danae, also found in

Kerguelen.

South Georgia presented higher availability of T. sp. B (Voss) and G. antarcticus, with the latter

known to have important juvenile stocks in which seabirds feed in the nearby Falkland islands

(Thompson, 1994). Both these species (and Mastigoteuthis sp. A) are responsible for most

differences observed in the numeric indexes, showing that albatross are more dependent on these

stocks in the Atlantic sector. The biodiversity of cephalopod prey found in the three islands show

that the Albatrosses in the Indian sector relay on a greater number of species (specially the

population nesting in Crozet) than in the Atlantic sector, probably due to the proximity of Crozet

and Kerguelen to the Subtropical Ocean and the Kerguelen plateau.

Moreover, the present findings also revealed clear indications that D. exulans shows a

scavenging strategy, especially at Kerguelen, since there are several captured prey found in their

diet that are several times heavier than the mean D. exulans, as other studies show (Croxall &

Prince, 1994; Xavier & Croxall, 2007).

55

4.3 Cephalopod habitats in the Southern Ocean and adjacent waters

Cephalopods on the Southern ocean are classified by their water masses, namely: Antarctic,

Subantarctic and Subtropical. Furthermore, some of them can display circumpolar or local

distributions. Xavier et al.(1999) has published distribution maps of several of these species in

GIS-maps, where he pinpointed the known locations of captured specimens. In those maps, K.

longimana, M. knipovitchi, B. skolops, A. antarcticus and G. glacialis present a Circumpolar

Antarctic distribution (South of the APF). As for Sub-antarctic species (North of the APF), there

were M. ingens, G. antarcticus, H. atlantica, H. eltaninae, M. hyadesi and occasionally Taonius

sp. (cf. pavo).

This study agrees with the Antarctic distribution for B.skolops (In South Georgia it is further

south than in the other 2 locations), K. longimana and M. knipovitchi found on previous studies (

Xavier et al., 1999). The last two squids presented subantarctic distributions in the Indian sector

(Cherel & Weimerskirch, 1999). It is plausible that the highly productive shelf in Kerguelen

(South of the APF) is pulling the Carbon signature to northern latitudes. Similar findings were

observed by Cherel & Hobson (2005).

In Cherel & Hobson (2005), individuals of M. knipovitchi with a sub-antarctic Carbon signature

were captured in the Kerguelen continental shelf by King Penguins (Aptenodytes patagonicus)

and presented higher values of Carbon than the ones found in the present study (whose signature

values were from Antarctic waters). If this species has true Antarctic distribution, then

potentially, M. knipovitchi comes from oceanic waters populations and the Kerguelen plateau is

adding 2‰ to the Carbon signature of the animals captured in there.

If we take the Kerguelen shelf’s effect, discussed on the previous paragraph, into consideration

than it can be used to explain the higher Carbon signatures within the same squid species on the

Indian sector – higher Carbon signatures come from Kerguelen shelf and lower from Open

Ocean.

It can be inferred then that M. knipovitchi of Crozet were taken almost exclusively from the

Kerguelen plateau (D. exulans males feed in this area ( Weimerskirch et al., 1997)) and the

remaining from oceanic waters (explaining the great standard deviation, and the proximity to the

values obtained in Kerguelen in a previous study (Cherel & Hobson 2005)), while at Kerguelen,

squids were from Antarctic Oceanic waters. Therefore, M. knipovitchi is probably rare or

56

nonexistent in the Crozet waters. Also, if we apply this to K. longimana, squids found in Crozet

diet actually came in part from Kerguelen shelf and from the open southern ocean (south of the

APF), while squid of the diet of Kerguelen were from the nearby shelf.

The standard deviation in the Carbon signatures for K. longimana and M. knipovitchi agree with

Cherel & Weimerskirch (1999) in extending the biogeography of both these squids north of the

APF, but not only at Crozet islands as proposed by them, but also at Kerguelen.

K. longimana presented great standard deviations, both in the South Georgia and Kerguelen

specimens, supporting a great flexibility for this squid to occupy different habitats. In the case of

South Georgia, the species can have a broader latitudinal distribution, as the oceanic fronts

deflect northwards between the South American continent and the Falkland islands, while in

Kerguelen, the species can explore the vast continental shelf and oceanic waters around the

islands (Figure 1.1).

According to the Carbon results, G. antarcticus also has a strong Antarctic distribution, against

the more exclusive northern Subantarctic that was previously thought (Collins & Rodhouse,

2006; Xavier et al., 1999). The high standard deviations verified in this species δ 13C could

mean that this species has no problem in settling in waters south of the STF (as previously

agreed in Xavier et al., 1999), up to the coastal areas of the Antarctic continent.

For Subantarctic species, there were M. ingens in Crozet islands, M. hyadesi of Kerguelen, H.

eltaninae at the Indian sector, and from the 3 studied islands T. sp. B (Voss), agreeing with

previous studies (Voss, 1980; Xavier et al., 1999). We also showed that M. hyadesi in Crozet and

H. eltaninae in South Georgia probably live around the APF, and adults of the H. atlantica in

South Georgia live in the lower latitudes of the Subantarctic waters or in the STF.

Complementarily to what was predicted in previous studies (Collins & Rodhouse, 2006; Xavier

et al., 1999), A. antarcticus and G. glacialis seem to also live in the Subantarctic waters, with the

Carbon signature distribution pointing out for the possibility of A. antarcticus and G. glacialis

living near the STF. M. sp. A(Clarke), T.danae and H.atlanticus also were present in these

waters.

Species that lived in the Subtropical waters north of the Southern Ocean, and in range of the

Wandering Albatrosses were T. sp. (Clarke) (Voss, 1980), C. akimushkini and H. atlantica (Voss

et al., 1998). H. atlantica Large presented the same pattern as K. longimana throughout the

57

islands: It had higher Carbon signatures in Kerguelen then South Georgia, due to the southern

position of South Georgia. This is going to be further developed in the last section of the

discussion.

4.4 Cephalopod trophic position in the Southern Ocean and adjacent waters

Information about diet and trophic position of Southern Ocean cephalopods is very scarce, and

limited to M. hyadesi and M. ingens (Cherel & Duhamel, 2003; Rodhouse et al., 1992). In fact,

for the other species the results are dubious due to: i) the low number of individuals available

(Collins & Rodhouse, 2006), and ii) biased source of information (nets sampling Krill) – i.e.

skewed towards a Krill (E. superba) dominated and specialized diet (Nemoto et al., 1985;

Nemoto et al., 1988).

The present study confirmed previous findings on the diet (and stable isotopes analysis) of M.

hyadesi (Cherel et al., 2008; Cherel & Hobson, 2005; Rodhouse et al., 1992), by showing the

lowest mean Nitrogen signature and TL (Table 3.4 ,Table 3.5 and Table 3.9). M. hyadesi diet is

known to feed mainly of Hyperiid amphipods and myctophid fish, although other cephalopods

(i.e. cannibalism) are registered (Rodhouse et al., 1992). Myctophid however, tend to have an

equal to higher trophic level than this squid ( Cherel et al., 2008), therefore, this squid feeds in

this fish in fairly lower quantities then previously suggested, at least in the Indian sector.

K. longimana, as the other SI studies showed, has a very low Nitrogen signature compared to its

size (Cherel et al., 2008; Cherel & Hobson, 2005). This can be due to this species feed on preys

that have low Nitrogen signatures, such as myctophids ( Cherel et al., 2008) and of E. superba

(Kaehler et al., 2000; Cherel et al., 2008; Stowasser et al., 2012). Probably the only works done

with diet in these animals (Nemoto et al., 1985; Nemoto et al., 1988; Kear 1992) showed an

association with E. superba because of the method used to collect information or krill is a minor

component of the diet (respectively). Clearly the size of these animals is not correlated to their

trophic level, as for the case of Baleen whales (Pauly et al., 1998). However, the results of Wada

et al.(1987) obtained in South Georgia are 4‰ lower than the ones from this study , but Wada et

al. do not provide any further information about the squids captured as for mantle length, or any

other biological data.

58

M. ingens presented higher Nitrogen values (i.e. trophic level; TL=4.82±0.06) then M. hyadesi

and fairly similar to K. longimana, which is within the expected values of a diet dominated by

mesopelagic fish (myctophids and paralepids) (Cherel & Duhamel, 2003).

G. glacialis showed higher values than the ones found in previous study (Stowasser et al., 2012).

This difference was greater than a trophic level, and as for the case of K. longimana (Wada et al.,

1987) no any other biological data was provided to figure out the difference between the 2

samples/studies. This trophic level is dominated by cephalopods of the mesopelagic realm (H.

atlanticus, H. eltaninae and G. glacialis). This comes with no surprise, as they are all dependent

of the sea snow that comes from the epipelagic layer, which is in some extent, slightly enriched

in Nitrogen heavy isotopes due to the microbial decomposition that occurs during the transport

from the surface to this depth, and also, some of the sea snow may be already enriched in

Nitrogen heavy isotopes before decomposition starts (E.g. dead high trophic animals).

M. sp. A (Clarke) from South Georgia and B. skolops Nitrogen signatures are near the ones

obtained for Mastigoteuthis psychrophila in Cherel & Hobson (2005), while M. sp. A (Clarke) of

Crozet agree with the ones obtained also for M. psychrophila in ( Cherel et al., 2008). These

values could be explained by a diet on benthonic-benthopelagic zooplankton, that in turn are

dependent on the bacterial decomposition of surface production that settles in the ocean floor, as

previously proposed (Roper & Vecchione, 1997) for Mastigoteuthids (Batoteuthids seem to share

adaptations with Mastigoteuthids for this kind of feeding strategy). M. sp. A (Clarke) from South

Georgia shows a higher Nitrogen signature(15,95±0,46‰) than the one observed in

Crozet(13,73±0,70‰).Several other species showed the same trend in South Georgia (higher

Nitrogen signatures) giving the impression that squids here are feeding differently than the

Indian Sector (higher trophic levels in South Georgia). This trend could be due to the

local/regional productivity, as cyanobacteria and flagellates that live in open ocean waters poor

in nutrients (probably the case of Crozet oceanic waters) have Nitrogen depleted signatures(Fry

and Wainwright, 1991; del Giorgio and France, 1996; Fawcett et al., 2010), in contrast with rich

upwelling waters with high diatom productivity (the case of South Georgia); Or squids in South

Georgia, are eating differently, due to competitive pressure from other low trophic animals or

normal prey in 1998 were unavailable and squid changed their diet to higher trophic more

available prey.

59

G. antarcticus presents the highest Nitrogen signature in the Antarctic water mass. These high

mean Nitrogen signature values are (2‰) higher than the ones found in previous studies ( Cherel

et al., 2008; Cherel & Hobson, 2005), and just below of M. hamiltoni. This may indicate that G.

antarcticus may feed on prey that has similar high Nitrogen signature values to the Patagonian

toothfish D. eleginoides ( Cherel et al., 2008) ( several squid in this study match that

requirement), or that depends on an alternate, and very inefficient, food chain. G. antarcticus and

T. sp. B (Voss) probably follows the last trend, as they are small squid wich would have

difficulties seizing such large and active prey. G. glacialis however, could easily be a prey of

these 2 squids.

T. danae is one of the top predator squid in the deep sea (Cherel et al., 2009), with Nitrogen

signature as high or higher than those from A. dux, and within the values registered in other

studies (Cherel & Hobson, 2005; Cherel et al. 2009). Trophic level in this study agreed with

these previous studies (Cherel & Hobson, 2005; Cherel et al. 2009), as it is around 6.01±0.15, the

highest in Subantarctic and Antarctic waters.

Subtropical species (H. atlantica, C. akimushkini and T. sp. (Clarke))presented some of the

highest Nitrogen signatures, much due to the Nitrogen baseline shift from Antarctic and

Subantarctic waters to Subtropical. Therefore, Trophic level for this species has to be calculated

with a different base standard then the one used in this study that comes from Antarctic waters.

C.akimushkini has the highest mean Nitrogen signature values in the total sample (17±0.52‰)

while H.atlantica shows a positive correlation between size of the individuals and their Nitrogen

signature, as this squid climb the food chain as they are able to feed on bigger prey.

Overall, squids of this study that live on the Antarctic and subantarctic, are forth level consumers

(TL>5), which is higher than the average level for marine mammals ( TL=4.02 (Pauly et al.,

1998)) and sharks ( TL>4 (Cortés, 1999)). Even so, the trophic span covered by these squids

from the TL=3 to 6, makes them good candidates for occupying the niche of great epipelagic fish

(Cortés, 1999; Rodhouse & White, 1995), to a point where they even compete with great, deep

diving mammals as seals and sperm-whales ( Cherel et al., 2008).

60

4.5 Implications on the conservation of wandering albatrosses

Currently there are several important fisheries within the foraging range of the Wandering

Albatross: i) The Longline fishery that is more intense near the continental shelfs of this region,

and therefore, closer to the breeding grounds of these seabirds; Ii) The Southern Blue-fin tuna

(SBT) Longline fishery, working south of 30ºS and north of 40ºS in the open ocean ( Xavier et

al., 2004; Nel et al., 2002; Weimerskirch et al., 1998).

As previously stated (in the Introduction), during the initial stages of the chick rearing period of

the Albatross, forage trip are shortest, and therefore, nearer their colony (Weimerskirch et al.,

1993; Nel et al., 2002; Xavier et al. 2004). During this time, albatrosses are more prone to follow

longline fishing vessels ( Xavier et al., 2004). Apart from this delicate period of development of

the chicks, trips tend to get further away from the colonies to avoid competition with the animals

that feed near the islands (seals, other smaller albatrosses) (Xavier et al., 2004), with females

going more northwards than males (Xavier et al. 2004; Weimerskirch et al.,1998; Weimerskirch

et al., 1993; Nel et al., 2002). During these trips is when Albatrosses get in contact with the SBT

fishery, especially females (Birdlife Internacional 2010; Nel et al., 2002; Xavier et al., 2004).

Mean Carbon signature of the cephalopods found on the diet of albatrosses can give us

information about the overall origin of the stocks these seabirds depend, and in a lesser degree,

where are these populations taking more foraging efforts. Taking this last thought into account,

according to the results gathered in the current study (Table 3.10), on average South Georgia

Wandering albatrosses are foraging in the APFZ waters (North of South Georgia), whereas in the

Indian sector, Crozet and Kerguelen Wanderers are in the Subantarctic (South and North of their

breeding colonies respectively), in agreement with previous studies (Xavier et al., 2004; Xavier

& Croxall, 2007; Weimerskirch et al., 1993).

In South Georgia, the main preys of D. exulans are the Antarctic K. longimana and Sub Antarctic

T .sp. B (Voss) (this study; Xavier et al., 2004; Rodhouse et al.,1987). Only these species

account for near half of the beaks found on the diet. Therefore, in South Georgia, D. exulans is

dependent on Antarctic and Subantarctic squids, rarely venturing to Subtropical waters (Xavier

et al. 2004), making them particularly exposed to the Patagonian Toothfish longliners around

South Georgia, and potentially in the Subantarctic, with Tuna fisheries. In some years, Illex

argentinus is the predominant species on the diet of D. exulans, which shows that they forage at

61

the Patagonian shelf too, overlapping with the longline fisheries known to operate there (Xavier

et al. 2004)

In Crozet, the main preys of wandering albatrosses, K. longimana and H. eltaninae seem to share

the same pattern as the one shown in South Georgia i.e. high abundance of Antarctic and

Subantarctic squid in the diet of D.exulans. This shows that, in Crozet, D.exulans forage mainly

in the Subantarctic water South of the Crozet archipelago and also near the Kerguelen plateau

(Weimerskirch et al., 1997), susceptible to the Patagonian Toothfish longliners, and more

exposed to the SBT fishery as showed in previous studies (Birdlife international 2010; Nel et al.,

2002; Weimerskirch et al., 1993).

In Kerguelen, the main squid found in the diet are different from the other two islands. In here,

the subtropical species H. atlantica accounts for a third of the beaks found, followed by G.

glacialis (Subantarctic, but near the STF) with 13% of the beaks, and finally K. longimana with a

tenth of the beaks. This shows an inversion of the trend shown by the other two islands, where

there was a dominance of Antarctic and Subantarctic species, while here, it is a subtropical

species that dominates the diet (by numbers). However, as this was a one year sampling, there is

the possibility that the dominance of H. atlantica was characteristic only for that year (1998) as

previously stated (this study; Cherel et al., 2004). Leaving to 2 possible conclusions: i) Or

D.exulans are feeding further north than in the other islands, leaving them deep in SBT fisheries

grounds or ii) the abundance of H.atlantica in this year was abnormal, and therefore, D.exulans

feeds in Subantarctic waters near Kerguelen and mainly close to the STF, exposed to being

bycatched in one of the longliners and by the SBT fishery respectively.

62

5. FINAL CONSIDERATIONS

Cephalopods in this ocean are truly important in the food web, as they occupy almost all trophic

positions from the second consumers (eating copepods and euphausiids), to the top predators at

the sixth trophic level, passing by the fifth trophic level gelatinous predators of the mesopelagic

and benthopelagic realm. By the analysis of the diet of D. exulans performed in this study,

onychoteuthids (specially K. longimana) dominated the diet of D. exulans , with histioteuthids,

cranchiids and giant teuthids playing also a relevant role (specifically in Kerguelen). D. exulans

scavenges squid for food, even if it is not provided by fishing vessels. The Indian sector diet had

more cephalopod diversity then the Atlantic sector, as the former is geographically located nearer

the subtropical region, and the latter is further south in Antarctic waters. Also, D. exulans feeds

in the three main water masses of the Southern Ocean (Antarctic, Subantarctic and subtropical

waters) except for the birds found in South Georgia, as the squids analyzed using stable isotopes

showed (only Antarctic and Subantarctic). The habitat use of the squid species in this ocean, and

their contribution to the diet of D. exulans point out for the threat that longliners operating near

the continental shelves of the breeding colonies pose for their survival, while the Tuna fisheries

further north only are a threat to the Kerguelen population, if H. atlantica is truly the main diet

component of D. exulans in here.

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7. ANNEXS

72

Table 7.1 – Alometric equations chosen from Xavier & Cherel (2009). Legend: a- Chiroteuthid family

formula; b- Brachioteuthid family formula; c- Cranchiid family formula; d- Taonius spp. formula; e-

Gonatus spp. Formula; f- Cycloteuthis akimushkini formulas; g- Galiteuthis glacialis formula.

Family (according to

(Clarke, 1986)) Species ML

ANCISTROCHEIRIDAE Ancistros lesueri (Clarke, 1986)

ARCHITEUTHIDAE Architeuthis dux (Clarke, 1986)

BATHYTEUTHIDAE Bathyteuthis abyssicola (Clarke, 1986)

BATOTEUTHIDAE Batoteuthis skolops (Clarke, 1986) a

BRACHIOTEUTHIDAE Slosarczykovia circumantarctica (Clarke, 1986) b

CHIROTEUTHIDAE Chiroteuthis veranyi (Clarke, 1986)

CRANCHIDAE Cranchiids -

CRANCHIDAE Galiteuthis glacialis (Lu & Williams, 1994)

CRANCHIDAE Galiteuthis stC sp.(Imber) (Lu & Williams, 1994) g

CRANCHIDAE Galiteuthis sp. 3(Imber) (Lu & Williams, 1994) g

CRANCHIDAE Taonius sp.B(Voss) (Rodhouse et al., 1990) d

CRANCHIDAE Taonius sp.(Clarke) (Rodhouse et al., 1990) d

CRANCHIDAE Teuthowenia pellucida (Rodhouse et al., 1990)

CRANCHIDAE Mesonichoteuthis hamiltoni (Rodhouse et al., 1990)

CYCLOTEUTHIDAE Cycloteuthis akimushkini (Clarke, 1986)

GONATIDAE Gonatus antarcticus (Clarke, 1986) e

HISTIOTEUTHIDAE Histioteuthis bonnellii corpuscula (Lu & Ickeringill, 2002)

HISTIOTEUTHIDAE Histioteuthis macrohista (Lu & Ickeringill, 2002)

HISTIOTEUTHIDAE Histioteuthis miranda (Lu & Ickeringill, 2002)

HISTIOTEUTHIDAE Histioteuthis atlantica (Lu & Ickeringill, 2002)

HISTIOTEUTHIDAE Histioteuthis eltaninae (Lu & Ickeringill, 2002)

LEPIDOTEUTHIDAE Lepidoteuthis grimaldii BAS unpublished

LYCOTEUTHIDAE Lycoteuthis logira (Lu & Ickeringill, 2002)

MASTIGOTEUTHIDAE Mastigoteuthis psychrophila BAS unpublished

MASTIGOTEUTHIDAE ?Mastigoteuthis A(Clarke) (Clarke, 1986)

NEOTEUTHIDAE Alluroteuthis antarcticus (Piatkowski et al., 2001)

NEOTEUTHIDAE Nototeuthis dimegacotyle (Piatkowski et al., 2001)

OCTOPOTEUTHIDAE Taningia danae (Clarke, 1986)

OCTOPOTEUTHIDAE Octopoteuthis sp. (Clarke, 1986)

OMMASTREPHIDAE Martialia hyadesi (Rodhouse & Yeatman, 1990)

OMMASTREPHIDAE Ilex argentinus (Santos & Haimovici, 2000)

OMMASTREPHIDAE Todarodes sp. (Clarke, 1986)

ONYCHOTEUTHIDAE Kondakovia longimana (Brown & Klages, 1987)

ONYCHOTEUTHIDAE Moroteuthis ingens (Jackson, 1995)

ONYCHOTEUTHIDAE Moroteuthis knipovitch Cherel unpublished

ONYCHOTEUTHIDAE Moroteuthis robsoni (Lu & Ickeringill, 2002)

73

ONYCHOTEUTHIDAE Moroteuthis sp.B(Imber) Cherel unpublished

ONYCHOTEUTHIDAE Onychoteuthis banksii (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Onychoteuthis sp. C(Imber) (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Onychoteuthis sp. 2 (Imber) (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Onychoteuthis sp. B(Imber) (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Notonykia africanae Cherel unpublished

PSYCHROTEUTHIDAE Psychroteuthis glacialis (Gröger et al., 2000)

ALLOPOSIDAE Haliphron atlanticus -

?Discoteuthis (Clarke, 1986) f

Family (according to

(Clarke, 1986)) Species W

ANCISTROCHEIRIDAE Ancistros lesueri (Clarke, 1986)

ARCHITEUTHIDAE Architeuthis dux (Clarke, 1986)

BATHYTEUTHIDAE Bathyteuthis abyssicola (Clarke, 1986)

BATOTEUTHIDAE Batoteuthis skolops (Clarke, 1986) a

BRACHIOTEUTHIDAE Slosarczykovia circumantarctica (Clarke, 1986) b

CHIROTEUTHIDAE Chiroteuthis veranyi (Clarke, 1986)

CRANCHIDAE Cranchiids (Clarke, 1962b)

CRANCHIDAE Galiteuthis glacialis (Lu & Williams, 1994)

CRANCHIDAE Galiteuthis stC sp.(Imber) (Clarke, 1962b) c

CRANCHIDAE Galiteuthis sp. 3(Imber) (Clarke, 1962b) c

CRANCHIDAE Taonius sp.B(Voss) (Rodhouse et al., 1990) d

CRANCHIDAE Taonius sp.(Clarke) (Rodhouse et al., 1990) d

CRANCHIDAE Teuthowenia pellucida (Rodhouse et al., 1990)

CRANCHIDAE Mesonichoteuthis hamiltoni (Clarke, 1962b) c

CYCLOTEUTHIDAE Cycloteuthis akimushkini (Clarke, 1986)

GONATIDAE Gonatus antarcticus (Clarke, 1986) e

HISTIOTEUTHIDAE

Histioteuthis bonnellii

corpuscula (Lu & Ickeringill, 2002)

HISTIOTEUTHIDAE Histioteuthis macrohista (Lu & Ickeringill, 2002)

HISTIOTEUTHIDAE Histioteuthis miranda (Lu & Ickeringill, 2002)

HISTIOTEUTHIDAE Histioteuthis atlantica (Lu & Ickeringill, 2002)

HISTIOTEUTHIDAE Histioteuthis eltaninae (Lu & Ickeringill, 2002)

LEPIDOTEUTHIDAE Lepidoteuthis grimaldii BAS unpublished

LYCOTEUTHIDAE Lycoteuthis logira (Lu & Ickeringill, 2002)

MASTIGOTEUTHIDAE Mastigoteuthis psychrophila BAS unpublished

MASTIGOTEUTHIDAE ?Mastigoteuthis A(Clarke) (Clarke, 1986)

NEOTEUTHIDAE Alluroteuthis antarcticus (Piatkowski et al., 2001)

NEOTEUTHIDAE Nototeuthis dimegacotyle (Piatkowski et al., 2001)

OCTOPOTEUTHIDAE Taningia danae (Clarke, 1986)

OCTOPOTEUTHIDAE Octopoteuthis sp. (Clarke, 1986)

74

OMMASTREPHIDAE Martialia hyadesi (Rodhouse & Yeatman, 1990)

OMMASTREPHIDAE Ilex argentinus (Santos & Haimovici, 2000)

OMMASTREPHIDAE Todarodes sp. (Clarke, 1986)

ONYCHOTEUTHIDAE Kondakovia longimana (Brown & Klages, 1987)

ONYCHOTEUTHIDAE Moroteuthis ingens (Jackson, 1995)

ONYCHOTEUTHIDAE Moroteuthis knipovitch Cherel unpublished

ONYCHOTEUTHIDAE Moroteuthis robsoni (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Moroteuthis sp.B(Imber) Cherel unpublished

ONYCHOTEUTHIDAE Onychoteuthis banksii (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Onychoteuthis sp. C(Imber) (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Onychoteuthis sp. 2 (Imber) (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Onychoteuthis sp. B(Imber) (Lu & Ickeringill, 2002)

ONYCHOTEUTHIDAE Notonykia africanae Cherel unpublished

PSYCHROTEUTHIDAE Psychroteuthis glacialis (Gröger et al., 2000)

ALLOPOSIDAE Haliphron atlanticus BAS unpublished

?Discoteuthis (Clarke, 1986) f

75

Table 7.2 – Distribution of mantle length (ML), weight (W) and LRL from all squids found on D. exulans diet

in the South Georgia, Crozet and Kerguelen islands.

South Georgia

Species Weight

mean

sd

min

max

Haliphron atlanticus 482.63

165.14

243.95

844.36

Alluroteuthis antarcticus 437.86

120.04

125.44

924.09

Ancistrocheirus lesueuri 1324.24

403.90

883.54

1676.79

Batoteuthis skolops 39.59

20.77

15.26

113.12

Brachioteuthis ?picta (Clarke) 14.45

0

14.45

14.45

Brachioteuthis ?picta (Rodhouse) 7.78

0

7.78

7.78

Mastigoteuthis sp. A 151.27

49.49

60.61

352.75

Chiroteuthis veranyi 95.23

39.39

67.38

123.08

Nototeuthis dimegacotyle 133.94

37.50

86.77

187.86

Galiteuthis glacialis 102.98

20.45

54.89

154.38

Gonatus antarcticus 228.12

112.49

30.57

573.51

Histioteuthis atlantica 295.28

70.41

158.16

468.79

Histioteuthis eltaninae 67.44

17.25

18.55

120.68

Histioteuthis corpuscula 97.97

29.26

61.95

125.79

Histioteuthis macrohista 101.54

22.61

69.23

138.48

Histioteuthis miranda 468.77

157.70

261.02

699.44

Illex argentinus 363.09

230.98

146.72

783.58

Kondakovia longimana 2709.54

978.52

136.78

5903.99

Lepidoteuthis 3327.68

0

3327.68

3327.68

Martialia hyadesi 219.93

46.52

180.23

271.11

Mastigoteuthis psychrophila 68.78

1.99

67.38

70.19

Moroteuthis ingens 1729.76

0

1729.76

1729.76

Moroteuthis knipovitchi 695.41

424.50

250.62

2057.44

Moroteuthis robsoni 1852.95

595.67

1362.61

2515.84

Psychroteuthis glacialis 135.32

0

135.32

135.32

Taningia danae 4609.20

2693.68

1520.51

6471.19

Taonius sp. B(Voss) 290.90

69.66

88.17

444.22

Species Mantle Length

mean

sd

min

max

Haliphron atlanticus 0

0

0

0


16.87

114.67

230.13


29.39

248.03

305.08


17.36

84.78

165.5


0

107.12

107.12

76


0

74.832

74.832


20.16

133.7

246.22


22.48

138.59

170.39


11.87

100.67

132.16


40.48

341.82

542.9


41.25

102.36

308.13


14.07

99.918

161.5


7.06

52.654

99.166


6.27

47.54

61.256


4.16

47.186

60.2


16.09

110.18

156.37


52.40

197.48

346.49


64.03

175.44

630.72

Lepidoteuthis 571.96

0

571.96

571.96


13.50

219.88

246.4


0.44

121.1

121.72


0

377.07

377.07


60.09

231.09

480.56


46.14

494.92

585.54


0

169.68

169.68


241.76

270.52

706.8

Taonius sp. B(Voss) 555.3

66.31

319.42

681.86

Species LRL

mean

sd

min

max

Haliphron atlanticus 12.51

2.92

7.9

18.6


0.48

3.4

6.7


0.72

7.1

8.5


0.71

3

6.3


0

4.5

4.5


0

2.9

2.9


0.82

5

9.6


0.92

5.2

6.5


0.34

3

3.9


0.48

4

6.4


0.96

3.4

8.2


0.55

4.3

6.7


0.29

2.3

4.2


0.41

3

3.9


0.29

3.1

4


0.63

4.7

6.5

77


0.95

3.8

6.5


1.72

5.3

17.5

Lepidoteuthis 15.80

0

15.8

15.8


0.46

4

4.9


0.07

4.3

4.4


0

9.9

9.9


0.96

5.4

9.4


0.31

7.6

8.2


0

5.1

5.1


3.21

11

16.8

Taonius sp. B (Voss) 9.24

1.08

5.4

11.3

Crozet

Species Weight

mean

sd

min

max

?Discoteuthis sp. 365.57

71.35

315.12

416.02

?Mastigoteuthis A (Clarke) 284.07

72.31

143.33

444.16


100.55

236.96

745.97


559.94

1048.63

2510.12

Architeuthis dux 3050.94

0

3050.94

3050.94


10.12

15.40

59.31

Chiroteuthis sp. F 79.34

13.40

69.86

88.81


35.18

82.71

199.98

Cycloteuthis akimushkini 982.31

350.48

246.34

1768.64


14.93

55.20

147.05

Galiteuthis sp. 3 1291.05

195.39

1152.89

1429.21


87.61

114.16

504.43


107.39

76.69

559.20

Histioteuthis bonnellii corpuscula 260.12

63.53

85.48

381.15


19.15

18.55

211.44

Histioteuthis hoylei 672.01

13.07

662.77

681.25


38.65

84.80

162.26


146.34

523.74

1175.27


113.27

310.16

537.35


796.43

224.24

7227.75

Lepidoteuthis grimaldii 8030.96

1048.03

6055.73

9205.65

Lycoteuthis lorigera 137.90

45.51

105.72

170.08


128.64

302.01

921.33


8.46

48.87

70.48

78

Mesonychoteuthis hamiltoni 4404.21

2081.24

1839.50

6724.83


683.18

413.88

4149.35


354.75

318.13

1796.30


1823.92

3491.97

6948.05

Notonykia africanae 101.83

32.63

78.75

124.90


47.60

78.53

247.01

Octopoteuthis sp. 1514.85

330.45

1281.19

1748.51

Onychoteuthis banskii 26.73

0

26.73

26.73

Onychoteuthis sp. 2 (Imber) 15.99

0

15.99

15.99

Onychoteuthis sp. C (Imber) 62.94

41.83

33.36

92.51

Pholidoteuthis massaye 669.87

0

669.87

669.87

Slosarczykovia circumantarctica 6.07

0.80

5.51

6.63


1699.85

2172.67

7310.69

Taonius sp. (Clarke) 78.76

9.56

59.72

98.87


77.59

100.78

470.46

Teuthowenia pellucida 40.83

8.86

27.95

48.16

Todarodes sp. 937.51

789.77

454.46

1848.91


mean

sd

min

max


24.33

224.75

259.16


18.06

154.76

228.33


13.23

143.36

213.69


33.26

262.29

346.64


0

450.31

450.31


11.02

85.02

132.72


8.47

140.30

152.29


15.63

148.62

201.70


78.90

198.09

544.36


29.49

342.65

531.17


38.51

689.52

743.98


27.40

173.09

294.84


21.44

71.69

174.33


7.71

53.33

91.43


7.90

52.65

119.48


1.57

171.85

174.07


6.54

50.66

63.67


13.77

175.67

237.25


25.57

254.33

305.65


51.13

209.02

674.01


35.27

698.30

802.92

79


17.84

133.84

159.07


24.31

254.36

367.23


1.88

116.69

121.78


149.60

579.27

927.58


47.65

236.25

492.99


52.26

252.91

459.98


59.50

636.89

751.67


37.23

5.42

58.07


14.06

97.17

145.46


36.39

356.77

408.24


0

109.73

109.73


0

91.72

91.72


36.13

118.57

169.66


0

301.40

301.40


4.57

62.12

68.58


129.49

361.54

752.68


17.55

265.36

337.24


73.76

340.31

700.29


16.55

137.68

175.06


97.94

261.26

436.22

Species LRL

mean

sd

min

max


0.78

7.25

8.36


0.62

5.26

7.79


0.38

4.22

6.23


0.82

7.45

9.52


0

8.53

8.53


0.45

3.01

4.96


0.35

5.27

5.76


0.64

5.61

7.78


2.55

6.39

17.56


0.35

4.01

6.26


0.46

8.15

8.80


0.64

5.05

7.89


0.84

3.20

7.20


0.51

3.38

5.88


0.32

2.30

5.03


0.07

8.35

8.45


0.45

3.34

4.24


0.40

5.91

7.71

80


0.46

4.83

5.76


1.37

6.20

18.66


0.97

19.29

22.18


0.52

4.25

4.98


0.83

5.17

9.00


0.30

3.59

4.41


2.44

9.63

15.30


1.04

5.82

11.67


0.84

5.75

9.07


0.39

8.54

9.30


0.35

3.55

4.05


0.40

2.90

4.28


2.10

20.61

23.58


0

26.73

26.73


0

15.99

15.99


1.10

3.55

5.11


0

7.06

7.06


0.23

2.27

2.59


1.72

12.21

17.41


0.29

4.52

5.69


1.20

5.74

11.60


0.55

3.86

5.11

Todarodes sp. 8.09

2.37

6.59

10.82

Kerguelen

Species Weight

mean

sd

min

max


113.27

107.50

493.46


102.55

228.79

701.07


639.23

99.08

2336.28


16350.63

1877.20

45525.42


16.51

26.30

81.12


39.82

96.95

234.29


322.37

286.14

1852.07


13.91

50.18

148.60


231.69

1056.58

1512.58

Galiteuthis Stc sp. 758.05

189.98

638.66

1041.67


105.19

140.07

523.85


101.80

43.55

678.21

81


65.27

142.09

382.91


15.60

24.34

107.77


78.61

412.44

554.57


20.19

112.84

193.09


252.18

57.05

1217.48


1034.12

1097.05

7701.93


0

8291.41

8291.41


111.97

214.35

669.61


5.96

45.76

69.62


0

4270.92

4270.92


741.94

1922.40

3769.18


303.82

328.77

1594.62


3446.28

2828.79

13740.81

Moroteuthis sp. B 330.23

168.20

147.92

500.90


0

47.76

47.76


41.22

153.33

301.53


266.14

235.51

1525.89


0

29.81

29.81


0

12.22

12.22

Onychoteuthis sp. B 119.55

0

119.55

119.55

Onychoteuthis sp. C 86.00

11.77

68.50

107.98


41.16

347.42

429.28


2669.42

1834.14

13040.49


7.17

60.88

88.17


74.70

138.64

482.08


5.40

30.53

52.07


86.14

298.44

550.08


mean

sd

min

max


27.66

140.22

236.77


14.05

141.61

209.14


55.70

115.18

338.90


168.74

399.31

858.37


13.82

101.17

147.64


16.29

156.94

213.20


71.57

213.90

557.38


27.39

328.41

533.68


45.75

668.58

759.07


49.33

559.66

665.23


31.28

186.81

298.70

82


19.10

54.76

189.47


7.29

64.00

91.58


7.07

57.79

95.49


11.42

137.43

158.08


2.95

56.01

67.72


35.11

70.99

240.33


56.57

360.53

688.19


0.00

775.40

775.40


23.77

230.49

328.33


1.42

115.89

121.59


0

786.90

786.90


38.11

383.20

477.82


46.80

256.03

442.52


88.04

603.66

875.51


52.29

187.43

298.44


0

111.96

111.96


9.12

123.06

155.95


46.49

171.17

384.85


0

113.99

113.99


0

83.53

83.53


0

185.71

185.71


7.90

152.63

179.16


28.70

308.71

365.77


163.14

317.16

994.14


13.59

267.82

319.42


66.83

395.60

708.27


9.53

143.07

181.34


19.45

223.62

280.29

Species LRL

mean

sd

min

max


0.95

4.76

8.08


0.40

4.17

6.10


1.37

3.84

9.33


2.85

7.67

15.41


0.57

3.67

5.57


0.67

5.95

8.25


2.31

6.90

17.98


0.33

3.84

6.29


0.55

7.90

8.98


0.59

6.60

7.86

83


0.73

5.37

7.98


0.74

2.54

7.79


0.48

4.08

5.89


0.29

2.51

4.05


0.51

6.80

7.73


0.20

3.71

4.52


1.03

2.85

7.80


1.52

10.26

19.04


0

21.42

21.42


0.81

4.36

7.68


0.23

3.46

4.38


0

13.01

13.01


0.85

9.21

11.33


0.75

5.80

8.79


0.58

8.32

10.12


0.84

4.70

6.48


0

3.49

3.49


0.26

3.64

4.58


2.68

9.90

22.23


0

3.41

3.41


0

5.60

5.60


0

2.48

2.48


0.24

4.59

5.40


0.28

7.14

7.70


2.17

11.62

20.62


0.22

4.56

5.40


1.09

6.64

11.73


0.32

4.04

5.32

Todarodes sp. 6.28

0.47

5.68

7.05

84

Table 7.3 – All squid items found on the D. exulans diet throughout the three studied isands, and their

respective contributions to the diet in terms of frequency, numeric and mass indexes.

South Georgia

F%

N%

W%

Species Lower beaks N%

Weight

W%

Haliphron atlanticus 52.63 14 1.05

6756.84

0.58

Alluroteuthis antarcticus 94.74 106 7.98

46413.33

4.02

Ancistrocheirus lesueuri 15.79 3 0.23

3972.72

0.34

Batoteuthis skolops 57.89 29 2.18

1148.21

0.10

Brachioteuthis ?picta (Clarke) 5.26 1 0.08

14.45

0.00

Brachioteuthis ?picta (Rodhouse) 5.26 1 0.08

7.78

0.00

Mastigoteuthis sp. A 78.95 52 3.91

7866.27

0.68

Chiroteuthis veranyi 10.53 2 0.15

190.47

0.02

Nototeuthis dimegacotyle 21.05 6 0.45

803.66

0.07

Galiteuthis glacialis 84.21 60 4.51

6178.96

0.53

Gonatus antarcticus 89.47 91 6.85

20758.55

1.80

Histioteuthis atlantica 89.47 77 5.79

22736.26

1.97

Histioteuthis eltaninae 100.00 141 10.61

9509.20

0.82

Histioteuthis corpuscula 21.05 4 0.30

391.86

0.03

Histioteuthis macrohista 42.11 16 1.20

1624.65

0.14

Histioteuthis miranda 42.11 12 0.90

5625.19

0.49

Illex argentinus 26.32 6 0.45

2178.55

0.19

Kondakovia longimana 94.74 322 24.23

872472.44

75.50

Lepidoteuthis 5.26 1 0.08

3327.68

0.29

Martialia hyadesi 10.53 3 0.23

659.80

0.06

Mastigoteuthis psychrophila 10.53 2 0.15

137.57

0.01

Moroteuthis ingens 5.26 1 0.08

1729.76

0.15

Moroteuthis knipovitchi 68.42 43 3.24

29902.49

2.59

Moroteuthis robsoni 10.53 3 0.23

5558.84

0.48

Octopodid 10.53 2 0.15

0

0

Psychroteuthis glacialis 5.26 1 0.08

135.32

0.01

Taningia danae 10.53 3 0.23

13827.61

1.20

Taonius sp. B (Voss) 100.00 315 23.70

91633.47

7.93

Unknown

12 0.90

-

-

Crozet

N%

W%

Species F% Lower beaks N%

Weight

W%

?Discoteuthis sp. 6.06 2 0.05

731.14

0.02

?Mastigoteuthis A (Clarke) 54.55 33 0.85

9374.47

0.25

85


50718.84

1.35


12011.73

0.32

Architeuthis dux 12.12 4 0.10

12203.74

0.32


3847.70

0.10

Chiroteuthis sp. F 6.06 2 0.05

158.67

0.00


2582.85

0.07

Cirrata sp. A 3.03 1 0.03

-

-

Cycloteuthis akimushkini 57.58 38 0.97

37327.71

0.99


36520.81

0.97

Galiteuthis sp. 3 6.06 2 0.05

2582.10

0.07


12378.93

0.33


40568.63

1.08

Histioteuthis bonnellii corpuscula 60.61 42 1.08

10924.86

0.29


66984.65

1.78

Histioteuthis hoylei 6.06 2 0.05

1344.01

0.04


480.01

0.01


28080.96

0.75

Histioteuthis sp. 6.06 2 0.05

250.00

0.01

Illex argentinus 9.09 4 0.10

1689.13

0.04


2856984.12

75.95

Lepidoteuthis grimaldii 18.18 7 0.18

56216.74

1.49

Lycoteuthis lorigera 6.06 2 0.05

275.80

0.01


89515.06

2.38


344.47

0.01

Mesonychoteuthis hamiltoni 12.12 5 0.13

22021.04

0.59


222159.54

5.91


111831.96

2.97


14649.25

0.39

Notonykia africanae 9.09 3 0.08

305.48

0.01


1453.94

0.04

Octopodidae 6.06 2 0.05

-

-

Octopoteuthis sp. 6.06 2 0.05

3029.70

0.08

Oegopsida sp. A 6.06 2 0.05

-

-

Onychoteuthis banskii 3.03 1 0.03

26.73

0.00

Onychoteuthis sp. 2 (Imber) 3.03 1 0.03

15.99

0.00

Onychoteuthis sp. C (Imber) 6.06 2 0.05

125.88

0.00

Pholidoteuthis massaye 3.03 1 0.03

669.87

0.02

Slosarczykovia circumantarctica 9.09 3 0.08

18.21

0.00

Stauroteuthis gilchristi 3.03 1 0.03

-

-


27956.29

0.74

Taonius sp. (Clarke) 48.48 39 1.00

3071.73

0.08

Taonius sp. B (Voss) 57.58 64 1.64

16211.15

0.43

Teuthowenia pellucida 12.12 4 0.10

163.32

0.00

86

Todarodes sp. 9.09 4 0.10

3750.04

0.10

Unknown (eroded) 45.45 40 1.02

-

-

Unknown uneroded 3.03 1 0.03

-

-

Kerguelen

F%

N%

W%

Species Lower beaks N%

Weight

W%

?Mastigoteuthis A (Clarke) 23.33 11 0.41

3509.07

0.15


42944.66

1.85


29871.86

1.29

Architeuthis dux 63.33 22 0.82

347948.84

15.00


1916.51

0.08


3014.40

0.13

Cycloteuthis akimushkini 86.67 86 3.22

84344.37

3.64


35501.92

1.53

Galiteuthis sp. 3 10.00 3 0.11

3782.45

0.16

Galiteuthis Stc sp. 10.00 4 0.15

3032.19

0.13


11958.77

0.52


298847.28

12.89

Histioteuthis bonnellii corpuscula 53.33 21 0.79

5340.62

0.23


11517.83

0.50

Histioteuthis hoylei 10.00 6 0.22

2899.57

0.13


3533.00

0.15


27180.40

1.17

Histioteuthis sp. 6.67 2 0.07

-

-


719800.35

31.04

Lepidoteuthis grimaldii 3.33 1 0.04

8291.41

0.36


41121.75

1.77


942.73

0.04

Mesonychoteuthis hamiltoni 3.33 1 0.04

4270.92

0.18


20906.04

0.90


45613.24

1.97


158329.95

6.83

Moroteuthis sp. B 16.67 5 0.19

1651.15

0.07

Notonykia africanae 3.33 1 0.04

47.76

0.00


5725.19

0.25

Octopodidae 16.67 5 0.19

-

-

Octopoteuthis sp. 30.00 24 0.90

13201.87

0.57

Oegopsida sp. B 10.00 5 0.19

-

-

Onychoteuthis banskii 3.33 2 0.07

59.62

0.00

Onychoteuthis sp. 2 (Imber) 3.33 1 0.04

12.22

0.00

87

Onychoteuthis sp. B 3.33 1 0.04

119.55

0.01

Onychoteuthis sp. C 30.00 11 0.41

946.01

0.04

Psychroteuthis glacialis 10.00 4 0.15

1557.89

0.07


306242.20

13.21

Taonius sp. (Clarke) 60.00 56 2.10

4147.72

0.18

Taonius sp. B (Voss) 53.33 181 6.77

57427.09

2.48

Teuthowenia pellucida 66.67 31 1.16

1283.98

0.06

Todarodes sp. 36.67 25 0.94

10056.59

0.43

Unknown (eroded) 36.67 15 0.56

-

-

88

Table 7.4 – Chi-squared results on the diet indexes (Frequency of occurrence (F%), numeric (N%) and mass

(W%) indexes).

F%

Species Crozet

South Georgia

Kerguelen


0.02

0.00


0.10

0.37


0.01

0.01


0.37

0.03


0.00

0.00


0.12

0.00


0.01

0.00


0.02

0.02


0.09

0.18


0.01

0.01


0.01

0.01


0.12

0.41


0.65

0.13

Mastigoteuthis sp. A(Clarke) 0.00

0.44

0.33


0.27

0.52


0.73

0.27


0.01

0.00


0.22

1.03


0.28

0.63

Octopodidae 0.23

0.00

0.19

Taningia danae 0.10

0.29

0.60

Taonius sp.B (Voss) 0.05

0.32

0.08

Sum of χ2= 13.26

Degrees of freedom= 40

p-value= 0.99

N%

Species Crozet

South Georgia

Kerguelen


1.36

0.02


0.16

0.95


0.00

0.16


0.47

0.10


0.26

0.10


3.20

0.09


0.30

1.84


0.14

0.28

89


1.35

0.38


0.02

0.11


0.00

0.34


0.11

0.45


0.87

0.01

Mastigoteuthis sp A(Clarke) 0.09

4.94

0.44


0.25

0.95


0.93

0.77


0.00

0.04


0.15

1.81


0.00

0.75

Octopodidae 0.30

0.10

0.41

Taonius sp B (Voss 0.59

5.50

0.00

OTHERS 0.07

0.36

0.46

Taningia danae 0.56

0.39

1.97

Sum of χ2= 39.68


p-value= 0.66

W%

Species Crozet

South Georgia

Kerguelen


1.00

0.00


0.23

0.98


0.00

0.02


0.64

0.35


0.27

0.15


3.15

0.04


0.39

2.32


0.12

0.36


0.54

0.84


0.20

0.13


0.03

0.26


0.50

0.39


0.94

0.00

Mastigoteuthis sp. A(Clarke 0.01

1.65

0.23


0.17

1.05


0.92

0.55


0.00

0.07


0.66

2.93


0.15

1.42

Taonius sp. B Voss 0.65

5.49

0.00

90

OTHERS 4.29

0.92

13.66

Taningia danae 0.71

0.58

2.85

Sum of χ2= 57.57


p-value= 0.055

Documents

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