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 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
7 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
Figure 3.4 Lower Rostral Length (LRL) distribution of the squids found on the diet of 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
Figure 3.6 Lower Rostral Length (LRL) distribution of the squids found on the diet of 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
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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
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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)
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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
16 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
17 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.,
18 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).
19
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 (CO 2) 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 CO 2 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.
20
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
21 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 Clean and separation in upper and lower beaks (Xavier et al . Beak 2003a). Upper beak Counted
Counted, measurement of lower rostral length (LRL) with callipers with a precision of a tenth of a millimeter and Lower beak 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:
;
22
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).
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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.
24
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.
25
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
26
(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 ).
27
Figure 3.2 – Lower Rostral Length (LRL) distribution of the squids found on the diet of Wandering Albatross in South Georgia.
28
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)
Haliphron 12.51 ± 2.92 - 482.63 ± 165.14 Alloposidae atlanticus 7.90 - 18.60 - 243.95 - 844.36
Architeuthis - - - Architeuthidae dux
Batoteuthis 4.17 ± 0.71 113.37 ± 17.36 39.59 ± 20.77 Batoteuthidae skolops 3.00 - 6.30 84.78 - 165.50 15.26 - 113.12
Galiteuthis 5.30 ± 0.48 450.60 ± 40.48 102.98 ± 20.45
glacialis 4.00 - 6.40 341.82 - 542.90 54.89 - 154.38
Taonius - - - Cranchidae sp.(Clarke)
Taonius sp.B 9.24 ± 1.08 555.30 ± 66.31 290.90 ± 69.66
(Voss) 5.40 - 11.30 319.42 - 681.86 88.17 - 444.22
Cycloteuthis - - - Cycloteuthidae akimushkini
Gonatus 6.05 ± 0.96 215.94 ± 41.25 228.12 ± 112.49 Gonatidae antarcticus 3.40 - 8.20 102.36 - 308.13 30.57 - 573.51
Histioteuthis 5.51 ± 0.55 130.95 ± 14.07 295.28 ± 70.41
atlantica 4.30 - 6.70 99.92 - 161.50 158.16 - 468.79
Histioteuthis 3.46 ± 0.29 81.01 ± 7.06 67.44 ± 17.25 Histioteuthidae eltaninae 2.30 - 4.20 52.65 - 99.17 18.55 - 120.68
Histioteuthis 5.63 ± 0.63 134.13 ± 16.09 468.77 ± 157.70
miranda 4.70 - 6.50 110.18 - 156.37 261.02 - 699.44
Mastigoteuthis 6.93 ± 0.82 181.02 ± 20.16 151.27 ± 49.49 Mastigoteuthidae sp.A (Clarke) 5.00 - 9.60 133.70 - 246.22 60.61 - 352.75
Alluroteuthis 5.16 ± 0.48 176.10 ± 16.88 437.86 ± 120.04 Neoteuthidae antarcticus 3.40 - 6.70 114.67 - 230.13 125.44 - 924.09
Martialia 4.40 ± 0.46 231.67 ± 13.50 219.93 ± 46.52 Ommastrephidae hyadesi 4.00 - 4.90 219.88 - 246.40 180.23 - 271.11
29
Kondakovia 13.45 ± 1.72 479.46 ± 64.04 2709.54 ± 978.52
longimana 5.30 - 17.50 175.44 - 630.72 136.78 - 5903.99
Moroteuthis 9.90 377.07 1729.76 ingens Onychoteuthidae Moroteuthis 6.87 ± 0.96 322.81 ± 60.09 695.41 ± 424.50
knipovitchi 5.40 - 9.40 231.09 - 480.56 250.62 - 2057.44
Moroteuthis 7.87 ± 0.31 535.19 ± 46.14 1852.95 ± 595.67
robsoni 7.60 - 8.20 494.92 - 585.54 1362.61 - 2515.84
Taningia 14.70 ± 3.21 548.83 ± 241.76 4609.20 ± 2693.68 Octopoteuthidae danae 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)
Haliphron Alloposidae - - - atlanticus Architeuthis Architeuthidae 8.53 450.31 3050.94 dux
Batoteuthis 4.02 ± 0.45 109.82 ± 11.02 34.66 ± 10.12 Batoteuthidae skolops 3.01 - 4.96 85.02 - 132.72 15.40 - 59.31
Galiteuthis 5.38 ± 0.35 457.83 ± 29.49 106.17 ± 14.93
glacialis 4.01 - 6.26 342.65 - 531.17 55.20 - 147.05
Taonius 5.12 ± 0.29 302.21 ± 17.55 78.76 ± 9.56 Cranchidae sp.(Clarke) 4.52 - 5.69 265.36 - 337.24 59.72 - 98.87
Taonius sp.B 8.65 ± 1.20 518.86 ± 73.76 253.30 ± 77.59
(Voss) 5.74 - 11.60 340.31 - 700.29 100.78 - 470.46
Cycloteuthis 12.76 ± 2.55 395.42 ± 78.90 982.31 ± 350.48 Cycloteuthidae akimushkini 6.39 - 17.56 198.09 - 544.36 246.34 - 1768.64
Gonatus 6.05 ± 0.64 215.75 ± 27.40 217.17 ± 87.61 Gonatidae antarcticus 5.05 - 7.89 173.09 - 294.84 114.16 - 504.43
Histioteuthis 5.64 ± 0.84 134.36 ± 21.44 319.44 ± 107.39
atlantica 3.20 - 7.20 71.69 - 174.33 76.69 - 559.20
Histioteuthis 3.46 ± 0.32 80.98 ± 7.90 67.73 ± 19.15 Histioteuthidae eltaninae 2.30 - 5.03 52.65 - 119.48 18.55 - 211.44
Histioteuthis 6.84 ± 0.40 207.56 ± 13.77 825.91 ± 146.34
miranda 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
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sp.A (Clarke) 5.26 - 7.79 154.76 - 228.33 143.33 - 444.16
Alluroteuthis 5.46 ± 0.38 186.70 ± 13.23 512.31 ± 100.55 Neoteuthidae antarcticus 4.22 - 6.23 143.36 - 213.69 236.96 - 745.97
Martialia 6.81 ± 0.83 302.57 ± 23.31 532.83 ± 128.64 Ommastrephidae hyadesi 5.17 - 9.00 254.36 - 367.23 302.01 - 921.33
Kondakovia 12.58 ± 1.37 447.30 ± 51.13 2174.27 ± 796.43
longimana 6.20 - 18.66 209.02 - 674.01 224.24 - 7227.75
Moroteuthis 8.70 ± 1.04 343.04 ± 47.65 1397.23 ± 683.18
ingens 5.82 - 11.67 236.25 - 492.99 413.88 - 4149.35 Onychoteuthidae Moroteuthis 7.30 ± 0.84 349.35 ± 52.26 840.84 ± 354.75
knipovitchi 5.75 - 9.07 252.91 - 459.98 318.13 - 1796.30
Moroteuthis 8.86 ± 0.39 685.22 ± 59.50 4883.08 ± 1823.92
robsoni 8.54 - 9.30 636.89 - 751.67 3491.97 - 6948.05
Taningia 15.07 ± 1.72 576.67 ± 129.49 4659.38 ± 1699.85 Octopoteuthidae danae 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)
Haliphron - - - Alloposidae atlanticus
Architeuthis 11.16 ± 2.85 606.10 ± 168.75 15815.86 ± 16350.63 Architeuthidae dux 7.67 - 15.41 399.31 - 858.37 1877.20 - 45525.42
Batoteuthis 4.71 ± 0.57 126.62 ± 13.82 53.24 ± 16.51 Batoteuthidae skolops 3.67 - 5.57 101.17 - 147.64 26.30 - 81.12
Galiteuthis 5.45 ± 0.33 463.27 ± 27.39 108.90 ± 13.91
glacialis 3.84 - 6.29 328.41 - 533.68 50.18 - 148.60
Taonius 4.98 ± 0.22 293.70 ± 13.59 74.07 ± 7.17 Cranchidae sp.(Clarke) 4.56 - 5.40 267.82 - 319.42 60.88 - 88.17
Taonius sp.B 9.62 ± 1.09 578.55 ± 66.83 317.28 ± 74.70
(Voss) 6.64 - 11.73 395.60 - 708.27 138.64 - 482.08
Cycloteuthis 12.78 ± 2.31 396.29 ± 71.57 980.75 ± 322.37 Cycloteuthidae akimushkini 6.90 - 17.98 213.90 - 557.38 286.14 - 1852.07
Gonatus 6.37 ± 0.73 229.64 ± 31.28 259.97 ± 105.19 Gonatidae antarcticus 5.37 - 7.98 186.81 - 298.70 140.07 - 523.85
Histioteuthis 6.05 ± 0.75 144.71 ± 19.10 374.03 ± 101.80 Histioteuthidae atlantica 2.54 - 7.79 54.76 - 189.47 43.55 - 678.21
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Histioteuthis 3.22 ± 0.29 75.23 ± 7.07 54.33 ± 15.60
eltaninae 2.51 - 4.05 57.79 - 95.49 24.34 - 107.77
Histioteuthis 6.41 ± 1.03 192.63 ± 35.11 715.27 ± 252.18
miranda 2.85 - 7.80 70.99 - 240.33 57.05 - 1217.48
Mastigoteuthis 6.84 ± 0.95 200.60 ± 27.66 319.01 ± 113.27 Mastigoteuthidae sp.A (Clarke) 4.76 - 8.08 140.22 - 236.77 107.50 - 493.46
Alluroteuthis 5.41 ± 0.40 184.93 ± 14.05 499.36 ± 102.55 Neoteuthidae antarcticus 4.17 - 6.10 141.61 - 209.14 228.79 - 701.07
Martialia 5.97 ± 0.81 278.05 ± 23.77 411.22 ± 111.97 Ommastrephidae hyadesi 4.36 - 7.68 230.49 - 328.33 214.35 - 669.61
Kondakovia 13.44 ± 1.52 479.37 ± 56.57 2685.82 ± 1034.12
longimana 10.26 - 19.04 360.53 - 688.19 1097.05 - 7701.93
Moroteuthis 10.49 ± 0.85 440.15 ± 38.11 2986.58 ± 741.94
ingens 9.21 - 11.33 383.20 - 477.82 1922.40 - 3769.18 Onychoteuthidae Moroteuthis 6.94 ± 0.75 327.06 ± 46.80 691.11 ± 303.82
knipovitchi 5.80 - 8.79 256.03 - 442.52 328.77 - 1594.62
Moroteuthis 9.17 ± 0.58 731.55 ± 88.04 6883.91 ± 3446.28
robsoni 8.32 - 10.12 603.66 - 875.51 2828.79 - 13740.81
Taningia 17.36 ± 2.17 748.56 ± 163.14 7656.06 ± 2669.42 Octopoteuthidae danae 11.62 - 20.62 317.16 - 994.14 1834.14 - 13040.49
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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
Galiteuthis glacialis 84.2 4.5 0.5 97.0 8.8 1.0 96.7 12.2 1.5
Cranchidae 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
Histioteuthis atlantica 89.5 5.8 2.0 84.8 3.3 1.1 96.7 29.9 12.9
Histioteuthidae 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
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 Onychoteuthidae 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‰).
33
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 LRL(mm) Nitrogen (‰) Carbon (‰) Family Species 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
Galiteuthis glacialis 5.30 ± 0.48 13.39 ± 1.10 -22.27 ± 0.82
Cranchidae 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
Histioteuthis atlantica 5.51 ± 0.55 16.34 ± 0.78 -20.17 ± 0.59
Histioteuthis atlantica - - 15.89 ± 0.58 -19.92 ± 0.48 small Histioteuthidae Histioteuthis atlantica - - 16.75 ± 0.72 -20.39 ± 0.61 Large Histioteuthis eltaninae 3.46 ± 0.29 14.28 ± 0.76 -22.66 ± 1.20
Histioteuthis miranda ------
Mastigoteuthis sp. A Mastigoteuthidae 6.93 ± 0.82 15.95 ± 0.46 -21.26 ± 0.75 (Clarke) Neoteuthidae Alluroteuthis antarcticus 5.16 ± 0.48 13.52 ± 0.98 -21.67 ± 1.46
Ommastrephidae Martialia hyadesi ------
Kondakovia longimana 13.45 ± 1.72 11.97 ± 0.38 -24.37 ± 1.59
Onychoteuthidae Moroteuthis ingens ------
Moroteuthis knipovitchi 6.87 ± 0.96 13.88 ± 0.63 -23.85 ± 1.00
Octopoteuthidae Taningia danae ------
34
18
19.5 20
22 22.3
24 δ 13C‰ 26
28
30 Galiteuthis glacialis Batoteuthis skolops Haliphron atlanticus Mean Taonius sp.B (Voss) Gonatus antarcticus Histioteuthis eltaninae
Moroteuthis knipovitchi Mean±SD Kondakovia longimana Histioteuthis atlantica L Histioteuthis atlantica S Alluroteuthis antarcticus Mean±2*SD ?Mastigoteuthis A (Clarke) 19
18
17
16
15
14 δ 15N‰ 13
12
11
10 Galiteuthis glacialis Haliphron atlanticus Batoteuthis skolops Mean Taonius sp.B (Voss) Gonatus antarcticus Histioteuthis eltaninae
Moroteuthis knipovitchi Mean±SD Kondakovia longimana Histioteuthis atlantica L Histioteuthis atlantica S Alluroteuthis antarcticus Mean±2*SD ?Mastigoteuthis A (Clarke)
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
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).
36
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‰).
37
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
LRL(mm) Nitrogen (‰) Carbon (‰) Family Species mean ± sd mean ± sd mean ± sd
Alloposidae Haliphron atlanticus ------
Batoteuthidae Batoteuthis skolops 4.02 ± 0.45 15.15 ± 0.69 -23.62 ± 0.50
Galiteuthis glacialis 5.38 ± 0.35 13.67 ± 0.55 -21.29 ± 0.53
Cranchidae Taonius sp. (Clarke) 5.12 ± 0.29 15.62 ± 0.42 -19.41 ± 0.30
Taonius sp. B (Voss) 8.65 ± 1.20 15.75 ± 0.80 -21.38 ± 1.05
Cycloteuthidae Cycloteuthis akimushkini 12.76 ± 2.55 - - - -
Gonatidae Gonatus antarcticus 6.05 ± 0.64 15.58 ± 0.61 -23.94 ± 1.18
Histioteuthis atlantica 5.64 ± 0.84 15.63 ± 0.65 -19.34 ± 0.20 Histioteuthis atlantica ------small Histioteuthis atlantica Histioteuthidae ------Large Histioteuthis eltaninae 3.46 ± 0.32 13.81 ± 0.32 -21.42 ± 0.56
Histioteuthis miranda 6.84 ± 0.40 - - - -
Mastigoteuthis sp. A Mastigoteuthidae 6.62 ± 0.62 13.73 ± 0.70 -21.42 ± 0.51 (Clarke) Neoteuthidae Alluroteuthis antarcticus 5.46 ± 0.38 13.01 ± 0.23 -21.29 ± 1.38
Ommastrephidae Martialia hyadesi 6.81 ± 0.83 8.4 ± 0.84 -22.57 ± 0.42
Kondakovia longimana 12.58 ± 1.37 12.22 ± 0.40 -22.60 ± 0.65
Onychoteuthidae Moroteuthis ingens 8.70 ± 1.04 12.69 ± 0.20 -21.79 ± 0.35
Moroteuthis knipovitchi 7.30 ± 0.84 12.81 ± 0.45 -22.09 ± 1.47
Octopoteuthidae Taningia danae ------
38
18
19 19.5 20
21
22 22.3 23 δ 13C‰ 24
25
26
27 Martialia hyadesi Galiteuthis glacialis Moroteuthis ingens Taonius sp.(Clarke) Batoteuthisskolops Gonatus antarcticus Taonius sp.B (Voss) Histioteuthis atlantica Histioteuthis eltaninae Moroteuthis knipovitchi Kondakovia longimana
Alluroteuthis antarcticus Mean
?Mastigoteuthis A (Clarke) Mean±SD Mean±2*SD
18
16
14
12 δ 15N‰ 10
8
6 Martialia hyadesi Galiteuthis glacialis Taonius sp.(Clarke) Moroteuthis ingens Batoteuthis skolops
Taonius sp.B (Voss) Gonatus antarcticus Mean Histioteuthis atlantica Histioteuthis Histioteuthis Histioteuthis eltaninae
Moroteuthis knipovitchi Mean±SD Kondakovia longimana Alluroteuthis antarcticus Mean±2*SD ?Mastigoteuthis A (Clarke)
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
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%).
40
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‰).
41
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 LRL(mm) Nitrogen (‰) Carbon (‰) Family Species mean ± sd mean ± sd mean ± sd
Alloposidae Haliphron atlanticus ------
Batoteuthidae Batoteuthis skolops 4.71 ± 0.57 15.1 ± 0.41 -23.69 ± 0.73
Galiteuthis glacialis 5.45 ± 0.33 13.26 ± 0.71 -21.07 ± 0.59
Cranchidae Taonius sp. (Clarke) 4.98 ± 0.22 16.28 ± 0.70 -19.28 ± 0.22
Taonius sp. B (Voss) 9.62 ± 1.09 16.61 ± 0.48 -21.85 ± 0.84
Cycloteuthidae Cycloteuthis akimushkini 12.78 ± 2.31 17 ± 0.52 -19.32 ± 0.32
Gonatidae Gonatus antarcticus 6.37 ± 0.73 15.04 ± 0.51 -22.48 ± 1.80
Histioteuthis atlantica 6.05 ± 0.75 15.74 ± 1.08 -19.41 ± 0.54
Histioteuthis atlantica - - 15.07 ± 0.97 -19.36 ± 0.40 small Histioteuthis atlantica Histioteuthidae - - 16.42 ± 0.69 -19.46 ± 0.66 Large Histioteuthis eltaninae 3.22 ± 0.29 13.51 ± 0.47 -21.50 ± 1.11
Histioteuthis miranda 6.41 ± 1.03 - - - -
Mastigoteuthis sp. A Mastigoteuthidae 6.84 ± 0.95 - - - - (Clarke) Neoteuthidae Alluroteuthis antarcticus 5.41 ± 0.40 13.2 ± 0.36 -20.70 ± 0.90
Ommastrephidae Martialia hyadesi 5.97 ± 0.81 9.26 ± 0.45 -21.75 ± 0.79
Kondakovia longimana 13.44 ± 1.52 12.59 ± 0.75 -22.34 ± 1.84
Onychoteuthidae Moroteuthis ingens ------
Moroteuthis knipovitchi 6.94 ± 0.75 13.44 ± 0.41 -23.71 ± 0.95
Octopoteuthidae Taningia danae 17.36 ± 2.17 16.64 ± 0.50 -20.68 ± 1.04
42
17
18
19 19.5 20
21
22 22.3
δ 13C‰ 23
24
25
26
27 Taningia danae Taningia
Martialia hyadesi Mean Galiteuthis glacialis Galiteuthis Batoteuthis skolops Taonius sp.(Clarke) Taonius Gonatus antarcticus Taonius sp.B (Voss) Taonius Mean±SD Histioteuthis eltaninae Histioteuthis Moroteuthis knipovitchi Kondakovia Kondakovia longimana Histioteuthis atlantica L atlantica Histioteuthis Histioteuthis atlantica S atlantica Histioteuthis
Alluroteuthis antarcticus Mean±2*SD Cycloteuthis akimushkini Cycloteuthis 20
18
16
14
δ 15N‰ 12
10
8
6 Taningia danae Martialia hyadesi Martialia Mean Galiteuthis Galiteuthis glacialis Taonius sp.(Clarke) Batoteuthisskolops Taonius sp.B (Voss) Gonatus antarcticus Mean±SD
Figure 8. Distribution of the stable isotopes signaturesHistioteuthis eltaninae of the squids of Kerguelen. Top panel Moroteuthis knipovitchi Kondakovia longimana Histioteuthis atlantica L Histioteuthis atlantica S Alluroteuthis antarcticus Alluroteuthis Mean±2*SD shows the CycloteuthisCarbon akimushkini signature(Red line and Blue line correspond to Subtropical and Polar fronts
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
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 (χ 2=13.261 ; p = 0.99 ). Similar findings were observed for the numeric and weight index values (χ 2=39.68 ; p = 0.66 and χ 2=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%).
44
h Georgia, Crozet and Kerguelen. 3.8 - 3.8 Coleman Curves the of squiddiversity in Sout
Figure 45
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.
LRL (mm) Family Species South Georgia Crozet Kerguelen Test P-Value
Haliphron Alloposidae 12.51 ± 2.92 ------atlanticus Batoteuthis Batoteuthidae 4.17 ± 0.71 4.02 ± 0.45 4.71 ± 0.57 K-W <0.01 skolops Galiteuthis 5.30 ± 0.48 5.38 ± 0.35 5.45 ± 0.33 K-W <0.01 glacialis Taonius sp. Cranchidae - - - 5.12 ± 0.29 4.98 ± 0.22 K-W 0.021 (Clarke) Taonius sp. B 9.24 ± 1.08 8.65 ± 1.20 9.62 ± 1.09 K-W <0.01 (Voss) Cycloteuthis Cycloteuthidae - - - 12.76 ± 2.55 12.78 ± 2.31 K-W 0.997 akimushkini Gonatus Gonatidae 6.05 ± 0.96 6.05 ± 0.64 6.37 ± 0.73 K-W 0.111 antarcticus Histioteuthis 5.51 ± 0.55 5.64 ± 0.84 6.05 ± 0.75 K-W <0.01 atlantica Histioteuthis Histioteuthidae 3.46 ± 0.29 3.46 ± 0.32 3.22 ± 0.29 K-W <0.01 eltaninae Histioteuthis - - - 6.84 ± 0.40 6.41 ± 1.03 K-W 0.056 miranda Mastigoteuthis Mastigoteuthidae 6.93 ± 0.82 6.62 ± 0.62 6.84 ± 0.95 K-W 0.201 sp. A (Clarke) Alluroteuthis Neoteuthidae 5.16 ± 0.48 5.46 ± 0.38 5.41 ± 0.40 K-W <0.01 antarcticus Martialia Ommastrephidae - - - 6.81 ± 0.83 5.97 ± 0.81 K-W <0.01 hyadesi Kondakovia 13.45 ± 1.72 12.58 ± 1.37 13.44 ± 1.52 K-W <0.01 longimana Onychoteuthidae Moroteuthis - - - 8.70 ± 1.04 - - - - - ingens
46
Moroteuthis 6.87 ± 0.96 7.30 ± 0.84 6.94 ± 0.75 K-W <0.01 knipovitchi 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.
Nitrogen (‰) Family Species South Georgia Crozet Kerguelen Test P-Value
Haliphron Alloposidae 13.80 ± 0.41 ------atlanticus Batoteuthis Batoteuthidae 14.45 ± 0.28 15.15 ± 0.69 15.1 ± 0.41 A <0.01 skolops Galiteuthis 13.39 ± 1.10 13.67 ± 0.55 13.26 ± 0.71 A 0.53 glacialis Taonius sp. Cranchidae - - - 15.62 ± 0.42 16.28 ± 0.70 T 0.02 (Clarke) Taonius sp. B 16.74 ± 0.64 15.75 ± 0.80 16.61 ± 0.48 A <0.01 (Voss) Cycloteuthis Cycloteuthidae ------17 ± 0.52 - - akimushkini Gonatus Gonatidae 16.46 ± 0.73 15.58 ± 0.61 15.04 ± 0.51 A <0.01 antarcticus Histioteuthis 16.34 ± 0.78 15.63 ± 0.65 15.74 ± 1.08 A 0.06 atlantica Histioteuthis 15.89 ± 0.58 - - - 15.07 ± 0.97 T 0.04 atlantica small Histioteuthis Histioteuthidae 16.75 ± 0.72 - - - 16.42 ± 0.69 T 0.31 atlantica Large Histioteuthis 14.28 ± 0.76 13.81 ± 0.32 13.51 ± 0.47 A 0.01 eltaninae Histioteuthis ------miranda Mastigoteuthis Mastigoteuthidae 15.95 ± 0.46 13.73 ± 0.70 - - - T <0.01 sp. A (Clarke)
47
Alluroteuthis Neoteuthidae 13.52 ± 0.98 13.01 ± 0.23 13.2 ± 0.36 A 0.20 antarcticus Martialia Ommastrephidae - - - 8.4 ± 0.84 9.26 ± 0.45 T(EXP) 0.02 hyadesi Kondakovia 11.97 ± 0.38 12.22 ± 0.40 12.59 ± 0.75 A 0.05 longimana Moroteuthis Onychoteuthidae - - - 12.69 ± 0.20 - - - - - ingens Moroteuthis 13.88 ± 0.63 12.81 ± 0.45 13.44 ± 0.41 A <0.01 knipovitchi Octopoteuthidae Taningia danae ------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.
Carbon (‰) Family Species South Georgia Crozet Kerguelen Test P-Value
Haliphron Alloposidae -20.91 ± 0.30 ------atlanticus Batoteuthis Batoteuthidae -25.14 ± 0.54 -23.62 ± 0.50 -23.69 ± 0.73 A <0.01 skolops Galiteuthis -22.27 ± 0.82 -21.29 ± 0.53 -21.07 ± 0.59 A <0.01 glacialis Taonius sp. Cranchidae - - - -19.41 ± 0.30 -19.28 ± 0.22 T 0.26 (Clarke) Taonius sp. B -21.94 ± 0.82 -21.38 ± 1.05 -21.85 ± 0.84 A 0.36 (Voss) Cycloteuthis Cycloteuthidae ------19.32 ± 0.32 - - akimushkini Gonatus Gonatidae -23.28 ± 2.33 -23.94 ± 1.18 -22.48 ± 1.80 A 0.22 antarcticus Histioteuthis -20.17 ± 0.59 -19.34 ± 0.20 -19.41 ± 0.54 A <0.01 atlantica Histioteuthis -19.92 ± 0.48 - - - -19.36 ± 0.40 T 0.11 atlantica small Histioteuthis Histioteuthidae -20.39 ± 0.61 - - - -19.46 ± 0.66 T <0.01 atlantica Large Histioteuthis -22.66 ± 1.20 -21.42 ± 0.56 -21.50 ± 1.11 A 0.02 eltaninae Histioteuthis ------miranda
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Mastigoteuthis Mastigoteuthidae -21.26 ± 0.75 -21.42 ± 0.51 - - - T 0.59 sp. A (Clarke) Alluroteuthis Neoteuthidae -21.67 ± 1.46 -21.29 ± 1.38 -20.70 ± 0.90 A 0.24 antarcticus Mart ialia Ommastrephidae - - - -22.57 ± 0.42 -21.75 ± 0.79 T <0.01 hyadesi Kondakovia -24.37 ± 1.59 -22.60 ± 0.65 -22.34 ± 1.84 A <0.01 longimana Moroteuthis Onychoteuthidae - - - -21.79 ± 0.35 - - - - - ingens Moroteuthis -23.85 ± 1.00 -22.09 ± 1.47 -23.71 ± 0.95 A 0.04 knipovitchi Octopoteuthidae Taningia danae ------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) South Georgia Crozet Kerguelen
Family Species mean ± sd mean ± sd mean ± sd
Range Range Range
5.27 ± 0.13 Alloposidae Haliphron atlanticus 5.09 - 5.52
5.47 ± 0.08 5.56 ± 0.21 5,54 ± 0,12 Batoteuthidae Batoteuthis skolops 5.29 - 5.60 5.38 - 6.09 5.31 - 5.67
5.15 ± 0.33 5.11 ± 0.17 4.99 ± 0.21 Galiteuthis glacialis 4.69 - 5.87 4.82 - 5.40 4.63 - 5.30 Cranchidae 6.16 ± 0.20 5.74 ± 0.24 6.00 ± 0.15 Taonius sp. B (Voss) 5.76 - 6.38 5.30 - 6.21 5.79 - 6.18
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6.08 ± 0.22 5.69 ± 0.18 5.53 ± 0.15 Gonatidae Gonatus antarcticus 5.87 - 6.58 5.30 - 5.90 5.27 - 5.72
5.42 ± 0.23 5.15 ± 0.10 5.06 ± 0.14 Histioteuthidae Histioteuthis eltaninae 5.02 - 5.86 4.98 - 5.29 4.83 - 5.27
Mastigoteuthis sp. A 5.92 ± 0.14 5.13 ± 0.21 Mastigoteuthidae (Clarke) 5.72 - 6.14 4.87 - 5.39
5.19 ± 0.30 4.91 ± 0.07 4.97 ± 0.11 Neoteuthidae Alluroteuthis antarcticus 4.80 - 5.63 4.82 - 5.04 4.82 - 5.17
3.52 ± 0.25 3.78 ± 0.14 Ommastrephidae Martialia hyadesi 3.15 - 3.87 3.52 - 3.98
4.72 ± 0.11 4.67 ± 0.12 4.79 ± 0.23 Kondakovia longimana 4.50 - 4.88 4.54 - 4.87 4.35 - 5.07
4.82 ± 0.06 Onychoteuthidae Moroteuthis ingens 4.72 - 4.94
5.37 ± 0.19 4.85 ± 0.14 5.04 ± 0.12 Moroteuthis knipovitchi 4.83 - 6.00 4.54 - 5.01 4.89 - 5.22
6.01 ± 0.15 Octopoteuthidae Taningia danae 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 C 13 ( 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
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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
51 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
52 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
53
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).
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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
55 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
56 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.
57
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.
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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).
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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
60 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.
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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
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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)
72
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 Histioteuthis bonnellii HISTIOTEUTHIDAE 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)
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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
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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 Weight Species 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
Mantle Length Species mean sd min max Haliphron atlanticus 0 0 0 0 Alluroteuthis antarcticus 176.1 16.87 114.67 230.13 Ancistrocheirus lesueuri 280.63 29.39 248.03 305.08 Batoteuthis skolops 113.37 17.36 84.78 165.5 Brachioteuthis ?picta (Clarke) 107.12 0 107.12 107.12
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Brachioteuthis ?picta (Rodhouse) 74.832 0 74.832 74.832 Mastigoteuthis sp. A 181.02 20.16 133.7 246.22 Chiroteuthis veranyi 154.49 22.48 138.59 170.39 Nototeuthis dimegacotyle 116.41 11.87 100.67 132.16 Galiteuthis glacialis 450.6 40.48 341.82 542.9 Gonatus antarcticus 215.94 41.25 102.36 308.13 Histioteuthis atlantica 130.95 14.07 99.918 161.5 Histioteuthis eltaninae 81.013 7.06 52.654 99.166 Histioteuthis corpuscula 55.541 6.27 47.54 61.256 Histioteuthis macrohista 53.693 4.16 47.186 60.2 Histioteuthis miranda 134.13 16.09 110.18 156.37 Illex argentinus 259.11 52.40 197.48 346.49 Kondakovia longimana 479.46 64.03 175.44 630.72 Lepidoteuthis 571.96 0 571.96 571.96 Martialia hyadesi 231.67 13.50 219.88 246.4 Mastigoteuthis psychrophila 121.41 0.44 121.1 121.72 Moroteuthis ingens 377.07 0 377.07 377.07 Moroteuthis knipovitchi 322.81 60.09 231.09 480.56 Moroteuthis robsoni 535.19 46.14 494.92 585.54 Psychroteuthis glacialis 169.68 0 169.68 169.68 Taningia danae 548.83 241.76 270.52 706.8 Taonius sp. B(Voss) 555.3 66.31 319.42 681.86
LRL Species mean sd min max Haliphron atlanticus 12.51 2.92 7.9 18.6 Alluroteuthis antarcticus 5.16 0.48 3.4 6.7 Ancistrocheirus lesueuri 7.90 0.72 7.1 8.5 Batoteuthis skolops 4.17 0.71 3 6.3 Brachioteuthis ?picta (Clarke) 4.50 0 4.5 4.5 Brachioteuthis ?picta (Rodhouse) 2.90 0 2.9 2.9 Mastigoteuthis sp. A 6.93 0.82 5 9.6 Chiroteuthis veranyi 5.85 0.92 5.2 6.5 Nototeuthis dimegacotyle 3.45 0.34 3 3.9 Galiteuthis glacialis 5.30 0.48 4 6.4 Gonatus antarcticus 6.05 0.96 3.4 8.2 Histioteuthis atlantica 5.51 0.55 4.3 6.7 Histioteuthis eltaninae 3.46 0.29 2.3 4.2 Histioteuthis corpuscula 3.53 0.41 3 3.9 Histioteuthis macrohista 3.55 0.29 3.1 4 Histioteuthis miranda 5.63 0.63 4.7 6.5
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Illex argentinus 4.92 0.95 3.8 6.5 Kondakovia longimana 13.45 1.72 5.3 17.5 Lepidoteuthis 15.80 0 15.8 15.8 Martialia hyadesi 4.40 0.46 4 4.9 Mastigoteuthis psychrophila 4.35 0.07 4.3 4.4 Moroteuthis ingens 9.90 0 9.9 9.9 Moroteuthis knipovitchi 6.87 0.96 5.4 9.4 Moroteuthis robsoni 7.87 0.31 7.6 8.2 Psychroteuthis glacialis 5.10 0 5.1 5.1 Taningia danae 14.70 3.21 11 16.8 Taonius sp. B (Voss) 9.24 1.08 5.4 11.3
Crozet Weight Species 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 Alluroteuthis antarcticus 512.31 100.55 236.96 745.97 Ancistrocheirus lesueuri 1715.96 559.94 1048.63 2510.12 Architeuthis dux 3050.94 0 3050.94 3050.94 Batoteuthis skolops 34.66 10.12 15.40 59.31 Chiroteuthis sp. F 79.34 13.40 69.86 88.81 Chiroteuthis veranyi 135.94 35.18 82.71 199.98 Cycloteuthis akimushkini 982.31 350.48 246.34 1768.64 Galiteuthis glacialis 106.17 14.93 55.20 147.05 Galiteuthis sp. 3 1291.05 195.39 1152.89 1429.21 Gonatus antarcticus 217.17 87.61 114.16 504.43 Histioteuthis atlantica 319.44 107.39 76.69 559.20 Histioteuthis bonnellii corpuscula 260.12 63.53 85.48 381.15 Histioteuthis eltaninae 67.73 19.15 18.55 211.44 Histioteuthis hoylei 672.01 13.07 662.77 681.25 Histioteuthis macrohista 120.00 38.65 84.80 162.26 Histioteuthis miranda 825.91 146.34 523.74 1175.27 Illex argentinus 422.28 113.27 310.16 537.35 Kondakovia longimana 2174.26 796.43 224.24 7227.75 Lepidoteuthis grimaldii 8030.96 1048.03 6055.73 9205.65 Lycoteuthis lorigera 137.90 45.51 105.72 170.08 Martialia hyadesi 532.83 128.64 302.01 921.33 Mastigoteuthis psychrophila 57.41 8.46 48.87 70.48
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Mesonychoteuthis hamiltoni 4404.21 2081.24 1839.50 6724.83 Moroteuthis ingens 1397.23 683.18 413.88 4149.35 Moroteuthis knipovitchi 840.84 354.75 318.13 1796.30 Moroteuthis robsoni 4883.08 1823.92 3491.97 6948.05 Notonykia africanae 101.83 32.63 78.75 124.90 Nototeuthis dimegacotyle 181.74 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 Taningia danae 4659.38 1699.85 2172.67 7310.69 Taonius sp. (Clarke) 78.76 9.56 59.72 98.87 Taonius sp. B (Voss) 253.30 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
Mantle Length Species mean sd min max ?Discoteuthis sp. 241.96 24.33 224.75 259.16 ?Mastigoteuthis A (Clarke) 194.26 18.06 154.76 228.33 Alluroteuthis antarcticus 186.70 13.23 143.36 213.69 Ancistrocheirus lesueuri 303.99 33.26 262.29 346.64 Architeuthis dux 450.31 0 450.31 450.31 Batoteuthis skolops 109.82 11.02 85.02 132.72 Chiroteuthis sp. F 146.30 8.47 140.30 152.29 Chiroteuthis veranyi 175.17 15.63 148.62 201.70 Cycloteuthis akimushkini 395.42 78.90 198.09 544.36 Galiteuthis glacialis 457.83 29.49 342.65 531.17 Galiteuthis sp. 3 716.75 38.51 689.52 743.98 Gonatus antarcticus 215.75 27.40 173.09 294.84 Histioteuthis atlantica 134.36 21.44 71.69 174.33 Histioteuthis bonnellii corpuscula 78.99 7.71 53.33 91.43 Histioteuthis eltaninae 80.97 7.90 52.65 119.48 Histioteuthis hoylei 172.96 1.57 171.85 174.07 Histioteuthis macrohista 56.73 6.54 50.66 63.67 Histioteuthis miranda 207.56 13.77 175.67 237.25 Illex argentinus 280.26 25.57 254.33 305.65 Kondakovia longimana 447.30 51.13 209.02 674.01 Lepidoteuthis grimaldii 765.87 35.27 698.30 802.92
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Lycoteuthis lorigera 146.45 17.84 133.84 159.07 Martialia hyadesi 302.57 24.31 254.36 367.23 Mastigoteuthis psychrophila 118.58 1.88 116.69 121.78 Mesonychoteuthis hamiltoni 777.38 149.60 579.27 927.58 Moroteuthis ingens 343.04 47.65 236.25 492.99 Moroteuthis knipovitchi 349.35 52.26 252.91 459.98 Moroteuthis robsoni 685.22 59.50 636.89 751.67 Notonykia africanae 31.74 37.23 5.42 58.07 Nototeuthis dimegacotyle 129.45 14.06 97.17 145.46 Octopoteuthis sp. 382.51 36.39 356.77 408.24 Onychoteuthis banskii 109.73 0 109.73 109.73 Onychoteuthis sp. 2 (Imber) 91.72 0 91.72 91.72 Onychoteuthis sp. C (Imber) 144.12 36.13 118.57 169.66 Pholidoteuthis massaye 301.40 0 301.40 301.40 Slosarczykovia circumantarctica 65.35 4.57 62.12 68.58 Taningia danae 576.67 129.49 361.54 752.68 Taonius sp. (Clarke) 302.21 17.55 265.36 337.24 Taonius sp. B (Voss) 518.86 73.76 340.31 700.29 Teuthowenia pellucida 161.90 16.55 137.68 175.06 Todarodes sp. 323.30 97.94 261.26 436.22
LRL Species mean sd min max ?Discoteuthis sp. 7.81 0.78 7.25 8.36 ?Mastigoteuthis A (Clarke) 6.62 0.62 5.26 7.79 Alluroteuthis antarcticus 5.46 0.38 4.22 6.23 Ancistrocheirus lesueuri 8.47 0.82 7.45 9.52 Architeuthis dux 8.53 0 8.53 8.53 Batoteuthis skolops 4.02 0.45 3.01 4.96 Chiroteuthis sp. F 5.52 0.35 5.27 5.76 Chiroteuthis veranyi 6.70 0.64 5.61 7.78 Cycloteuthis akimushkini 12.76 2.55 6.39 17.56 Galiteuthis glacialis 5.38 0.35 4.01 6.26 Galiteuthis sp. 3 8.48 0.46 8.15 8.80 Gonatus antarcticus 6.05 0.64 5.05 7.89 Histioteuthis atlantica 5.64 0.84 3.20 7.20 Histioteuthis bonnellii corpuscula 5.06 0.51 3.38 5.88 Histioteuthis eltaninae 3.46 0.32 2.30 5.03 Histioteuthis hoylei 8.40 0.07 8.35 8.45 Histioteuthis macrohista 3.76 0.45 3.34 4.24 Histioteuthis miranda 6.84 0.40 5.91 7.71
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Illex argentinus 5.30 0.46 4.83 5.76 Kondakovia longimana 12.58 1.37 6.20 18.66 Lepidoteuthis grimaldii 21.16 0.97 19.29 22.18 Lycoteuthis lorigera 4.62 0.52 4.25 4.98 Martialia hyadesi 6.81 0.83 5.17 9.00 Mastigoteuthis psychrophila 3.89 0.30 3.59 4.41 Mesonychoteuthis hamiltoni 12.86 2.44 9.63 15.30 Moroteuthis ingens 8.70 1.04 5.82 11.67 Moroteuthis knipovitchi 7.30 0.84 5.75 9.07 Moroteuthis robsoni 8.86 0.39 8.54 9.30 Notonykia africanae 3.80 0.35 3.55 4.05 Nototeuthis dimegacotyle 3.82 0.40 2.90 4.28 Octopoteuthis sp. 22.10 2.10 20.61 23.58 Onychoteuthis banskii 3.28 0 26.73 26.73 Onychoteuthis sp. 2 (Imber) 2.73 0 15.99 15.99 Onychoteuthis sp. C (Imber) 4.33 1.10 3.55 5.11 Pholidoteuthis massaye 7.06 0 7.06 7.06 Slosarczykovia circumantarctica 2.43 0.23 2.27 2.59 Taningia danae 15.07 1.72 12.21 17.41 Taonius sp. (Clarke) 5.12 0.29 4.52 5.69 Taonius sp. B (Voss) 8.65 1.20 5.74 11.60 Teuthowenia pellucida 4.67 0.55 3.86 5.11 Todarodes sp. 8.09 2.37 6.59 10.82
Kerguelen Weight Species mean sd min max ?Mastigoteuthis A (Clarke) 319.01 113.27 107.50 493.46 Alluroteuthis antarcticus 499.36 102.55 228.79 701.07 Ancistrocheirus lesueuri 1493.59 639.23 99.08 2336.28 Architeuthis dux 15815.86 16350.63 1877.20 45525.42 Batoteuthis skolops 53.24 16.51 26.30 81.12 Chiroteuthis veranyi 177.32 39.82 96.95 234.29 Cycloteuthis akimushkini 980.75 322.37 286.14 1852.07 Galiteuthis glacialis 108.90 13.91 50.18 148.60 Galiteuthis sp. 3 1260.82 231.69 1056.58 1512.58 Galiteuthis Stc sp. 758.05 189.98 638.66 1041.67 Gonatus antarcticus 259.97 105.19 140.07 523.85 Histioteuthis atlantica 374.03 101.80 43.55 678.21
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Histioteuthis bonnellii corpuscula 254.32 65.27 142.09 382.91 Histioteuthis eltaninae 54.33 15.60 24.34 107.77 Histioteuthis hoylei 483.26 78.61 412.44 554.57 Histioteuthis macrohista 147.21 20.19 112.84 193.09 Histioteuthis miranda 715.27 252.18 57.05 1217.48 Kondakovia longimana 2685.82 1034.12 1097.05 7701.93 Lepidoteuthis grimaldii 8291.41 0 8291.41 8291.41 Martialia hyadesi 411.22 111.97 214.35 669.61 Mastigoteuthis psychrophila 58.92 5.96 45.76 69.62 Mesonychoteuthis hamiltoni 4270.92 0 4270.92 4270.92 Moroteuthis ingens 2986.58 741.94 1922.40 3769.18 Moroteuthis knipovitchi 691.11 303.82 328.77 1594.62 Moroteuthis robsoni 6883.91 3446.28 2828.79 13740.81 Moroteuthis sp. B 330.23 168.20 147.92 500.90 Notonykia africanae 47.76 0 47.76 47.76 Nototeuthis dimegacotyle 238.55 41.22 153.33 301.53 Octopoteuthis sp. 550.08 266.14 235.51 1525.89 Onychoteuthis banskii 29.81 0 29.81 29.81 Onychoteuthis sp. 2 (Imber) 12.22 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 Psychroteuthis glacialis 389.47 41.16 347.42 429.28 Taningia danae 7656.05 2669.42 1834.14 13040.49 Taonius sp. (Clarke) 74.07 7.17 60.88 88.17 Taonius sp. B (Voss) 317.28 74.70 138.64 482.08 Teuthowenia pellucida 41.42 5.40 30.53 52.07 Todarodes sp. 402.26 86.14 298.44 550.08
Mantle Length Species mean sd min max ?Mastigoteuthis A (Clarke) 200.60 27.66 140.22 236.77 Alluroteuthis antarcticus 184.93 14.05 141.61 209.14 Ancistrocheirus lesueuri 284.25 55.70 115.18 338.90 Architeuthis dux 606.10 168.74 399.31 858.37 Batoteuthis skolops 126.62 13.82 101.17 147.64 Chiroteuthis veranyi 192.27 16.29 156.94 213.20 Cycloteuthis akimushkini 396.29 71.57 213.90 557.38 Galiteuthis glacialis 463.27 27.39 328.41 533.68 Galiteuthis sp. 3 709.91 45.75 668.58 759.07 Galiteuthis Stc sp. 591.70 49.33 559.66 665.23 Gonatus antarcticus 229.64 31.28 186.81 298.70
81
Histioteuthis atlantica 144.71 19.10 54.76 189.47 Histioteuthis bonnellii corpuscula 78.40 7.29 64.00 91.58 Histioteuthis eltaninae 75.23 7.07 57.79 95.49 Histioteuthis hoylei 147.76 11.42 137.43 158.08 Histioteuthis macrohista 61.39 2.95 56.01 67.72 Histioteuthis miranda 192.63 35.11 70.99 240.33 Kondakovia longimana 479.37 56.57 360.53 688.19 Lepidoteuthis grimaldii 775.40 0.00 775.40 775.40 Martialia hyadesi 278.05 23.77 230.49 328.33 Mastigoteuthis psychrophila 119.13 1.42 115.89 121.59 Mesonychoteuthis hamiltoni 786.90 0 786.90 786.90 Moroteuthis ingens 440.15 38.11 383.20 477.82 Moroteuthis knipovitchi 327.06 46.80 256.03 442.52 Moroteuthis robsoni 731.55 88.04 603.66 875.51 Moroteuthis sp. B 248.70 52.29 187.43 298.44 Notonykia africanae 111.96 0 111.96 111.96 Nototeuthis dimegacotyle 143.18 9.12 123.06 155.95 Octopoteuthis sp. 241.72 46.49 171.17 384.85 Onychoteuthis banskii 113.99 0 113.99 113.99 Onychoteuthis sp. 2 (Imber) 83.53 0 83.53 83.53 Onychoteuthis sp. B 185.71 0 185.71 185.71 Onychoteuthis sp. C 165.04 7.90 152.63 179.16 Psychroteuthis glacialis 337.96 28.70 308.71 365.77 Taningia danae 748.56 163.14 317.16 994.14 Taonius sp. (Clarke) 293.70 13.59 267.82 319.42 Taonius sp. B (Voss) 578.55 66.83 395.60 708.27 Teuthowenia pellucida 163.34 9.53 143.07 181.34 Todarodes sp. 248.62 19.45 223.62 280.29
LRL Species mean sd min max ?Mastigoteuthis A (Clarke) 6.84 0.95 4.76 8.08 Alluroteuthis antarcticus 5.41 0.40 4.17 6.10 Ancistrocheirus lesueuri 7.99 1.37 3.84 9.33 Architeuthis dux 11.16 2.85 7.67 15.41 Batoteuthis skolops 4.71 0.57 3.67 5.57 Chiroteuthis veranyi 7.39 0.67 5.95 8.25 Cycloteuthis akimushkini 12.78 2.31 6.90 17.98 Galiteuthis glacialis 5.45 0.33 3.84 6.29 Galiteuthis sp. 3 8.39 0.55 7.90 8.98 Galiteuthis Stc sp. 6.98 0.59 6.60 7.86
82
Gonatus antarcticus 6.37 0.73 5.37 7.98 Histioteuthis atlantica 6.05 0.74 2.54 7.79 Histioteuthis bonnellii corpuscula 5.03 0.48 4.08 5.89 Histioteuthis eltaninae 3.22 0.29 2.51 4.05 Histioteuthis hoylei 7.27 0.51 6.80 7.73 Histioteuthis macrohista 4.08 0.20 3.71 4.52 Histioteuthis miranda 6.41 1.03 2.85 7.80 Kondakovia longimana 13.44 1.52 10.26 19.04 Lepidoteuthis grimaldii 21.42 0 21.42 21.42 Martialia hyadesi 5.97 0.81 4.36 7.68 Mastigoteuthis psychrophila 3.98 0.23 3.46 4.38 Mesonychoteuthis hamiltoni 13.01 0 13.01 13.01 Moroteuthis ingens 10.49 0.85 9.21 11.33 Moroteuthis knipovitchi 6.94 0.75 5.80 8.79 Moroteuthis robsoni 9.17 0.58 8.32 10.12 Moroteuthis sp. B 5.68 0.84 4.70 6.48 Notonykia africanae 3.49 0 3.49 3.49 Nototeuthis dimegacotyle 4.22 0.26 3.64 4.58 Octopoteuthis sp. 13.97 2.68 9.90 22.23 Onychoteuthis banskii 3.41 0 3.41 3.41 Onychoteuthis sp. 2 (Imber) 5.60 0 5.60 5.60 Onychoteuthis sp. B 2.48 0 2.48 2.48 Onychoteuthis sp. C 4.97 0.24 4.59 5.40 Psychroteuthis glacialis 7.43 0.28 7.14 7.70 Taningia danae 17.36 2.17 11.62 20.62 Taonius sp. (Clarke) 4.98 0.22 4.56 5.40 Taonius sp. B (Voss) 9.62 1.09 6.64 11.73 Teuthowenia pellucida 4.72 0.32 4.04 5.32 Todarodes sp. 6.28 0.47 5.68 7.05
83
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 N% W% Species F% 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
84
Alluroteuthis antarcticus 87.88 99 2.54 50718.84 1.35 Ancistrocheirus lesueuri 18.18 7 0.18 12011.73 0.32 Architeuthis dux 12.12 4 0.10 12203.74 0.32 Batoteuthis skolops 84.85 111 2.84 3847.70 0.10 Chiroteuthis sp. F 6.06 2 0.05 158.67 0.00 Chiroteuthis veranyi 42.42 19 0.49 2582.85 0.07 Cirrata sp. A 3.03 1 0.03 - - Cycloteuthis akimushkini 57.58 38 0.97 37327.71 0.99 Galiteuthis glacialis 96.97 344 8.81 36520.81 0.97 Galiteuthis sp. 3 6.06 2 0.05 2582.10 0.07 Gonatus antarcticus 60.61 57 1.46 12378.93 0.33 Histioteuthis atlantica 84.85 127 3.25 40568.63 1.08 Histioteuthis bonnellii corpuscula 60.61 42 1.08 10924.86 0.29 Histioteuthis eltaninae 100.00 989 25.33 66984.65 1.78 Histioteuthis hoylei 6.06 2 0.05 1344.01 0.04 Histioteuthis macrohista 12.12 4 0.10 480.01 0.01 Histioteuthis miranda 54.55 34 0.87 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 Kondakovia longimana 100.00 1314 33.66 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 Martialia hyadesi 84.85 168 4.30 89515.06 2.38 Mastigoteuthis psychrophila 18.18 6 0.15 344.47 0.01 Mesonychoteuthis hamiltoni 12.12 5 0.13 22021.04 0.59 Moroteuthis ingens 93.94 159 4.07 222159.54 5.91 Moroteuthis knipovitchi 93.94 133 3.41 111831.96 2.97 Moroteuthis robsoni 9.09 3 0.08 14649.25 0.39 Notonykia africanae 9.09 3 0.08 305.48 0.01 Nototeuthis dimegacotyle 21.21 8 0.20 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 - - Taningia danae 18.18 6 0.15 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
85
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 N% W% Species F% Lower beaks N% Weight W% ?Mastigoteuthis A (Clarke) 23.33 11 0.41 3509.07 0.15 Alluroteuthis antarcticus 90.00 86 3.22 42944.66 1.85 Ancistrocheirus lesueuri 43.33 20 0.75 29871.86 1.29 Architeuthis dux 63.33 22 0.82 347948.84 15.00 Batoteuthis skolops 66.67 36 1.35 1916.51 0.08 Chiroteuthis veranyi 36.67 17 0.64 3014.40 0.13 Cycloteuthis akimushkini 86.67 86 3.22 84344.37 3.64 Galiteuthis glacialis 96.67 326 12.20 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 Gonatus antarcticus 73.33 46 1.72 11958.77 0.52 Histioteuthis atlantica 96.67 799 29.90 298847.28 12.89 Histioteuthis bonnellii corpuscula 53.33 21 0.79 5340.62 0.23 Histioteuthis eltaninae 86.67 212 7.93 11517.83 0.50 Histioteuthis hoylei 10.00 6 0.22 2899.57 0.13 Histioteuthis macrohista 53.33 24 0.90 3533.00 0.15 Histioteuthis miranda 60.00 38 1.42 27180.40 1.17 Histioteuthis sp. 6.67 2 0.07 - - Kondakovia longimana 86.67 268 10.03 719800.35 31.04 Lepidoteuthis grimaldii 3.33 1 0.04 8291.41 0.36 Martialia hyadesi 86.67 100 3.74 41121.75 1.77 Mastigoteuthis psychrophila 43.33 16 0.60 942.73 0.04 Mesonychoteuthis hamiltoni 3.33 1 0.04 4270.92 0.18 Moroteuthis ingens 20.00 7 0.26 20906.04 0.90 Moroteuthis knipovitchi 83.33 66 2.47 45613.24 1.97 Moroteuthis robsoni 46.67 23 0.86 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 Nototeuthis dimegacotyle 3.33 24 0.90 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
86
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 Taningia danae 46.67 40 1.50 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 - -
87
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
Alluroteuthis antarcticus 0.01 0.02 0.00 Ancistrocheirus lesueuri 0.11 0.10 0.37 Batoteuthis skolops 0.03 0.01 0.01 Chiroteuthis veranyi 0.13 0.37 0.03 Galiteuthis glacialis 0.00 0.00 0.00 Gonatus antarcticus 0.06 0.12 0.00 Histioteuthis atlantica 0.01 0.01 0.00 Histioteuthis eltaninae 0.00 0.02 0.02 Histioteuthis macrohista 0.46 0.09 0.18 Histioteuthis miranda 0.00 0.01 0.01 Kondakovia longimana 0.00 0.01 0.01 Lepidoteuthis grimaldii 0.90 0.12 0.41 Martialia hyadesi 0.11 0.65 0.13 Mastigoteuthis sp. A(Clarke) 0.00 0.44 0.33 Mastigoteuthis psychrophila 0.08 0.27 0.52 Moroteuthis ingens 1.59 0.73 0.27 Moroteuthis knipovitchi 0.01 0.01 0.00 Moroteuthis robsoni 0.37 0.22 1.03 Nototeuthis dimegacotyle 0.11 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
Alluroteuthis antarcticus 0.10 1.36 0.02 Ancistrocheirus lesueuri 0.28 0.16 0.95 Batoteuthis skolops 0.08 0.00 0.16 Chiroteuthis veranyi 0.00 0.47 0.10 Galiteuthis glacialis 0.00 0.26 0.10 Gonatus antarcticus 0.16 3.20 0.09 Histioteuthis atlantica 0.55 0.30 1.84 Histioteuthis eltaninae 0.24 0.14 0.28
88
Histioteuthis macrohista 0.67 1.35 0.38 Histioteuthis miranda 0.03 0.02 0.11 Kondakovia longimana 0.16 0.00 0.34 Lepidoteuthis grimaldii 0.33 0.11 0.45 Martialia hyadesi 0.07 0.87 0.01 Mastigoteuthis sp A(Clarke) 0.09 4.94 0.44 Mastigoteuthis psychrophila 0.24 0.25 0.95 Moroteuthis ingens 0.86 0.93 0.77 Moroteuthis knipovitchi 0.01 0.00 0.04 Moroteuthis robsoni 0.62 0.15 1.81 Nototeuthis dimegacotyle 0.33 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 Degrees of freedom= 44 p-value= 0.66
W% Species Crozet South Georgia Kerguelen Alluroteuthis antarcticus 0.08 1.00 0.00 Ancistrocheirus lesueuri 0.23 0.23 0.98 Batoteuthis skolops 0.01 0.00 0.02 Chiroteuthis veranyi 0.01 0.64 0.35 Galiteuthis glacialis 0.01 0.27 0.15 Gonatus antarcticus 0.21 3.15 0.04 Histioteuthis atlantica 0.61 0.39 2.32 Histioteuthis eltaninae 0.25 0.12 0.36 Histioteuthis macrohista 0.69 0.54 0.84 Histioteuthis miranda 0.01 0.20 0.13 Kondakovia longimana 0.07 0.03 0.26 Lepidoteuthis grimaldii 0.40 0.50 0.39 Martialia hyadesi 0.12 0.94 0.00 Mastigoteuthis sp. A(Clarke 0.01 1.65 0.23 Mastigoteuthis psychrophila 0.27 0.17 1.05 Moroteuthis ingens 0.62 0.92 0.55 Moroteuthis knipovitchi 0.03 0.00 0.07 Moroteuthis robsoni 0.70 0.66 2.93 Nototeuthis dimegacotyle 0.41 0.15 1.42 Taonius sp. B Voss 0.65 5.49 0.00
89
OTHERS 4.29 0.92 13.66 Taningia danae 0.71 0.58 2.85 Sum of χ2= 57.57 Degrees of freedom= 42 p-value= 0.055
90