Geographic variation in cephalopod life history traits

Instituto Nacional de Recursos Biológicos INRB, I.P. / L-IPIMAR

Geographic variation in cephalopod life history traits

Ana Moreno Dissertação original apresentada para acesso à categoria de Investigador Auxiliar Unidade de Recursos Marinhos e Sustentabilidade L-IPIMAR 2008

Geographic variation in cephalopod life history traits

Ana Cristina Andrade Moreno Marques Dissertação apresentada para acesso à categoria de Investigador Auxiliar Unidade de Recursos Marinhos e Sustentabilidade L-IPIMAR 2008

Orientador: A. Miguel P. Santos

Index _____________________________________________________________________________________________________________

Índice Agradecimentos

i

Nota introdutória

iii

Resumo, Abstract

v

General Introduction

1

Part I - Geographic variation in the population dynamics of squid and octopus juveniles and adults Chapter

1.

Biological

variation

of

Loligo vulgaris (Cephalopoda:

Loliginidae) in the eastern Atlantic end Mediterranean

11

1.1. Introduction

11

1.2. Material and Methods

12

1.2.1. Biological Sampling

12

1.2.2. Data analysis

14

1.3. Results

16

1.3.1. Fisheries

16

1.3.2. Size and recruitment

17

1.3.3. Sex ratio

19

1.3.4. Maturity

21

1.3.5. Size at maturity

23

1.3.6. Length-weight relationship

26

1.3.7. Multivariate comparisons

26

1.3.8. Water temperature regimes

28

1.4. Discussion

29

1.4.1. Broad-scale patterns and geographic variation

29

1.4.2. Biological and environmental variation

33

Chapter 2. A comparison of the fishery biology of three Illex coindetii vérany, 1839 (cephalopoda: ommastrephidae) populations from the European Atlantic and Mediterranean waters.

37

2.1. Introduction

37


38

2.2.1. Study areas and sampling

38


39

Ana Moreno 2008 – Cephalopod Life History Traits _____________________________________________________________________________________________________________

2.3. Results

40

2.3.1. Fisheries

40

2.3.2. Size

41

2.3.3. Growth rates

41


43

2.3.5. Recruitment

44

2.3.6. Maturation

44

2.3.7. Sex ratio

48

2.3.8. Correlation with environmental variables

49

2.4. Discussion

50

Chapter 3. Biological variation of Octopus vulgaris in the northwest and southern Portuguese waters

59

3.1. Introduction

59


60

3.2.1. Biological sampling

60


63

3.3. Results

64

3.3.1. Size and weight

64


66

3.3.4. Size and maturation

67

3.3.5. Recruitment season

70

3.3.6. Spawning season

71

3.4. Discussion

73

Part 2 – Cephalopod early life stages: description and distribution patterns Chapter 4. Identification of cephalopod paralarvae from Portuguese and

81

adjacent waters

4.1. Checklist of species

81

4.2. Identification key to family level of early life stages of neritic and oceanic cephalopods in the Iberian Atlantic waters 4.3. Description and illustration of species

82 84

4.3.1. Family Sepiolidae

84

4.3.2. Family Loliginidae

86

4.3.3. Family Ommastrephidae

93

Index _____________________________________________________________________________________________________________

4.3.4. Family Enoploteuthidae

96

4.3.5. Family Ancistrocheiridae

97

4.3.6. Family Pyroteuthidae

97

4.3.7. Family Onychoteuthidae

100

4.3.8. Family Ctenopterygidae

101

4.3.9. Family Brachioteuthidae

102

4.3.10. Family Mastigoteuthidae

102

4.3.11. Family Chiroteuthidae

103

4.3.12. Family Cranchiidae

104

4.3.13. Family Ocythoidae

111

4.3.14. Family Octopodidae

112

Chapter 5. Distribution and abundance of cephalopod paralarvae off Portugal based on 19 years of historical data

117

5.1. Introduction

117

5.2. Material and methods

118

5.2.1. Sampling

118


120

5.3. Results 5.3.1. Neritic species

123 123

5.3.1.1. Loliginids

123

5.3.1.2. Octopus vulgaris

130

5.3.1.3. Sepiolids

139

5.3.1.4. Ommastrephids

141

5.3.2. Oceanic species

5.4. Discussion

143 147

5.4.1. Loligo vulgaris

147

5.4.2. Octopus vulgaris

149

5.4.3. Sepiolids

151

5.4.4. Ommastrephids

152

5.4.5. Oceanic species

153

Concluding Remarks

155

References

161

Agradecimentos

Esta dissertação não seria possível sem o carinho e o incentivo dos meus colegas do grupo de investigação de cefalópodes, por isso é para o João Pereira, a Manuela Cunha, o Pedro da Conceição e a Sílvia Lourenço que vão os meus maiores agradecimentos. Quero ainda expressar a minha gratidão à minha amiga e colega Antonina que não sendo a minha orientadora oficial me ensinou tudo o que sei sobre plâncton, que colaborou comigo no capítulo 5 e que sempre me incentivou a publicar os meus trabalhos. Estou claro muito grata ao meu orientador Dr. Miguel Santos pelo seu incentivo, disponibilidade e apoio e também pelos seus comentários que muito ajudaram a melhorar esta dissertação. Aos Presidentes e Directores do IPIMAR nos últimos anos, agradeço todo o apoio prestado e a oportunidade que me deram para estudar os cefalópodes, que julgo seremos recursos marinhos mais fascinantes. Depois vem o meu sincero agradecimento aos colegas do IPIMAR que me ajudaram e/ou escutaram os meus desabafos durante os meus anos como Assistente de Investigação: a Isabel Meneses, a Graça Pestana, a Fátima Cardador, a Manuela Azevedo, o Ernesto Jardim, a Cristina Morgado, o Ricardo Alpoim, o Alberto Murta, a Aida Campos, o Paulo Fonseca, a Rogélia Martins, o Miguel Carneiro, a Cristina Silva, a Susana Godinho, a Narcisa Bandarra, a Amparo Gonçalves, a Teresa Moita, a Helena Lourenço, a Corina Chaves, a Paula Ramos, a Cristina Nunes, o Victor Marques, o Miguel Neves dos Santos, a Leonor Nunes, a malta nova entusiasta e os mais veteranos com quem tenho embarcado no NE “Noruega”, e por fim também os outros que agora não me lembro. Em particular agradeço mais uma vez ao Pedro da Conceição pelo seu trabalho técnico exemplar, pela sua curiosidade científica, pelo seu entusiasmo, amizade e dedicação e por quem eu gostaria de ter “Poder” para ter a possibilidade de o recompensar profissionalmente. No âmbito dos projectos europeus de cefalópodes quero agradecer a colaboração, incentivo e os indispensáveis debates científicos aos meus colegas Peter Boyle, Graham Pierce, Angel Guerra, Catalina Perales Raya, Drosos

i


Koutsoubas, Jean-Paul Robin, Uwe Piatkowski, Christos Arvanitidis e Eduardo Balguerias. Agradeço ainda aos colegas do laboratório de zooplancton que recolheram as amostras, triaram as paralarvas de cefalópodes e disponibilizaram os dados associados, nomeadamente Lurdes Dias, Dra. A. Farinha, Dra. I. Meneses, Dra. P. Lopes, Dr. Y. Stratoudakis e Dra. M. Angélico; e agradeço também aos colegas dos

laboratórios

da

Aquacultura

pelas

facilidades

concedidas

para

as

experiências de incubação de posturas. Ao meu orientador de Doutoramento Dr. Henrique Cabral, agradeço a sua colaboração no capítulo 5 e a compreensão da necessidade de interromper os meus trabalhos de doutoramento para a realização desta dissertação. Este trabalho foi em parte financiado ao abrigo de vários projectos nacionais e europeus, nomeadamente: Project EUROSQUID-FAR-MA-1-203, EUROSQUID-AIR1-CT92-0573,

SEFOS-AIR2-CT93-1105,

CEPHVAR-FAIR-

CT96-1520, PNAB-QCAIII, NEOMAV-FEDER/UE/PIDDAC/QCAIII, SIGAP-22-0501-FDR-00013.

À minha mãe, ao meu pai, ao Pedro, à Catarina e à Raquel

ii

Objectivos _____________________________________________________________________________________________________________

Nota introdutória

Para que a exploração de um recurso natural seja sustentável é necessário delinear uma estratégia de gestão adequada, apenas possível através do conhecimento aprofundado do próprio recurso e dos factores que o influenciam. Esta dissertação resulta de um trabalho de colaboração com colegas de várias equipas de investigação nacionais e europeias. Tem como objectivo global determinar a influência da variabilidade ambiental nas estratégias de ciclo de vida de várias espécies de cefalópodes com relevância nas pescarias a nível europeu, e como objectivos parciais: 1. Determinar o ciclo reprodutivo e outros parâmetros biológicos da lula-vulgar, Loligo

vulgaris, e avaliar a variação geográfica destes em populações da costa Atlântica e Mar Mediterrâneo; 2. Determinar o ciclo reprodutivo e outros parâmetros biológicos da pota-voadora, Illex

coindetii, e avaliar a variação geográfica destes em populações da costa Atlântica e Mar Mediterrâneo; 3. Determinar o ciclo reprodutivo e outros parâmetros biológicos do polvo-comum,

Octopus vulgaris, e avaliar a variação geográfica destes em duas populações das águas portuguesas sob a influência de condições oceanográficas distintas; 4. Identificar e descrever morfologicamente as paralarvas dos cefalópodes das águas portuguesas, como uma ferramenta para o posterior estudo da fase planctónica das várias espécies; 5. Determinar a época de eclosão e estudar os padrões de distribuição e abundância das paralarvas de cefalópodes ao longo da costa portuguesa e das condições ambientais que os determinam. Esta dissertação está dividida numa introdução geral, cinco capítulos agrupados em duas partes, a primeira englobando a análise da fase juvenil e adulta de três espécies e a segunda englobando a análise da fase planctónica, e as conclusões finais.

iii

Ana Moreno 2008 – Cephalopod Life History Traits __________________________________________________________________________________________________________

Os capítulos 1 e 2, resultantes dos estudos no âmbito do projecto europeu “Cephalopod Dynamics: patterns in environmental and genetic variation” (CEPHVAR - FAIR-CT961520), encontram-se publicados e o capítulo 5 em fase de publicação: Moreno, A., Pereira J., Arvanitidis, C., Robin, J.P., Koutsoubas, D., Perales-Raya, C., Cunha, M.M., Balguerias, E. e Denis, V., 2002. Biological variation of Loligo vulgaris (Cephalopoda: Loliginidae) in the eastern Atlantic and Mediterranean. Bulletin of Marine Science, 71(1): 515-534. Arvanitidis, C., Koutsoubas, D., Robin, J.P., Pereira, J., Moreno, A., Cunha, M.M., Valavanis, V. e Eleftheriou, A., 2002. A comparison of the fishery biology of three Illex

coindetii vérany, 1839 (Cephalopoda: Ommastrephidae) populations from the European Atlantic and Mediterranean waters. Bulletin of Marine Science, 71(1): 129-146. Moreno, A., dos Santos, A., Piatkowski, U., Santos, A.M.P e Cabral, H. 2008. Distribution of cephalopod paralarvae off western Iberia in relation to the prevailing oceanographic regimes (aceite para publicação no Journal of Plankton Research). A autora desta dissertação declara, para os efeitos no disposto no nº 2 do Artigo 8 do Decreto-Lei 388/70, que interveio na concepção e execução dos trabalhos experimentais, na interpretação dos resultados e na redacção dos manuscritos das publicações acima descriminadas.

iv

Abstract e Resumo __________________________________________________________________________________________________________

Abstract The common squid, Loligo vulgaris Lamark, 1798, the short-finned squid, Illex

condetii Vérany, 1839, and specially the common octopus, Octopus vulgaris Cuvier 1797, are among the most important harvested cephalopods in Portugal. All share of a short life cycle with a planktonic life phase strongly influenced by regional environmental conditions. The main purpose of this dissertation is to have a better understanding of the environmental effects on life-cycle strategies of those species. Geographic variation in life history traits within squid and octopus populations was assessed by the analysis of simultaneous biological sampling across their distribution range of the juveniles and adults, from the fisheries and survey cruises, coupled with the analysis of the of the early young stages, from plankton sampling. The biological characteristics of the squid Loligo vulgaris from north France, northwest Portugal, the Saharan Bank, and the Greek Seas are analyzed to describe large scale biological patterns and to evaluate geographical variation in the Atlantic and the Mediterranean. In northwest Portugal and on the Saharan Bank population length structures are more complex due to extended spawning and recruitment periods. Squid spawn only between November and April in the north France and the Greek Seas waters. Gonadosomatic indices decrease with decreasing latitude in the Atlantic, while the highest indices occur on the Mediterranean. Full maturity occurs at smaller size in the northwest Portugal than on other areas of the Atlantic, and at similar size to Mediterranean squid. Length-weight relationship slopes increase from the north to the south in the Atlantic and from the Atlantic to the Mediterranean. Multivariate analysis of seasonal biological indices demonstrate significant biological differences between squid of different areas, mainly in terms of size at maturity, male GSI and average body size and weight. Three populations of the short-finned squid Illex coindetii were simultaneously sampled and studied from the Southern Celtic Sea and Bay of Biscay, Portuguese waters and Greek Seas. Differences among the three populations are observed for several lifecycle parameters. Males from the Portuguese waters have significantly lower lengthweight slopes than those from the remainder areas. Size at full recruitment is lower in females from the Portuguese waters than on Southern Celtic Sea and Bay of Biscay and the Greek Seas. L50 for both females and males from the three studied areas gradually decreased from the North Atlantic to the Mediterranean. The recruitment season is restricted to autumn months in the Southern Celtic Sea and Bay of Biscay while in

v

Ana Moreno 2008 – Cephalopod Biological Variation __________________________________________________________________________________________________________

Portuguese waters and the Greek Seas recruitment is extended throughout the year. The main spawning season is in spring and summer in the Atlantic and throughout the year on the Greek Seas. Environmental variables (sea surface temperature and chlorophyll-a concentration) are correlated with some of the biological indices of the I.

coindetii populations. Biological variation in O. vulgaris was assessed between populations on the northwest and southern Portuguese waters. Mean ML and BW are significantly lower in summer than in winter in the northwest, while the mean ML and BW are significantly higher in summer than in winter in south octopus. As in L. vulgaris, octopus becomes significantly heavier with length on the south area than on the northern area. There are also differences in size at maturity between areas in both sexes, with the maturation process beginning at lower sizes on the northwest population and the resulting BW50 lower on the northwest than on the southern area. Small octopus appear in fisheries in higher proportions from June to December, on the northwest area, and from August until April of the next year on the southern area. Spawning females are present throughout the year on the northwest area and from March until December on the southern area. Higher proportions of mature females may be found from January until August on the northwest area and restricted to summer months in the southern area. The distribution of cephalopod paralarvae off the Portuguese coast were analysed based on 19 year of plankton sampling. The effects of temporal and physical variables on Loligo vulgaris, Octopus vulgaris, sepiolid and ommastrephid densities are analysed with GLM models and their distribution patterns discussed in relation to the oceanographic meso-scale features, including currents, thermal fronts, and coastal upwelling cross-shelf transport, prevailing in the western Iberia upwelling system and in the Gulf of Cádiz ecosystem. Temperature and upwelling revealed to be the most determinant variables in modulating population dynamics of neritic paralarvae in the region. The influence of the physical environment is specially pronounced for the paralarvae of O. vulgaris, following distinct patterns according to the oceanography of the western Iberia and the Gulf of Cádiz systems. The paralarvae of oceanic species, which in many cases have their northern limit of distribution at these latitudes, were mainly found in the southern part of the sampling area. The distribution of those species highlighted that the prevailing oceanographic features of the Gulf of Cádiz system, especially fronts, together with temperature act as boundaries to geographic dispersal, contributing for the existence of an area of high cephalopod biodiversity in the southern Portuguese waters, within the transition from subtropical to temperate ecosystems.

vi


Resumo A lula-vulgar, Loligo vulgaris Lamark, 1798, a pota-voadora, Illex condetii Vérany, 1839, e em particular o polvo-comum, Octopus vulgaris Cuvier 1797, encontram-se entre as espécies de cefalópodes mais importantes nas pescarias portuguesas. Todas partilham de um ciclo de vida curto e uma fase planctónica fortemente influenciada pelas condições ambientais regionais.O principal objectivo desta dissertação é um conhecimento mais aprofundado do efeito dos factores ambientais nas estratécies de ciclode vida daquelas espécies. A variação geográfica nos parâmetros biológicos do ciclo de vida das lulas e polvo foi analisada com base na amostragem biológica simultânea dos juvenis e adultos em vários locais da sua distribuição, provenientes da pescaria e cruzeiros demersais e com base na análise da fase paralarvar, através de amostragem do zooplâncton. As características biológicas da lula-vulgar, Loligo vulgaris, das águas do norte de França, noroeste de Portugal, Banco do Sahara e Grécia são analisadas para descrever os padrões biológicos de grande escala e avaliar a variabilidade geográfica desta espécie no Atlântico e Mediterrâneo. Na costa oeste portuguesa e no Banco do Sahara as populações apresentam estruturas de comprimentos complexas, devido aos extensos períodos de recrutamento e desova. A desova ocorre apenas entre Novembro e Abril no norte de França e Grécia. Os índices gonado-somáticos decrescem com a latitude no Atlântico, enquanto que no Mediterrâneo estes os índices são mais elevados. Nas lulas da costa noroeste de Portugal a maturação é atingida a um menor tamanho relativamente a outras áreas geográficas do Atlântico, e atingida a um tamanho semelhante relativamente à população dos mares gregos. O declive da relação comprimento-peso aumenta de norte para sul no Atlântico e do Atlântico para o Mediterrâneo. A análise multivariada dos índices biológicos sazonais demonstrou diferenças biológicas significativas entre populações de áreas geográficas distintas, em particular relativamente ao tamanho de maturação, índice gonado-somático dos machos e tamanho e peso médio individual. Três populações da pota-voadora, Illex coindetii, são analisadas das águas do Mar Celta Sul/Golfo da Biscaia, águas portuguesas e mares da Grécia, tendo-se detectado diferenças entre elas em diversos parâmetros do ciclo de vida daquela espécie. A população das águas portuguesas apresenta o declive da relação comprimento-peso

dos

machos

e

o

tamanho

de

recrutamento

das

fêmeas

significativamente menor do que nas restantes áreas. O comprimento de maturação

vii


(50% maduros) quer dos machos quer das fêmeas das três populações decresce gradualmente do norte do Atlântico para o Mediterrâneo. A época de recrutamento é restringida aos meses de Outono no Mar Celta Sul/Golfo da Biscaia, enquanto que nas águas portuguesas e mares da Grécia o recrutamento se estende ao longo de todo o ano. A principal época de desova é na Primavera e Verão no Atlântico, estendendo-se ao longo de todo o ano nos mares da Grécia. Alguns dos índices biológicos analisados demonstraram correlações significativas com as variáveis ambientais analisadas (temperatura de superfície e concentração de chlorofila-a). A análise dos parâmetros biológicos do polvo-comum, O. vulgaris, entre as populações do noroeste e sul de Portugal evidencia também uma variabilidade geográfica significativa. Os comprimentos e pesos médios são significativamente menores no Verão do que no Inverno na costa noroeste, e a situação inversa ocorre na costa sul. Tal como na lula-vulgar, o aumento em peso com o comprimento do polvo é significativamente maior na costa sul do que na costa noroeste. Diferenças no tamanho de maturação são também encontradas em ambos os sexos, em que o processo de maturação se inicia a um menor tamanho na população da costa noroeste e o peso de maturação resultante é menor relativamente ao polvo da costa sul. Os indivíduos pequenos aparecem na pescaria de covos e alcatruzes em maiores proporções de Junho a Dezembro na costa noroeste, e entre Agosto e Abril do ano seguinte na costa sul. As fêmeas em desova estão presentes ao longo de todo o ano na costa noroeste e apenas entre Março e Dezembro na costa sul. A principal época de desova estende-se de Janeiro a Agosto na costa noroeste (com dois picos distintos) e apenas nos meses de Verão na costa sul. Para melhor interpretar as estratégias populacionais das várias espécies de cefalópodes, a distribuição das paralarvas na costa portuguesa foi analisada com base em 19 anos de amostras de plâncton. Os efeitos de diversas variáveis temporais e ambientais na ocorrência e abundância das paralarvas de Loligo vulgaris, Octopus

vulgaris, sepiolídeos e ommastrefídeos são analisados com modelos lineares generalizados e os seus padrões de distribuição discutidos em relação às condições oceanográficas típicas do sistema de afloramento costeiro da costa oeste ibérica e do Golfo de Cádiz, nomeadamente a dinâmica de afloramento costeiro, correntes e frentes térmicas. A temperatura e o índice de afloramento são as variáveis mais determinantes na dinâmica populacional e distribuição das paralarvas neríticas. A influência do ambiente físico é especialmente evidente nas paralarvas de O. vulgaris, que adoptam distintos padrões de distribuição e sazonalidade de acordo com as condições oceanográficas dominantes dos sistemas de afloramento da costa oeste

viii


ibérica ou do Golfo de Cádiz. As paralarvas das espécies oceânicas, cujo limite norte de distribuição em muitos casos se localiza à latitude de Portugal, distribuem-se maioritariamente na parte sul da área de estudo. A distribuição destas espécies põe em evidência que as características oceanográficas do Golfo de Cádiz, em particular frentes e a temperatura em geral, actuam como barreiras geográficas da dispersão das espécies, contribuindo para a existência de uma área de elevada biodiversidade de cefalópodes no sul de Portugal, na transição entre os ecossistemas tipicamente sub-tropicais e temperados.

ix


x

General Introduction _____________________________________________________________________________________________________________

General Introduction

Cephalopods Cephalopods are among the most attractive of all invertebrates living in the sea, having received the attention of humans since at least the sixteen century BCE (Nixon and Young, 2003). They are apparently able to exploit most of marine habitats, but no cephalopod lives in fresh water. Salinity is considered to be a limiting factor in cephalopod distribution; they are generally restricted to salinity concentrations between 27 and 37‰. The name “Cephalopoda” is derived from the Greek for head and foot (the arms and tentacles attached to the head). Cephalopods can be considered subdominant predators that tend to increase in biomass when other species, particularly their predators and competitors for food, become depleted (Caddy and Rodhouse, 1998). Catches have increased steadily in the last 30 years, from about 1 million metric tonnes in 1970 to more than 3 million tones in 2001, alongside with a finfish generalized decrease (Jereb et al., 2005). Cephalopods are voracious, active predators that feed upon crustaceans, fishes, other cephalopods and, in the case O. vulgaris, on bivalved molluscs. Food conversion is highly efficient, especially in octopuses, where up to 50% of the food eaten can be converted into body mass. More active cephalopods like squids, however, need several times the amount of food required by octopuses and can eat from 3 to 15% of their body weight each day (Jereb et al., 2005). They are often considered ‘ecosystem accelerators’ to explain their main role in the oceanic system. Their high feeding rates and high turnover ratios mean that small increases in cephalopod standing stock result in a large increase in production, with consequent major effects on their predators or prey (Caddy and Rodhouse, 1998). The reproductive systems are highly complex structures with ducts, glands, and storage organs. Fertilized eggs are embedded in one or more layers of protective coatings produced by the oviducal and nidamental glands and generally are laid as egg masses. Egg masses are benthic in Loliginids and Octopodids and

1


pelagic in Ommastrephids. Development of embryos is direct, without true metamorphic stages and hatchlings undergo gradual changes in proportions during development. The term ‘paralarva’ has been introduced for the early stages of cephalopods that differ morphologically and ecologically from older stages. Cephalopods show great resilience to environmental change by having short lives, high turnover of generations, asynchronus growth and maturation, and extended spawning (Boyle and Boletzsky, 1996). This gives the populations the potential to exploit available food resources and overcome short adverse environmental episodes more efficiently (Katsanevakis and Verriopoulos, 2006). It is documented that populations of shelf species can fluctuate enormously from year to year and from season to season, and they survive to flourish in later years (Clarke, 2007). The potential biomass of any cephalopod population is totally dependent on the success of recruitment, conditions for growth and exposure to predation in that year, because there is no overlap between successive generations (Boyle and Boletzky, 1996). Therefore, despite their great resilience to environment, cephalopod populations are also extremely vulnerable to large adverse fluctuations of biological and physical variables, in particular during the paralarva phase. During the last 10 years, special attention has been given to the link between environmental variables and recruitment success or failure, using diverse variables as proxies for oceanographic variability (Semmens et al., 2007). Similarly, several studies and research projects began to address the influence of environmental variables on life cycle strategies of several cephalopod species. However, the understanding of these relationships is still in a very incipient stage. The present study aims to evaluate the biological geographic variation of some cephalopod species and discuss the influence of different oceanographic regimes on each population life history traits. This study focus on the three most important cephalopod fishery resources in Portugal, which have planktonic paralarvae: the squids Loligo vulgaris and Illex coindetii, and the octopus Octopus

vulgaris. Special attention is given to cephalopod paralarvae on Portuguese waters. The following section is a summary of the oceanography of the northwestern and southern Portuguese waters considered important for the understanding of the life cycle strategies and distribution patterns of paralarvae.

2


Further details on the main environmental features of other European areas analysed are given in the respective chapter.

Oceanography of the Portuguese waters relevant for the study The western coast of Portugal is within the North Atlantic Upwelling Region, which extends from the northern Iberian Peninsula at 43ºN to the south of Senegal at ~10ºN. This area is characterized off-shore by slow broad equatorward gyre recirculation, a meridional alignment of coastlines and a predominant equatorward wind. These winds force an offshore Ekman transport in the upper layer and the consequent decline of the sea level towards the coast. As a result an equatorward jet is formed, transporting cold and nutrient rich upwelled water (Relvas et al., 2007). Downwelling occurs when poleward winds induce net onshore surface Ekman transport, resulting in surface coastal convergence and, to compensate, deeper waters flow offshore. These flows act as a source of cross-shelf dispersion of passive particles (e.g. eggs/larvae) onshore or offshore, depending on location or vertical migration in the water column (Marta-Almeida et al., 2006; Peliz et al., 2007). The large-scale circulation in the western Iberian Peninsula comprise the broad southward-flowing Portugal Current (PoC) extending from the coast to about 24ºW (Pérez et al., 2001) and the eastern branch of the Azores current (AC), which transports eastwards warm and salty sub-tropical water until meeting the continental shelf (Pingree et al., 1999). During winter the direction of the dominant wind changes and a subsurface, density-driven current, the Iberian Poleward Current (IPC), flow poleward in the vicinity of the shelf-break (Peliz et al., 2005). Two thermal fronts are recurrent in the Iberia basin (Peliz et al., 2005): the Western Iberia Winter Front (WIWiF), which is formed only in winter at about 3940ºN (separating the colder northern waters from the southern warmer waters), and further to the south, the permanent Azores Current/Subtropical Front at ~3536ºN (Fig. 1).

3


Figure 1. The western Iberia and Gulf of Cádiz regimes in a) spring and summer, and b) autumn and winter. 1) Cape Finisterre; 2) River Douro; 3) Cabo da Roca; 4) Cape St. Vincent; 5) Guadiana River; 6) Guadalquivir River; 7) Strait of Gibraltar (from Mason et al., 2005).

4


The main upwelling season in the western Portuguese coast occurs between April and October, with maximum offshore Ekman transport between July and September (Wooster et al., 1976; Fiúza et al., 1982). In spite off the surface westward transport, during spring and summer upwelling, fronts along the shelf break may form, acting as a barrier to offshore dispersal away from the continental shelf (Bakun, 1996). A double frontal system is recurrent on the wider northwest shelf (Peliz et al. 2002). The main upwelling front, associate to the high speed current flowing equatorward over the continental shelf and slope (Upwelling jet), is meridionally oriented along the mid-shelf in summer, slightly off the 100 m isobath. That tongue of cold upwelled water with temperatures below 18.8 ºC is limited at the inner-shelf side by a warm intrusion with values between 19.0 and 19.8ºC, forming a second inshore upwelling front. The buoyant plume off western Iberia (WIBP), is present throughout the year and could be responsible for poleward advection in the inner shelf, close to the coastline (Peliz et al., 2002). During spring, a shallow thermocline starts to develop and the thermal stratification of the water column gives rise to a mild thermocline near the surface. Zooplankton peaks in April, more abundant over the slope and outer-shelf than over the inner-shelf (Cunha, 2001). In summer the ocean is highly stratified due to solar radiation and the thermocline become shallower and the upper layers nutrient depleted. Zooplankton has maximum biomass during late spring and early summer. The large zooplankton organisms tend to concentrate in the outer-shelf (Cunha, 2001). In autumn northerlies relax and begin a period of mainly coastal convergence (with some intermittent periods of upwelling) and warm and salty subtropical water flows into the shelf. The mixed layer is cooler than in summer and the upper 50 m is almost isothermic. During winter there is south-westward transport over the shelf of relatively cold, low salinity water from river runoff, giving rise to a highly stratified water mass with a shallow pynocline (Cunha, 2001). The discontinuity between the stratified shelf waters and the well-mixed open ocean forms a shelf-break front associated to the slope poleward flow (IPC, Peliz et al., 2003). Under downwelling-favourable winds, passive particles at the surface tend to move inshore until they enter the inner-shelf region, beyond the downwelling front, where they may be advected polewards by the WIBP and river plumes

5


associated with maximum rainfalls (Peliz et al., 2002). On the contrary, deeper particles tend to move offshore towards the open ocean, where they may be retained by the shelf-break front or advected polewards by the IPC beyond the front (Peliz et al., 2005). Zooplankton levels decrease during autumn and in winter levels are the lowest. The higher abundance is located in the outer shelf in autumn and in the inner shelf during winter (Cunha, 2001). The southern coast of Portugal is located within the Gulf of Cádiz ecosystem, between the North Atlantic and the Mediterranean Sea. It is limited at the west by the Cape St Vicente where the shoreline changes orientation from north to east at almost right angle. The Gulf of Cádiz separates the “western Iberian upwelling” from the “African upwelling systems”, between which continuity of flow is thought to be absent (Barton 1998). The large scale circulation of this area is mainly anticyclonic (García et al., 2002, Sánchez and Relvas, 2003) and affected by the eastern branch of the Azores, which advects warm and salty water eastwards. There are some indications that the large-scale circulation in winter may be occasionally cyclonic, flowing westwards along the northern Gulf of Cádiz (Folkard et al., 1997, Jia, 2000). The prevailing anticyclonic oceanic circulation provides a unidirectional connection between the northern Gulf of Cadiz and the Mediterranean Sea, while in winter the cyclonic circulation favour an inflow from the northern African shelf (García-Lafuente and Ruiz, 2007). The orientation of the southern Portuguese coast does not favour upwelling under northerly winds. Upwelling and downwelling events tend to be weak and the circulation is mainly wind forced and influenced by the local orography. The prominent Cape Stª Maria divides the continental shelf in two shelves of different shape that hold different oceanographic processes. The wider eastern shelf (~50 km) is more productive due to important river inputs and tidally-driven processes, which are independent of wind and represent a continuous source of nutrients. The narrower western shelf (~15 km) cut by the steep Portimão submarine canyon is more oligotrophic (García-Lafuente and Ruiz, 2007). However, westerly winds result in cold, low saline but nutrient rich upwelled water extending from the western Iberian Peninsula around Cape St. Vicente, flowing eastward along the slope and shelf break (Fiúza, 1983, Relvas and Barton, 2002). Additionally, during spring and summer westerlies occasionally induce generalised upwelling along the

6


southern coast of Iberian Peninsula. The upwelled water is transported either along the shelf break front or directly offshore by an upwelling filament anchored off the Cape Stª Maria (García-Lafuente and Ruiz, 2007). Inshore of the upwelling jet, a counter current of warmer and salty water flow poleward from the southern coast to the western coast (Sánchez and Relvas, 2003). This alongshore current is recurrent on the eastern shelf of the northern Gulf of Cádiz. Right after upwelling relaxation and under easterlies it flows beyond Cape Stª Maria invading the western shelf providing transport of biological material from the east to the west and a biological connection of the entire southern Portuguese shelf (GarcíaLafuente et al., 2006, Teles-Machado et al., 2007). In this case, the eastward extension of cooler water beyond Cape St. Vicente is less pronounced, and warmer water occupies a larger extension of the south Portuguese shelf (Fig.2). The conditions during winter are different from summer, because cool waters invade the entire coastline area (Mason et al., 2005). The mixed-layer reaches 150 m during this season (García-Lafuente and Ruiz, 2007).

Figure 2 - Sketch of the surface circulation in the Gulf of Cádiz. N2 = AC branch, Cyclonic eddy off Cape St. Vicente (SVE), N1 = Huelva front, CCC = coastal counter current. Dashed arrow = CCC bifurcates off Cape Santa Maria under easterlies and a branch invades the western shelf, making the SVE drift to the south (from García-Lafuente and Ruiz, 2007).

7


8

Part 1 – Geographic variation in the population dynamics of squid and octopus juveniles and adults

Chapter 1 - Biological variation of Loligo vulgaris _____________________________________________________________________________________________________________

Chapter

1.

Biological

variation

of

Loligo

vulgaris

(Cephalopoda: Loliginidae) in the eastern Atlantic end Mediterranean

1.1. Introduction Loligo vulgaris Lamark, 1798 is a neritic species living in temperate waters in the eastern Atlantic, from the North Sea and around the British Isles (55ºN) to the western African coast (20ºS), and throughout the Mediterranean Sea (Roper et

al., 1984). L. vulgaris and L. forbesi are the main targets of squid fisheries on the Atlantic European coasts. Catches of commercial importance are taken mainly by the United Kingdom, France, Spain and Portugal (Boyle and Pierce, 1994). Separate landings statistics for the two species are not recorded. In the northeast Atlantic Loligo species are mainly a by-catch of the multi-species bottom trawl fisheries, although some directed small-scale hand-jig fisheries exist in Spain (Guerra et al., 1994) and Portugal (Coelho et al., 1994a). However, L. forbesi is known to be more abundant in the northern areas, being replaced southwards by

L. vulgaris. In the Mediterranean, Loliginid populations, mostly made up of L. vulgaris, are not targeted, but are heavily fished by Spain and Italy (Worms, 1983). Published cephalopod fishery and abundance studies from the eastern Mediterranean are very limited, in particular with reference to L. vulgaris (e.g., D’Onghia et al., 1996; Lefkaditou et al., 1998). Unlike the northeast Atlantic and Mediterranean fisheries, L. vulgaris is an important secondary target species in the Saharan Bank cephalopod trawl fishery (Raya et al., 1999). Research on aspects of the life-cycle of L. vulgaris from various parts of its distribution, includes studies from the northeast Atlantic: the Dutch coast (Tingbergen and Verwey, 1945), the Galician coast (Guerra and Rocha, 1994; Rocha, 1994; Rocha and Guerra, 1996), and the Portuguese coast (Coelho et al., 1994a; Moreno et al., 1994, 1996; Bettencourt et al., 1996; Villa et al., 1997); from the central-east Atlantic (Baddyr, 1988; 1991; Bravo de Laguna, 1988; Arkhipkin, 1995; Raya et al., 1999); and from the western Mediterranean (Mangold-Wirz,

11

Ana Moreno 2008 – Cephalopod Life History Traits

_____________________________________________________________________________________________________________

1963, Worms, 1980, 1983; Natsukari and Komine, 1992). There are no published studies on the population biology of L. vulgaris in the eastern Mediterranean. Moreover, most studies were undertaken in distinct periods within a range of 50 yrs. Nevertheless, a certain degree of consistency can be found for some of the biological characteristics of L. vulgaris across its range. The following aspects can be considered typical of the species: a 1:1 sex ratio, a complex population structure driven by protracted recruitment and spawning periods, spawning in the colder seasons, spring and summer recruitment, lower size at maturity in males, and a one year life span (estimated from statolith analysis). A multinational European research project (FAIR CT96 1520) provided support for new biological data collection and a new analysis of historical data on

L. vulgaris. The surveyed areas (the English Channel, the Portuguese coast, the Saharan Bank, and the Greek Seas) have different environmental conditions, namely temperature regimes and food availability. This paper aims to describe broad-scale biological patterns of L. vulgaris populations and to evaluate the geographic variation, based on similar sampling at the limits of its distribution: from northern (English Channel) and southern areas (Portugal) in the northeast Atlantic, from the central-east Atlantic (Saharan Bank) and from the eastern Mediterranean (Greece). Furthermore, this paper examines the relationships between biological and environmental variation.

1.2. Material and Methods 1.2.1. Biological sampling Samples of L. vulgaris were collected monthly from the northeast Atlantic (English Channel and Portuguese waters) and the eastern Mediterranean (Greek Seas), between January 1997 and June 1999. Available historical data from the central east Atlantic (Saharan Bank) were re-analysed and used for comparisons, when appropriate. Fishery data (landings of L. vulgaris from all fishing gears) from the four areas were analysed for the period 1997–1998.

12


Samples from the English Channel (hereafter referred to as north France) were collected from trawl fishery landings at the Port-en-Bessin fish market between January 1997 and May 1999 (1475 specimens), during the periods when this species is present in the catches. The offshore bottom trawlers use nets with 80 mm cod-end stretched mesh size. The fishing grounds are located at a depth range of 50 to 150 m (49.5ºN - 50.5ºN, 1ºE - 5ºW). Portuguese samples (hereafter referred to as northwest Portugal) were taken from the trawl fishery landings in Peniche and Nazaré markets, between January 1997 and June 1999 (3040 specimens). Here, the fishing grounds are located off the coast (39º - 40.5ºN, 9ºW) at a depth range of 60 to 90 m. The stretched trawl mesh is approximately 65 mm long. Samples of all commercial size categories from the Saharan Bank (hereafter referred to as Saharan Bank) were obtained from the Spanish commercial trawl fishery (881 specimens) in June, September, November and December 1993, and January 1994 (21º – 28ºN, 13º - 17ºW). The trawlers use nets with a stretched mesh of 60 mm. Additional samples were collected during a research cruise onboard the Moroccan RV “Charif al Idrissi” in April 1994 (377 specimens). In this area, fishing grounds are located between 50 and 100 m depth.

L. vulgaris was also sampled from the trawl fishery in Greece (hereafter referred to as Greek Seas), between October 1997 and May 1999 (35 – 41ºN, 21 – 26ºE) (880 specimens). Commercial bottom trawlers use cod-end stretched mesh sizes of 26 mm. Fishery samples were not taken from June to September as this period is closed for the trawl fishery, but additional samples were collected when possible during research cruises in the RV “Philia” by means of a commercial net: in July 1997 and May 1998 (162 specimens). Squid sampling methods were similar within and between localities. Dorsal mantle length (ML) was recorded in all specimens. The monthly sampled specimens were sexed, body weight (BW) recorded, and maturity assessed (maturity scale after Lipinski, 1979 in the Saharan Bank and after Boyle and Ngoile, 1993 in the other areas). Gonad weight (testis or ovary) (GW) was recorded for sub-samples of the monthly samples.

13


_____________________________________________________________________________________________________________

1.2.2. Data analysis Variables of ML, BW, recruitment, maturity, size at maturity and sex ratio (22 biological indices) were computed for each time period, for each area and for the whole area. Average ML, overall (AvgML, mm) and by sex (AvgMLM and AvgMLF), and average BW, overall (AvgBW, g) and by sex (AvgBWM and AvgBWF) were estimated. The averages by sex were compared between geographic areas for the period October 1998-June 1999 (Saharan Bank, October 1993-June 1994) by two-factor ANOVA (area and trimester as factors). Individual measures (ML and BW) by sex were used in the analysis as replicates within trimesters. Since the F test is remarkably robust to deviations from normality and violation of homogeneity of variances (Lindman, 1974), only the correlation between variances and means was tested as a criteria for the applicability of ANOVA. A Scheffé test was performed to evaluate differences between pairs. The recruitment season in each area was determined by a Recruitment Index (RI) computed to standardised sample sizes between months and between areas (to 100 squid by sampled month in each area). The computation of the RI assumes that recruits are animals with ML < T. The species threshold T was defined as the modal ML of the size frequency distribution, thus:

Rm = number of recruits observed in month m R = ∑ Rm (all the recruits observed in a fishing season - from July to June next

year)

RI =

Rm R Sex ratios were estimated as the ratio of males to females (SR) in

standardized sample sizes. Significant deviations from 1:1 were tested (each quarter within each area and for the whole sampling period and area) by Chi-square tests. The spawning season was determined by evaluating the monthly proportion

14


of mature males (%matM) and females (%matF) in standardized sample sizes, and the average Gonadosomatic Index. The Gonadosomatic indices were calculated for maturing and mature males (GSIallM) and females (GSIallF), and for mature males (GSImatM) and mature females only (GSImatF), with 95% confidence interval as: n

GSI =

∑ GW

i

i =1

n

∑ ( BW i =1

i

− GWi )

The minimum size at maturity was defined as the ML of the smallest mature squid (MLmim, mm), male (MLminM, mm) or female (MLminF, mm) found in each period. Maturity curves were fitted using a logistic function (Sparre et al., 1989) for the percentage of mature animals in length class l,

Pl =

P max 1 + e −(a +bl )

[

]

Assuming Pmax = 1 it is possible to use a linear transformation of the same model, in the form:

ln(

Pl ) = a + bl Pmax − Pl Intercepts and slopes of the linear model were compared for each sex

between geographic area by the method in Campell and Madden (1990). The size at which 50% of males (ML50M, mm) or females (ML50F, mm) are found mature, was derived as the ratio of the parameters of the linear model above (ML50 = a/b), when a significant fit was obtained (least squares regression, P < 0.05). Length-weight relationships by trimester (power model: BW = a*MLb) were statistically compared for each area, by analyzing the similarity between intercepts and slopes (SlopeM and SlopeF) of the log transformed model, using the method

15


_____________________________________________________________________________________________________________

suggested by Campell and Madden (1990). A selection of variables from those above, computed by trimester and grouped by location, to include in the multivariate analysis was achieved by the following procedure: (a) a preliminary analysis of variance (one-factor ANOVA) was performed on the scores of the 22 variables. Missing values were replaced by within location arithmetic mean and the correlation between variances and means evaluated, (b) when the separation by location was significant, i.e., when the variance was greater inter-location than intra-location, and no significant correlation between variances and means was detected, the variable was selected. The selected variables were subsequently standardised (mean subtracted from each variable and the result divided by the standard deviation) and a discriminant analysis performed using the routines implemented in the Statistica v.5 software.

1.3. Results 1.3.1. Fisheries In the Atlantic and Mediterranean L. vulgaris is caught mainly as a bycatch of the multi-species trawl fishery. The seasonal pattern of L. vulgaris landings is somewhat similar across the range with higher landings in autumn or winter (Fig. 1.1). As it is mainly a by-catch fishery and catches are usually landed, the seasonal pattern of landings produces a good picture of the seasonal pattern of abundance in each area. The main geographic differences are the low landings of squid in February in the Saharan Bank, and the high landings in late summer in northwest Portugal, contrasting with the very low landings or absence of squid in north France and the Greek Seas, in late spring and summer months. The total absence of squid landings in north France in summer may not indicate total absence of the species, but presence of specimens below recruitment size. In the Greek Seas the low landings in late spring and summer may reflect the low catches of other fishing gears, at the time when the trawl fishery is closed, on a population of mostly small squid.

16


800 700

Landings (tonnes)

600 500 400 300 200 100 0 J

F M A M

J J A Month

N France (F) Saharan Bank (SB)

S

O N D NW Portugal (P) Greek Seas (G)

Figure 1.1. Monthly landings of Loligo vulgaris in the Atlantic and Mediterranean, average over 2 yrs (1997 and 1998) from all fishing gears. Absence of some monthly data corresponds to closed fishing seasons.

1.3.2. Size and recruitment The range of mantle lengths (ML) sampled was between 29 and 640 mm and that of body weights (BW) between 1 and 2302 g. This species is sexually dimorphic, with males attaining greater lengths and weights than females (Table 1.1). Averages for the whole area were similar between sexes, 160 mm and 180 g. Squid from the four geographic areas differ significantly in ML and BW (twofactor ANOVA ‘area’ P 3) in males and negatively allometric (b < 3) in females.

2.3.5. Recruitment Females are fully recruited in the size of 170 mm in samples from the Southern Celtic Sea and Bay of Biscay and from Greek Seas while for female samples from the Portuguese waters this size drops to 110 mm. Size at which males are fully recruited is 150 mm, throughout all areas sampled (Table 2.1). Following the plots of the percentages of recruits (females and males, stage I) over the sampling period (Fig. 2.2), two autumnal recruitment peaks, during 1997 and 1998 were recorded for the female squids in samples from the Southern Celtic Sea and Bay of Biscay, while male recruits showed very low percentages throughout the entire period. Female recruits were recorded in high percentages from the Greek Seas during winter and spring 1998 and during autumn 1998 and winter 1999. For males from the Greek Seas recruitment peaks were observed during winter and spring 1998 and during winter 1999. Finally, in the samples from Portuguese waters, recruitment percentages were high for both females and males during winter and summer of 1997 and autumn 1998.

2.3.6. Maturation The higher percentages in mature males and the earlier occurrence of mature males in relation to females is a common feature in the short-finned squid populations in all three sampled areas (Fig. 2.2). Another common observation was the absence of spent males and the low percentage of maturing animals (maturity stage III, 6.8 % of the total number of the individuals sampled). Immature females (stages I and II) are found at higher percentages during the first and fourth trimester while maturing and mature (stage III and stages IV and V,

44

Chapter 2 – Biological variation in Illex coindetii _____________________________________________________________________________________________________________

respectively) are mostly found during the second and third trimester in the samples from all the studied areas. Maturing and mature males were found to be abundant during the entire sampling period in samples from the Southern Celtic Sea and Bay of Biscay and from the Greek Seas, while in those from the Portuguese waters only during the second and third trimester. It should be noted that maturing males were found at high percentages only during the fourth trimester of 1998 and first of 1999, in the samples from the Southern Celtic Sea and Bay of Biscay, while in the remainder sampling areas maturing males were always in low percentages.

Figure 2.2. Percentage of the maturity stages of female and male short-finned squids, by trimester.

45


In the mature females from the Southern Celtic Sea and Bay of Biscay peaks of GSI values were scored during February to April of 1998 and 1999 and during September 1998 (Fig. 2.3). Peaks of mature females GSI values in the samples from the Greek Seas were recorded during April and August 1998 and during January and May 1999. Mature male GSI values were almost invariable for almost the entire sampling period in both of these areas, with slightly raised values in February and June 1998 and March 1999 in the samples from the Southern Celtic Sea and the Bay of Biscay and, with also slightly raised values during February to May 1999 in the samples from the Greek Seas. Values, as well as peaks of GSI derived from all animals follow those derived from mature animals with a few exceptions only. Males and females showed increasing maturity with size, in all studied areas (Fig. 2.4).

Figure 2.3. Monthly GSI values for females and males.

In Portuguese waters, very few females occurred above 250 mm and among those a small percentage was not mature animals. Females from the

46


Greek Seas showed a different pattern: at 170 mm, more than 69% of females were mature, but at 200 mm, only 47% of females were mature; at >210 mm, 100% of females were mature. These data may suggest that females from Greek Seas mature at two different modal sizes: first mode size at maturity is estimated at 140 mm and second between 190 and 360 mm. Nevertheless, the small number of animals after the inflexion point (6.4% of mature animals) and the fact that the animals were not directly aged during the present study do not permit any further analysis (e.g., Collins et al., 1995).

Figure 2.4. Cumulative percentage of mature females and males against length. Standard logistic curves are fitted for the estimation of the L50 values (straight lines).

47


Fitting the standard logistic function, the L50 for females from the Southern Celtic Sea and Bay of Biscay was estimated as high as 248 mm, for those from the Greek Seas 179 mm, and from the Portuguese waters 181 mm. For the males the L50 values were 153 mm, 113 mm and 129 mm, respectively (Fig. 2.4). A comparison of the L50 values estimated from areas along the Eastern Atlantic and the Mediterranean is given in Table 2.3. In the three sampled areas, gonad weight averaged 5.37% of the BW for females and 2.28% of BW for males.

Table 2.3. Comparison of the L50 values for females and males as calculated from areas along the Eastern Atlantic and Mediterranean. Area

L50 value (mm) Females

Reference

Males

S. Celtic Sea - Bay of Biscay

248

153

This study

Northwestern Africa

208

160

Hernández-Garcia and Castro, 1995

Galician waters

184

128

González and Guerra, 1996

Portuguese waters

191

129

This study

Western Mediterranean

150

120

Sánchez et al., 1998

Sicilian Channel

150

120

Jereb and Ragonese, 1995

Greek Seas

179

113

This study

2.3.7. Sex ratio There were more months where the sex ratio was significantly different from the expected 1:1 in the samples taken from the Southern Celtic Sea and Bay of Biscay than in samples taken from Greek Seas and Portuguese waters (Table 2.4). No significant differences were observed in the total female and male numbers over the entire sampling period, in all areas. In the Southern Celtic Sea and Bay of Biscay, males were predominant in four months out of the eighteen of the sampling period, while females were predominant in three. In all of these cases, sex ratio was close to 1.5-2:1 except in September 1998 where the ratio rose to 4:1 females to males. In the Greek Seas, sex ratio was 2-2.5:1, and males were only found in significantly higher numbers than females, in four months. Finally, in the Portuguese waters, male numbers

48


were significantly higher than female numbers in three months (ratio range, 13.9:1), while the opposite case occurred only once (2:1).

Table 2.4. Results of chi-square test performed on monthly sex ratio values. Y-M: year-month; nF: number of female individuals; nM: number of male individuals; Significance level: *: P < 0.05; **: P < 0.01. S. Celtic Sea – Bay of Biscay

Greek Seas

Y−M

nF

nM

χ2

Y −M

NF

1997-11

59

49

0.85

1997-5

26

1997-12

81

85

0.05

1997-11

1998-1

91

102

0.32

1998-2

44

52

1998-3

38

1998-4

nM

Portuguese waters χ2

Y−M

nF

nM

χ2

42

5.53**

1997-2

552

527

0.05

11

17

4.59*

1997-5

105

147

2.77

1997-12

9

18

11.11**

1997-6

101

163

5.51

0.69

1998-1

17

13

1.77

1997-7

17

26

4.38*

43

0.38

1998-2

22

30

2.36

1997-10

206

197

0.04

27

55

11.65**

1998-3

69

76

0.23

1997-11

32

34

0.09

1998-5

39

40

0.16

1998-4

23

26

0.37

1998-4

35

44

1.29

1998-6

25

35

2.77

1998-5

46

66

3.18

1998-5

96

119

1.14

1998-7

14

31

14.27**

1998-8

67

166

18.05**

1998-6

281

375

2.05

1998-8

15

12

1.23

1998-10

23

33

3.18

1998-7

92

101

0.21

1998-9

12

3

36.00**

1998-11

69

85

1.07

1998-8

28

14

11.11*

1998-11

12

24

11.11**

1998-12

35

29

0.87

1998-10

124

115

0.14

1998-12

89

83

0.12

1999-1

30

37

1.09

1998-11

21

34

5.58**

1999-2

50

59

0.68

1999-2

51

63

1.1

1999-6

122

479

35.28**

1999-3

53

89

6.42**

1999-3

57

71

1.19

1999-4

32

32

0

1999-4

18

24

2.04

1999-5

47

26

8.27**

1999-5

57

49

0.56

1999-6

41

27

4.23**

2.3.8. Correlation with environmental variables Values of Spearman’s rank correlation coefficient (r) performed between biological indices, and average SST values (and Chl-a, for the Greek Seas only), as calculated by month and by trimester within each area, are shown in Table 2.5. Both length and weight were found to be negatively correlated (though weakly) with SST monthly values in the samples taken from the Southern Celtic Sea and

49


Bay of Biscay. When female individuals only were considered, gonado-somatic index of mature animals was also negatively correlated with SST average values. When biological indices were calculated over trimester intervals, male gonado-somatic index (as calculated for matured animals), maximum length, maximum weight, and regression slope were strongly but negatively correlated, with SST values. Similar results have been obtained from the samples from Portuguese waters, with the addition of the positive and strong correlation of the recruitment index with the SST values as calculated by trimester. No significant correlation was found when the lifecycle indices were estimated on a monthly basis. The reverse correlation was revealed from the samples from the Greek Seas: SST values were positively correlated with length and weight of males and negatively correlate with recruitment index. Monthly average Chl-a values were found to be negatively correlated with female maximum weight values only. Male recruitment, spawning, length and weight, and female recruitment index were found to be negatively correlated with the range of Chl-a values, calculated on a trimester basis.

2.4. Discussion The high spatial and inter-annual variation in ommastrephid landings along with the mixed landings primarily of the species I. coindetii and T. eblanae are two of the characteristics of the ommastrephid fisheries throughout the Mediterranean and the Eastern Atlantic (e.g., Stergiou, 1989; Sánchez et al., 1998). The only observable pattern in landings was recorded in the Southern Celtic Sea and Bay of Biscay where raised values were observed during winter and spring. Highly variable annual catches have also been recorded for I. illecebrosus in the Canadian waters (Amaratunga et al., 1978; Dawe, 1988) and for I. argentinus off the Argentine exclusive economic zone (Arkhipkin, 1993). Based on the relevant literature (cited below) of the species from the European Atlantic and Mediterranean waters, the size of I. coindetii reaches 379 mm and 1630 g. The highest female DML and BW values were recorded from the Galician waters (González and Guerra, 1996) and from the Greek Seas (this

50

Table 2.5. Correlation (Spearman’s coefficient) between SST and Chl-a values and biological indices, calculated by month and by trimester, for the samples from the three studied areas. RI: recruitment index; Spawning: proportion of the mature animals; GSI all: gonadosomatic index calculated for all animals; GSI mat: gonadosomatic index calculated for mature animals only; rng: range of values; mat: mature animals, DML: dorsal mantle length; BW: total body weight; slope: regression length-weight slope. S. Celtic Sea – Bay of Biscay

Sex

Indices

F

RI

Greek Seas

Month

Trimester

Month

Trimester

SST avg

SST avg

SST avg

SST avg

Month

Trimester Chl-a avg

SST avg

SST avg

Chl-a avg

R

P

R

P

R

P

R

P

R

P

R

P

R

P

Rp

P

0.28

0.25

0.19

0.67

-0.12

0.66

0.78*

0.02

-0.55**

0.01

0.02

0.44

0.56

0.4

-0.78*

0.03

Spawning

-0.23

0.34

0.09

0.84

-0.05

0.85

-0.69*

0.05

0.26

0.31

-0.32

0.22

0.01

0.81

0.5

0.25

GSI all

-0.19

0.42

-0.16

0.72

-

-

-

-

0.08

0.92

-0.16

0.56

-0.28

0.72

0.14

0.75

-0.48**

0.04

-0.09

0.84

-

-

-

-

-0.11

0.61

0.26

0.32

-0.4

0.9

0.1

0.81

-0.41

0.08

-0.44

0.31

0.25

0.38

0.33

0.41

0.21

0.34

0.14

0.59

-0.46

0.52

0.5

0.25

GSI mat min DML mat min DML

-0.34

0.15

0.05

0.9

0.3

0.29

-0.63

0.09

0.29

0.42

0.16

0.54

0.03

0.89

0.5

0.25

max DML

-0.45*

0.05

-0.3

0.5

-0.23

0.41

-0.41

0.3

0.57**

0.01

-0.4

0.11

-0.33

0.92

0.32

0.48

avg DML

-0.48*

0.03

-0.52

0.22

0.03

0.89

-0.71*

0.04

0.67**

0.002

-0.37

0.15

-0.33

0.81

0.39

0.38

min BW

-0.1

0.68

0.3

0.5

0.28

0.32

-0.4

0.31

0.28

0.38

0.14

0.59

0.16

0.87

0.28

0.53

max BW

-0.49*

0.03

-0.45

0.31

-0.14

0.61

0.35

0.38

0.49*

0.03

-0.65**

0.006

-0.15

0.82

0

1

avg BW

-0.45*

0.05

0.03

0.93

0.07

0.79

-0.71*

0.04

0.66**

0.002

-0.44

0.08

-0.41

0.73

0.67

0.09

-

-

-0.16

0.1

-

-

-0.74*

0.03

-

-

-

-

-0.06

0.91

0.32

0.48

0.43

0.06

0.59

0.15

-0.19

0.51

0.83**

0.01

-0.44

0.08

0.32

0.21

-0.75**

0.01

0.71

0.07

slope M

Portuguese waters

RI Spawning

0.28

0.22

0.07

0.87

-0.01

0.95

-0.45

0.26

0.4

0.38

-0.39

0.12

0.26

0.62

-0.92**

0.002

GSI all

-0.11

0.62

-0.61

0.14

-

-

-

-

-0.28

0.45

0.12

0.64

-0.36

0.31

0.57

0.18

GSI mat

-0.22

0.35

-0.88**

0.01

-

-

-

-

-0.56

0.22

0.44

0.08

-0.38

0.42

0.67

0.09

min DML mat

-0.35

0.13

-0.55

0.2

-0.06

0.82

0.33

0.41

-0.09

0.92

0.12

0.63

-0.26

0.75

0.21

0.64

min DML

-0.07

0.75

-0.18

0.68

0.31

0.27

-0.28

0.49

0.11

0.66

0.05

0.85

-0.03

0.91

-0.1

0.85

max DML

-0.58**

0.01

-0.87**

0.01

-0.03

0.89

0.09

0.82

0.29

0.37

-0.33

0.2

0.51

0.18

-0.39

0.38

avg DML

-0.46*

0.04

-0.55

0.19

0.03

0.89

-0.71*

0.04

0.62

0.09

-0.32

0.22

0.71*

0.05

-0.85**

0.01

min BW

0.32

0.16

-0.08

0.86

0.42

0.12

-0.43

0.27

0.18

0.56

-0.09

0.71

0.05

0.91

-0.28

0.53

max BW

-0.6**

0.01

-0.81**

0.02

-0.05

0.85

-0.33

0.41

0.38

0.25

-0.41

0.11

0.45

0.37

-0.14

0.75

avg BW

-0.2

0.04

-0.16

0.72

0.02

0.93

-0.76*

0.02

0.67**

0.002

-0.53*

0.03

0.65

0.45

-0.92**

0.002

-

-

-0.88**

0.01

-

-

-0.28

0.49

-

-

-

-

-0.21

0.62

0.39

0.38

slope

51


study). Maximum male DML and BW values were recorded from Galician waters and Southern Celtic Sea and Bay of Biscay (320 mm by 606 g; Sánchez et al., 1998, and present study, respectively). The low percentage of females from the Portuguese waters with DML > 250 mm cannot be attributed to the low number of animals sampled (over 4000) but, rather, to the population structure in this particular area. Similar results have been reported from a population of the species studied in the Sicilian Channel of the Mediterranean (Jereb and Ragonese, 1995). The previously mentioned maximum size values are comparable with those reported for the congener species distributed on the other side of the Atlantic: I. illecebrosus (Amaratunga et

al., 1978; Laptikhovsky and Nigmatullin, 1993) and I. argentinus (Nesis, 1987 ; Arkhipkin and Laptikhovsky, 1994), but larger than those reported for the T.

eblanae populations (González et al., 1994; Hastie et al., 1994) studied in the European waters. A comparison between available information on growth rate and life span of I. coindetii populations studied in the Eastern Atlantic and the Mediterranean and the results of the present study are presented in Table 2.2. Growth rates may well range from 0.32-1.78 mm d-1 and life span from 0.5-2 yrs, depending on the studied area and on the method performed. Results derived by MPA, during the present study, suggest faster growth than the previous estimations, and are comparable with those derived by direct ageing of populations from the Galician waters and Western Mediterranean (González et al., 1996; Sánchez, 1995; Sánchez et al., 1998) although the major disadvantage of the indirect (MPA) method is that the multi-cohort structure of squid populations, combined with the simultaneous presence of different ontogenetic stages, mask natural modes and do not allow MPA to resolve them entirely and detect their appearance in certain time intervals (Caddy, 1991; Pierce

et al., 1994). Additionally, the presence of female immature (González et al., 1996) and maturing (this study) outliers indicates an even greater maximum age of the species from that already reported in the literature. Studies in I. illecebrosus (e.g., Dawe, 1988; Coelho et al., 1994b) and in I. argentinus (e.g., Rodhouse and Hatfield, 1990; Laptikhovsky and Nigmatullin, 1993; Arkhipkin and Laptikhovsky, 1994) suggest a 1 yr life span. Finally, Hastie et al. (1994) found a life span of 1-2

52


yrs for both sexes of T. eblanae in populations from the Scottish coastal waters. The existence of positive allometry in mature males and negative allometry in females in the length-weight relationship has been considered as indicative of the general morphological and functional characteristics not only of the species I. coindetii (Sánchez et al., 1998) but of the entire family Ommastrephidae (Forsythe and van Heukelem, 1987). This has been consistently reported from studies along the Mediterranean and the Northeastern Atlantic (e.g., González et al. 1994, 1996; Sánchez et al., 1998) with two exceptions: (a) in the Tyrrhenian Sea (Belcari, 1996), where female length-weight slope found to be isometric; (b) in the Northwestern Spain, where the slope was found to be higher than three but still lower than the corresponding one for males (Sánchez et al., 1998). Positive allometric growth in the case of males may be interpreted as greater strength in the arms which increases the effectiveness of copulation, while in the case of females negative allometric growth may be explained by the large variability of ovary mass in mature individuals and, consequently, the size at which full maturity is reached. However, positively allometric length-weight relationship was observed for both sexes of I. illecebrosus populations studied in the Newfoundland and the eastern Canadian waters (Amaratunga et al., 1978; Dawe, 1988). In the T. eblanae populations studied from the Scottish and Galician waters (González et al., 1994; Hastie et al., 1994), slopes were consistently < 3 for both sexes, with male slope significantly higher than female slope only in the latter population. The consistent appearance of recruits throughout the year is a feature commonly shared in all sampling areas. However, peaks of recruitment events show spatial and inter-annual variation. The low percentages of male recruits from the Southern Celtic Sea and Bay of Biscay can most probably be explained by the selectivity of the gear used. There is a pronounced seasonality in female recruits in the samples from Southern Celtic Sea and Bay of Biscay and in those from the Portuguese waters, over the entire sampling period: most of the recruits appear in autumn and winter. In the samples from the Greek Seas female recruits may remain in high percentages during the autumn, winter and spring. It is not surprising, however, that the pronounced seasonality in recruits appears in the edges of the Northern part of the geographical distribution of the species. The

53


difference in size at full recruitment between females from the Portuguese waters and those from the remainder areas may be also attributed to different gear selectivity. Continuous recruitment throughout the year has also been observed in populations of I. illecebrosus from the Newfoundland waters (Dawe and Beck, 1997) while in populations of T. eblanae, recruitment occurs from winter to summer in the Scottish waters (Hastie et al., 1994) and from autumn to spring in the Galician waters (González et al., 1994). Results of this study as well as those from the literature (e.g., MangoldWirz, 1963; Jereb and Ragonese, 1995; González and Guerra, 1996; Sánchez et

al., 1998) point to some maturation features, commonly shared in all areas studied: (1) wide size range of mature animals; (2) males appear to mature at smaller size than females; (3) lack of spent (maturity stage VI) males; (4) extended spawning period covering the whole year with greater reproductive activity during particular seasons, depending on the studied area, but usually spring and summer. From the above maturation features (1), (2) and (4) are also commonly occurring in the studied populations of I. argentinus, I. illecebrosus and T. eblanae (e.g., O’Dor, 1983; Rodhouse and Hatfield, 1990; Laptikhovsky and Nigmatullin, 1993; Arkhipkin and Laptikhovsky, 1994; Hastie et al., 1994). Extended spawning throughout the year (point (4)) has been interpreted as an adaptation, which is critical for the survival of the populations of I. illecebrosus since it ensures the interaction of migratory and non-migratory life history strategies (Coelho et al., 1994b). Absence of spent animals (point (3)) has been reported from populations of I. illecebrosus from the Canadian Atlantic waters (O’Dor, 1983) and T. eblanae from Scottish waters (Hastie et al., 1994). Conversely, spent females have been recorded from I. argentinus populations (Laptikhovsky and Nigmatullin, 1993). The most plausible explanation for the absence of spent males is that they continue to produce spermatophores until death (Jereb and Ragonese, 1995). Low percentages of maturing animals suggest the very fast transition from the immature to the mature stage according to González and Guerra (1996). Although a certain degree of bias caused by the different seasonal sampling in the studied areas is expected, high percentages of maturing and mature animals show similar seasonal pattern in the female samples from the Southern Celtic Sea and Bay of Biscay and from the Portuguese waters, while no single pattern was found over

54


the entire sampling season in the female samples from the Greek Seas. Females from the Greek Seas show a more flexible spawning peak activity, potentially subjected to the influence of the environmental variables. The latter is further strengthened by the correlations between spawning and environmental variables. Variability in spawning peaks has also been documented for the species T.

eblanae in which mature animals are abundantly occurring during summer and autumn in the Scottish waters (Hastie et al., 1994), during winter and spring in Galician waters (González et al., 1994) and during autumn in the Mediterranean (Mangold-Wirz, 1963). In I. argentinus, spawning peaks have been consistently reported during winter (Laptikhovsky and Nigmatullin, 1993; Arkhipkin and Laptikhovsky, 1994), while in I. illecebrosus populations from the Canadian Atlantic waters major spawning peaks are occurring during winter and summer and minor spawning peaks during spring. In the latter species, the resulting overlap-spawning season has been interpreted as critical for the maintenance of the population as it ensures the gene flow between summer and winter breeding components. The use of Gonado-Somatic index (GSI) for the determination of the spawning period was found to be much more efficient for females than for males. This is probably caused by the fact that females spent much more energy for their reproductive output than males. In the Tyrrhennian Sea for example, as much as 16% of the total BW was invested in female gonads and accessory organs while in males this investment was almost threefold lower (Belcari, 1996). Taking into account the L50 values for both sexes calculated from this study and the corresponding ones from the literature (González and Guerra, 1996; Jereb and Ragonese, 1995), a west-east gradient of decreasing values, in I.

coindetii populations from the Atlantic to the Eastern Mediterranean, appears: higher L50 values were calculated for populations from the most distal areas in the Atlantic: Southern Celtic Sea and Bay of Biscay and Northwestern Africa; intermediate values from the Atlantic areas proximal to the Mediterranean: Portuguese waters and Galician waters; lower values from the Mediterranean: Sicilian Channel and Greek Seas. Geographical north-south gradient in decreasing L50 values has been reported for the species I. illecebrosus studied in the Canadian Atlantic waters (Coelho and O’Dor, 1993). In the latter study, the L50

55


values varied markedly from year to year. The potential of two mode sizes at maturity in females has never been reported for I. coindetii although a narrow inflexion appears in the data presented by González and Guerra (1996) from Galician waters. However, in European waters, two clear size modes at maturity have been observed for both males and females of the loliginid species Loligo

forbesi from Scottish and Spanish waters (Boyle et al., 1995; Guerra and Rocha, 1994). These findings have been interpreted as indicative of either two different growth cohorts at breeding or mixing of two populations from different centers of origin (Boyle et al., 1995). In the present study, the existence of one or potentially two (Greek Seas) mode sizes at maturity may suggest two reproductive strategies of the species along the Atlantic and the Mediterranean. Female and male numbers were not significantly different over the entire sampling period. However, this is not the case when sex ratio is calculated over trimester and monthly intervals. Significant monthly deviations of sex ratio from 1:1 do not follow any repetitive pattern over the samples taken from the three areas. Therefore, all of the deviations, which occurred, could be attributed only to sampling error and/or occasional variations in population structure as suggested by Sánchez et al. (1998) for I. coindetii and by Moreno et al. (1994) for the loliginid squids L. forbesi and L. vulgaris. Sex ratios close to 1:1 have also been reported from the Sicilian Channel (Jereb and Ragonese, 1995), Catalonian Sea and Western Africa (Sánchez et al., 1998), while significant deviations in sex ratio were recorded only from the Galician waters (González and Guerra, 1996) and the Ionian Sea (Tursi and D’Onghia, 1992). Sex ratio calculated from populations of T.

eblanae from the European waters was close to 1:1. However, in populations of I. illecebrosus from the Canadian Atlantic waters sex ratio appeared either to be close to 1:1 for long periods of the year (Amaratunga, 1978; Lange and Sissenwine, 1983) or to vary significantly from one population to another (O’Dor, 1983). Two main conclusions may be derived from the results of the correlation of the environmental variables with the biological indices of the species: (1) both temperature and food availability, which were represented only by SST values and Chl-a in surface water during this study, are important factors in the cephalopod life-cycle. The significance of temperature and food availability for the growth rate,

56


spawning season, reproductive peaks, maturation rates, recruitment, and other biological characteristics not only for this species but also for its congeners have been pointed out by various authors (e.g., Forsythe and van Heukelem, 1987; Mangold, 1987; Dawe, 1988; Nigmatullin, 1989; Coelho and O’Dor, 1993; Forsythe, 1993); (2) different correlation patterns in the areas sampled also suggest high levels of environmentally driven flexibility of the life cycle of the I.

coindetii (e.g., Forsythe and van Heukelem, 1987; González et al., 1994). Large variations in landings (e.g., Sánchez et al., 1998) could be also attributed to the previously-mentioned flexibility of the species. Further detailed studies of the lifehistory, and particularly the influence of oceanographic variables, are required before sustainable management can be undertaken.

57


58

Chapter 3 – Biological variation in Octopus vulgaris _____________________________________________________________________________________________________________

Chapter 3. Biological variation of Octopus vulgaris in the northwest and southern Portuguese waters

3.1. Introduction The common octopus, Octopus vulgaris Cuvier 1797, is one of the most commercially important cephalopods worldwide. In Portugal it is also one of the most important fisheries resources (~6% of marine fisheries), with average landings of 8500 tonnes per year (1986 - 2007), representing the most important species in first sale value (2006). The exploitation of octopus in Portugal increased 50% in the last 20 years. It is captured mainly with traps (~95%), thus having a major social and economic importance in the Portuguese artisanal fishery, namely on the southern region (Algarve), where it accounts for more than 20% of the fishery income (DGPA, 2007). The biology of O. vulgaris has been the subject of many studies in the last decades in the Mediterranean (e.g. Mangold-Wirz, 1963; Quetglas et al., 1998), the central eastern Atlantic (e.g. Hatanaka, 1979; Hernández-García et al., 2002), and more recently in the NE Atlantic (Silva et al., 2002; Rodríguez-Rúa et al., 2005; Otero et al., 2007). Despite its high economic value in Portugal little has been published on the biology of this species on Portuguese continental waters (e.g. Carvalho and Sousa-Reis, 2003). The little research investment on octopus has been proportional to its little importance on the whole NE Atlantic European context and not to its major importance to Spain and Portugal.

O. vulgaris has a short life cycle of 12-14 months (Domain et al., 2002; Iglesias et al., 2004) and terminal spawning with egg care by the female. The incubation of eggs lasts from 36 days at 23ºC, 60 days at 21ºC, 80 days at 17ºC, and 120 days at 13ºC (Mangold and Boletzky, 1973; Caverivière et al., 1999; Martins, 2003). Paralarvae are planktonic for one to three months, depending on the effect of temperature on growth rates to reach the critical size for settlement (> 7.5 mm ML) to the benthic life mode of the adults (Villanueva et al., 1995). The mortality on the paralarvae phase is sough to be very high and dependent on

59


environmental

conditions,

inducing

high

variability

on

the

recruitment

success/biomass (Faure, 2002). The growth is very rapid with extreme individual variation in growth rates, observed in culture experiments (Iglesias et al., 2004) and in wild populations (Domain et al., 2000). O. vulgaris like other cephalopods is ecologically opportunistic capable of a high labile life history well correlated with the local environment dynamics. The aim of this work is to compare the main biological parameters, the timing of recruitment, and the timing of spawning between the populations of the northwest coast and south coast of Portugal, i.e. within the Iberian coastal upwelling ecosystem vs. within the Gulf of Cádiz ecosystem. Life cycle strategies are discussed in relation to the different environmental conditions between those areas.

3.2. Material and Methods 3.2.1. Biological Sampling Biological data on O. vulgaris was obtained from fishery sampling in two areas of the Portuguese coast: the northwest coast (NWT) grouping catches at latitudes 38.5 ºN to 41 ºN and the southern coast (STH) grouping catches at longitudes 7 to 8 ºW. Monthly samples of ~30 specimens from NWT were obtained from the trap fishery landings in Peniche or other neighbour ports, between February 1997 and January 2008. Samples from STH were obtained monthly from the trap artisanal fishery landings in Sta Luzia, between November 2000 and November 2001 and landings in Olhão, between December 2006 and January 2008. Additional samples, taken between October 1996 and October 2007 on both geographical areas, were gathered from several bottom trawl survey cruises on board IPIMAR research vessels. NWT cruise samples cover latitudes between 38.5 ºN and 42ºN and STH cruise samples cover longitudes between 7 and 9 ºW (Fig. 3.1). A total of 5049 and 2120 octopus were sampled respectively from NWT and STH areas. The number of specimens sampled per month and area are summarized in table 3.1.

60


50 ºN

40

NWT P

Portugal

45

O

SHT Gulf of Cádiz

35

15

10

5º W

0

Figure 3.1. Sampling area on the northwest coast (NWT) grouping catches at latitudes 38.5 ºN to 42 ºN and sampling area on the southern coast (STH) grouping catches at longitudes 7 to 9 ºW. Location of landing ports Peniche (P) and Olhão/Sta Luzia (O).

In each specimen dorsal mantle length (ML) and body weight (BW) were measured, and sex, maturity stage determined. Maturity stage was assessed following a maturity scale adapted from Gonçalves (1993) and updated with new observations. The macroscopic maturity scale has five stages for females (immature, maturing, pre-spawning, spawning, post-spawning) and four stages for males (immature, maturing, mature, spent) (Table 3.2). In specimens collected from fishery, other biological parameters were measured, such as the ovary weight (OW), testis weight (TW) and Needham complex weight (NCW).

61


Table 3.1. Number of octopus specimens sampled by month from fishery and survey cruises from the northwest coast (NWT) and south Portuguese coast (STH). sampling fishery samples month NWT STH Out-96 Nov-96 Dez-96 Jan-97 Fev-97 Mar-97 Abr-97 Mai-97 Jun-97 Jul-97 Ago-97 Set-97 Out-97 Nov-97 Dez-97 Jan-98 Fev-98 Mar-98 Abr-98 Mai-98 Jun-98 Jul-98 Ago-98 Set-98 Out-98 Nov-98 Dez-98 Jan-99 Fev-99 Mar-99 Abr-99 Mai-99 Jun-99 Jul-99 Ago-99 Set-99 Out-99 Nov-99 Dez-99 Jan-00 Fev-00 Mar-00 Abr-00 Mai-00 Jun-00

14 39 59 42 16 53 33 45 50 36 32 17 31 30 28 36 48 43 45 43 39 69 24 24 30 35 34 45 45 43 30 40 30 24 45 31 45 46 34 32 63

Jul-00

34

survey samples NWT STH 162 104 36

46

35 50 43 29 21 36 26 30 30 25 42 45 50 101 42 42 20

55 10

Mai-04

23

47 121

4 11

1

1

2 1

2 1

2

29

19

46

6

5 20

fishery samples NWT STH

Ago-00 Set-00 Out-00 Nov-00 Dez-00 Jan-01 Fev-01 Mar-01 Abr-01 Mai-01 Jun-01 Jul-01 Ago-01 Set-01 Out-01 Nov-01 Dez-01 Jan-02 Fev-02 Mar-02 Abr-02 Mai-02 Jun-02 Jul-02 Ago-02 Set-02 Out-02 Nov-02 Dez-02 Jan-03 Fev-03 Mar-03 Abr-03 Mai-03 Jun-03 Jul-03 Ago-03 Set-03 Out-03 Nov-03 Dez-03 Jan-04 Fev-04 Mar-04 Jan-00

9

4 2

Sampling Month

38

survey samples NWT STH 11 2

11

38 43 21 25 22 44 73 8 54

54

18 29 31 21 36 20 32 41 30 23 23

3 8 2

24

23

9 5 21 1

21 24 44 26 25 34 31 31 32 33 18 27 24 30 6

45

120 31 6

62

30

sampling month Jun-04 Jul-04 Ago-04 Set-04 Out-04 Nov-04 Dez-04 Jan-05 Fev-05 Mar-05 Abr-05 Mai-05 Jun-05 Jul-05 Ago-05 Set-05 Out-05 Nov-05 Dez-05 Jan-06 Fev-06 Mar-06 Abr-06 Mai-06 Jun-06 Jul-06 Ago-06 Set-06 Out-06 Nov-06 Dez-06 Jan-07 Fev-07 Mar-07 Abr-07 Mai-07 Jun-07 Jul-07 Ago-07 Set-07 Out-07 Nov-07 Dez-07 Jan-08 total

fishery samples NWT STH 26 24 26 36 25 30 20 24 24 23 24 25 30 34 23 28 31 27 20 8 36 23 26 24 30 25 36 34 40 27 19 23 30 27 31 82 27 17 31 32 22 35 4168

survey samples NWST STH 10

76 49

52

32 250 7 34 124 50

2 1

10

11 26 2

15 163 19 15

5 4 42 41 28 0 50 10

70 22

49

35 14 19 32 36

1 1

1

74 620

881

1400


3.2.2. Data analysis Mean ML and BW were estimated for males and females of each area. Effects of sex and season on ML and BW were assessed by factorial ANOVA. Monthly frequency of body weight classes was estimated grouping specimens sampled from the fishery into commercial classes: T1 ≥ 3 kg, 3 kg > T2 ≥ 2 kg, 2 kg > T3 ≥ 1 kg, T4 < 1 kg. Samples sizes were first standardised between months to 100 specimens by sampled month.

Table 3.2. Macroscopic maturity scale for O. vulgaris. Females maturity stage

ovary

oviducal gland

I

immature

white, small, homogeneous tissue

white, small, varying from homogeneous tissue to the

II

maturing

white, medium size, homogeneous tissue

Small to medium size, varying from a small proximal white

detection of a small proximal white denticulate band denticulate band and distal portion white to three areas well differentiated ( white denticulate band, brown band and ivory stripped band) III pre-spawning

creamy to yellow, big size (~1/3 mantle),

larger size, proximal white denticulate band larger followed

some hyaline eggs

by a brown band, (stripped) ivory band on distal side

IV spawning

yellowish, very big, all hyaline eggs,

maximum size, proximal white denticulate band followed by a

some easily detached

brown band reaching almost half gland, (stripped) yellowish band on distal part.

V post-spawning

smaller size, part of the tissue is

smaller size, thee regions less distinct, distal half brownish

brownish and without eggs Males maturity stage

testis

Needham sac

Gonoduct

I

immature

transparent white

absence of spermatophores with sperm

transparent

II

maturing

white

few spermatophores, mostly empty

white, thin

III mature

ivory

many spermatophores full of sperm

ivory, thick

IV senile

brownish, reduced size

few spermatophores

Ivory

Length-weight relationships were fitted for males and females for each area. The parameters of the power model were estimated with 95% confidence and slopes compared between sexes within each area, by ANCOVA. The minimum size and weight at maturity was defined as the ML and BW of the smallest octopus in maturity stage III. The frequency of maturity stages by

63


BW class and ML class was assessed for each area. Maturity curves were fitted for each area, as described for squid in chapters 1 and 2. The weight at which 50% of males or females are found mature, was derived as the ratio of the parameters of the linear model (BW50 = a/b), when a significant fit was obtained (least squares regression, p < 0.05). The gonadosomatic indices (GSI) were calculated for males (GSIM) and females (GSIF) as GSI=(GW/(BW-GW))x100, where GW of males is testis plus spermatophoric complex weight and GW of females is the ovary weight. The recruitment season in each area was determined by a Recruitment Index RI=Rm/R (computed for standardised sample sizes), for fishery data. Rm = number of recruits observed in month m, R = ∑ R m (all the recruits observed in each sampling period). The computation of the RI assumes that recruits are animals with BW ≤ T. The species threshold T was defined as the modal BW of the body weight frequency distribution, computed pulling together all animals sampled from the fishery in both geographical areas. The recruitment seasonality (RI grouped by trimester) was compared between areas by factorial ANOVA. The spawning season was determined by evaluating the monthly proportion of maturity stages in each sex, the mean frequency of mature females and females mean GSI by month. Data from fisheries and cruise sampling was pulled together for the spawning season analysis, because exploratory analysis of spawning patterns with and without cruise data was similar. The spawning seasonality (grouped by trimester) was compared between areas by factorial ANOVA.

3.3. Results 3.3.1. Size and weight Mean and maximum ML and BW of males and females on the NWT and SHT observed in fisheries and cruise sampling are displayed in Table 3.3. The samples from cruises present lower mean sizes and weights, obviously because of

64


the presence of high percentage of pre-recruits to the fishery. Both fishery and cruise sampling show higher mean ML and higher mean BW on the SHT area (Table 3.3), but differences are not significant (P > 0.05). Mean size and weight by trimester and sex for both areas is displayed in figure 3.2, coupling both fisheries and cruise data. On the northwest area there is a significant effect of trimester independently of sex on mean size and weight (F(3,5043) = 77.72, p < 0.001 and F(3,5043) = 59.39, p < 0.001, respectively). Post hoc Scheffé tests indicate that mean ML and BW are significantly lower in summer and autumn and significantly higher in winter and spring in this area.

Table 3.3. Mean and maximum mantle length (ML) and body weight (BW) of males and females on the northwest (NWT) and south (SHT) Portugal. area

fisheries

size and weight

cruise

fisheries

males

NWT

SHT

ML max

250

210

275

205

ML mean±sd

154 ± 25

99 ± 32

158 ± 29

101 ± 35

BW max

6120

5118

6050

4022

BW mean±sd

1376 ± 753

636 ± 628

1400 ± 741

658 ± 625

ML max

235

235

270

230

ML mean±sd

159 ± 27

107 ± 30

159 ± 29

108 ± 31

BW max

4800

6100

4850

4470

BW mean±sd

1671 ± 812

713 ± 600

1652 ± 795

739 ± 623

1800

170

1800

BW ML

170

160

1600

160

1400

150

1400

150

1200

140

1200

140

1000

130

1000

130

800

120

800

120

110

600

600

(a)

win

spr

sum

aut

win

males

spr

sum

BW (g)

1600

aut

(b)

females

ML (mm)

BW ML

ML (mm)

BW (g)

cruise females

110 win

spr

sum

aut

win

males

spr

sum

aut

females trimester

trimester

Figure 3.2. Seasonal mean (± standard error) body weight (BW) and size (ML) of O. vulgaris males and females, from fisheries and research cruises on northwest, NWT (a) and southern Portugal, SHT (b).

65


On the other hand, in spite of the effect of trimester being also significant on the southern area (F(3,2066) = 32.44, p < 0.001 and F(3,2066) = 28.98, p < 0.001, respectively), the pattern is distinct from NWT. The mean ML and BW on SHT is significantly lower in winter and significantly higher in summer, with no significant differences between spring and autumn (Post hoc tests). The monthly frequency of body weight classes of octopus from the trap fishery shows the geographic differences (Fig. 3.3). On the northwest area, small octopus appear in fisheries in higher proportions from June to December. On the south, high proportions of small octopus appear in fisheries from August until April of the next year. The proportion of big octopus (T1) is more similar between areas, higher during winter and spring.

SHT

1.0

1.0

0.8

0.8

0.6

0.6

Freq.

Freq.

NWT

0.4

T1 T2 T3 T4

0.4 0.2

0.2

0.0

0.0 1

2

3

4

5

6

7

8

9

1

10 11 12

2

3

4

5

6

7

8

9

10 11 12

Month

Month

Figure 3.3 – Monthly frequency of body weight classes (T1 ≥ 3 kg, 3 kg > T2 ≥ 2 kg, 2 kg > T3 ≥ 1 kg, T4 < 1 kg) of O. vulgaris from the trap fishery on northwest, NWT (a) and southern Portugal, SHT (b), during November 2000 to November 2001 and December 2006 to January 2008 sampling periods.

3.3.2. Length-weight relationship O. vulgaris have negatively allometric growth as, in general, in the other cephalopod species analysed (Fig. 3.4). On the northwest there is a significant difference between sexes in the length-weight relationship slope (P < 0.01). Males become significantly heavier with length than females. This sexual difference is not significant on the south area (P > 0.05).

66


The length-weight relationship slope was also statistically compared between areas showing that octopus on the SHT become significantly heavier with length than octopus on the NWT (P < 0.001). Paired within sex tests, demonstrate that these differences are significant also between males or females of both areas (P < 0.001).

BW (g)

BW (g)

3000

3000

2000

2000

1000

1000

1000

0

0

(a)

100

200

300

ML (mm)

(b)

SHT BW = 0.004.ML2.53(±0.02) r2=0.93, n=2056

4000

2000

0

NWT BW = 0.013.ML2.28(±0.01) r2=0.86, n=5020

5000

F BW = 0.005.ML2.51(±0.02) r2=0.93, n=1025

4000

3000

6000

M BW = 0.004.ML2.55(±0.02) r2=0.92, n=1031

5000

F BW = 0.016.ML2.24(±0.02) r2=0.87, n=2459

4000 BW (g)

6000

M BW = 0.011.ML2.32(±0.02) r2=0.86, n=2561

5000

NWT vs. SHT

SHT

NWT 6000

0

0

100

200 ML (mm)

300

(c)

0

100

200

300

ML (mm)

Figure 3.4. Length-weight relationships for males (thick line) and females (thin line) of O. vulgaris on northwest Portugal, NWT (a) and south Portugal, SHT (b). Length-weight relationships for both sexes combined on NWT (thick line) and SHT (thin line) (c).

3.3.3. Size and maturation The frequency of maturity stages by BW or ML class indicates that gonad maturation may start at very different sizes and probably ages. We may find very small mature specimens as well as very large completely immature ones, namely females (Figs. 3.5 and 3.6). Females attain maturity generally at a larger size than males. The smallest mature female was 577 g and the smallest mature male was 152 g. The commercial category T4, which groups all the recruits, includes more than 90% of immature and/or maturing animals. However, the commercial category T1, which groups the larger animals, contains also many maturing females (> 50% on SHT). In fact, there are differences in size at maturity between areas in both sexes, with the maturation process beginning at lower sizes on the NWT population. Within each area the mean weight at maturity presents also seasonal variation (Fig. 3.7).

67

Ana Moreno 2008 – Cephalopod Life History Traits _____________________________________________________________________________________________________________ females

males

1

1

freq. maturity stages

5 4

0.6

3 2 1

0.4 0.2

0.8 4

0.6

3 2

0.4

1

0.2

0

0 T4

T3

T2

T1

T4

T3

BW class (g)

T1

1

2 1

250

230

50

250

230

210

190

170

150

130

0

110

0 90

0.2

70

0.2

50

3

0.4

210

2 1

190

3 0.4

4

0.6

170

4

130

0.6

0.8

90

5

110


0.8

70

1


T2

BW class (g)

150


0.8

ML class (g)

ML class (mm)

Figure 3.5. Frequency of maturity stages by body weight class (BW) and size class (ML) of females and males on the northwest Portugal (NWT). BW classes grouped into commercial categories.

females

males 1

0.8 5 4

0.6

3 2 1

0.4


0.2

0.8 4

0.6

3 2

0.4

1

0.2 0

0 T4

T3

T2

T4

T1

T3

T1

1

0.8 5 4 3 2 1

0.6 0.4 0.2


1

0

0.8 4 3 2 1

0.6 0.4 0.2

ML class (mm)

230

210

190

170

150

110

90

70

50

230

210

190

170

150

130

110

90

70

0

50


T2

BW class (g)

BW class (g)

130


1

ML class (g)

Figure 3.6. Frequency of maturity stages by body weight class (BW) and size class (ML) of females and males on south Portugal (SHT). BW classes grouped into commercial categories.

68


SHT

2800

2800

2400

2400 BW (g)

BW (g)

NWT

2000 1600

2000 1600

1200

1200 win

spr

sum trimester

aut

win

spr

sum trimester

aut

Figure 3.7. Mean size at maturity of females estimated by trimester on the NWT and SHT areas. Vertical bars denote standard error.

The mean size at maturity was lower during summer on the NWT area and during autumn on the SHT area. The BW50 was 2520 g for females and 1450 g for males in the northwest and 2890 g for females and 1750 g for males in the southern area (Fig. 3.8). Due to the large range for the size at maturity, GSI presents also large ranges for each maturity stage, namely for pre-spawning and spawning females and maturing and mature males (Fig. 3.9). No significant differences were found in mean GSI in females by maturity stage between areas (ANOVA, area effect: F(1, 2203) = 0.49, p > 0.05). SHT

NWT 1

freq. mature

freq. mature

1

0.5

0.5

BW50F=2.52 kg BW50F=2.89 kg BW50M=1.45 kg

BW50M=1.75 kg

0

0

0

0.75

1.5

2.25

3

3.75

4.5

5.25

6

0

BW class (kg)

0.75

1.5

2.25

3

3.75

4.5

5.25

6

BW class (kg)

Figure 3.8. Maturity ogives for males (dots) and females (open circles) on the northwest Portugal (NHT) and south (SHT) Portugal.

69


NWT males

24

4

18

3 GSI

GSI

females

12 6

2 1

0

0

1

2

3

4

5

1

Maturity stage

2

3

4

Maturity stage

4

18

3 GSI

GSI

SHT 24

12 6

2 1

0

0

1

2

3

4

5

1

2

3

4

Maturity stage

Maturity stage

Figure 3.9. Gonadosomatic indices (GSI) by maturity stage of females and males on northwest Portugal (NWT) and of females and males on south Portugal (SHT). Vertical bars denote GSI range.

3.3.4. Recruitment season All specimens ≤ 1000 g are considered recruits to the trap fishery. The modal body weight class is the 750 g BW class (750 to 1000 g), which corresponds to the modal size class of 140 mm ML (Fig. 3.10). Recruits appear in trap fisheries throughout the year on both areas (Fig. 3.11). However, each geographic area show significantly distinct recruitment seasonality (ANOVA, area x trimester effect: F(3, 37) = 3.15, p < 0.05). Recruitment on the NWT shows an extended season from June until December, despite the evidence of two peaks, one in late summer (September) and another in late autumn (December). On the other hand, two marked recruitment seasons are present on the SHT. The most important season beginning in August and lasting until January of the next year, with a maximum RI in November. A

70


secondary recruitment season starts in March and ends in June, with a maximum RI in April.

0.25

0.20 0.15

0.15

Freq.

Freq.

0.20

0.10

0.10 0.05

0.05 0.00

0.00 100

500

1000

1500

2000

2500

3000

3500

4000

60

BW class (g)

80

100

120

140

160

180

200

220

240

260

ML class (mm)

Figure 3.10. Overall length frequency and body weight frequency of O. vulgaris from trap fisheries.

0.4

NWT SHT

0.3

Figure 3.11. Monthly recruitment indices (RI) periods Nov. 2000 to Nov. 2001 and Dec.

RI

on NWT and SHT areas for the sampling

0.2

0.1

2006 to Jan. 2008. Vertical bars denote monthly standard error.

0.0 Jan Feb Mar Apr May Jun

Jul Aug Sep Oct Nov Dec

month

3.3.5. Spawning season Spawning females are present throughout the year on the northwest area and from March until December on the southern area (Fig. 3.12). Pre-spawning and spawning females were caught always in low proportions. Mature males, on the other hand, appear in samples in high proportions throughout the year on both areas, with maximum values between February and May on the northwest and in July and August on the south. Immature females (stage 1) and maturing males (stage 2) are present throughout the year on both areas. Higher proportions occur

71


between August and December on the northwest and between October and March on the south. Post-spawning females were very rare and occurred only between September and January on NWT and between September and November on the SHT.

NWT males

1

1

0.8

0.8

5

0.6

4 0.4

freq.

freq.

NWT females

3

3

0.4

2

2

0.2

4

0.6

0.2 1

1 0

0

J

F M A M J

J

A

S O N D

J

J

A S O N D

SHT males

1

1

0.8

0.8

5

0.6

4 0.4

freq.

freq.

SHT females

F M A M J

3

3

0.4

2

2

0.2

4

0.6

0.2 1

1 0

0

J

F M A M J

J

A

S O N D

J

F M A M J

J

A S O N D

Figure 3.12. Monthly proportion of maturity stages of females and males on NWT and SHT areas.

The frequency of mature females on standardised monthly samples highlights the main differences concerning the spawning season between the NWT and SHT (Fig. 3.13). The population on the NWT show a winter/early spring spawning season not matched on the SHT, where the spawning activity remains low. On the other hand, the summer spawning season with higher proportions of mature females in July and August, decreasing abruptly on September, is more similar between geographic areas. Nevertheless, the spawning activity seems to be extended through autumn months only on the SHT. The seasonal differences between areas are statistically significant (ANOVA, area x trimester effect: F(3,

72


152) = 5.08, p < 0.01). The gonadosomatic indices (GSI) of females computed by trimester put also in evidence the geographic differences related to the spawning activity (Fig. 3.14).

SHT

0.4

0.4 freq. mature

0.5

0.3 0.2 0.1

0.3 0.2 0.1

0.0

0.0

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

month

month

Figure 3.13 – Mean frequency of mature females by month on NWT and SHT areas. Vertical bars denote standard error from monthly samples.

NWT

SHT

2.0

2.0

1.6

1.6

1.2

1.2

GSI

GSI

freq. mature

NWT 0.5

0.8

0.8

0.4

0.4

0.0 win

spr

sum

aut

0.0

trimester

win

spr

sum

aut

trimester

Figure 3.14. Seasonal mean GSI for females on NWT and SHT areas. Vertical bars denote standard error.

3.4. Discussion O. vulgaris living in Portuguese waters share similar life cycle traits with the populations living in the Mediterranean, NW African waters and the neighbouring Spanish waters. Likewise for those areas, our study highlights the short life span,

73


fast growth, negatively allometric growth in weight with length, lower size at maturity of males and extended spawning and recruitment seasons (Silva et al., 2002; Otero et al., 2007; Rodríguez-Rúa et al., 2005; Faraj and Bez, 2007). Nevertheless, we detected important geographic differences between the northwest and the southern populations, as well as in relation to other geographic areas. These differences are essentially the distinct seasonal patterns and also a latitudinal trend of the biological parameters linked to growth. The differences in maximum and mean weight between the NWT and SHT were not significant. However, octopus on the SHT showed significantly higher growth in weight becoming heavier with length than octopus on the NWT, as evidenced by the differences in slopes of the length-weight relationship in each sex. This difference may be a direct effect of the higher mean temperatures of the SHT area. This conclusion is supported by the lower values estimated for octopus living in generally colder waters of NW Spain (Otero et al., 2007) and the higher values estimated for octopus living in warmer waters of the Canary Islands (Hernández-García et al., 2002) or in the Mediterranean (Guerra and Manriquez, 1980). The values estimated in the Spanish waters of the Gulf of Cádiz (Silva et

al., 2002), lower than those found for the neighbouring Portuguese waters, seem to contradict our interpretation. However, those values may not be comparable due to the influence of inter-annual differences. Size at maturity showed also marked geographic variability, as maturation in both sexes is reached at a smaller size and weight on the NWT area. Size at maturity is controlled by a combination of several endogenous and exogenous factors controlling simultaneously somatic growth and maturation rates (Mangold, 1987). Therefore, size at maturity tends to be very variable not only between geographic areas but also within each population, especially those living in fluctuating temperate environments, such as in Portuguese waters. We observed that females tend to mature at a smaller size during the periods of higher spawning activity in both areas. The absence of geographic variability in GSI by maturity stage seems to indicate the lack of significant differences in reproductive investment between areas. However, size at maturity of females was significantly higher on the SHT area, which means potentially larger reproductive output in this

74


area, knowing that number of eggs is well correlated with the size of females (Gonçalves, 1993; Silva et al., 2002; Otero et al., 2007). The seasonality of reproduction and recruitment were the main differences found between the octopus populations living on the NWT and the SHT areas and this seems to be closely related with the oceanographic regimes of the western Iberia upwelling ecosystem and the Gulf of Cádiz ecosystem, where they are respectively located. On the NWT recruits start to appear in April in fisheries but in higher proportions in September and December, decreasing thereafter. The proportion of recruits is therefore low during winter and spring when large octopus dominates the catches (see figure 3.2). The late summer recruits, which are animals between 750 and 1000 g and ~6-7 months old (Domain et al., 2000), will mate and spawn mainly during the next winter. The late autumn recruits grow more slowly through winter and originate the spawning peak of the next summer. The extended recruitment season and the individual variability in growth, enables part of the population to spawn already during the next spring. As a consequence, the spawning season in the NWT area is quite extended through winter and summer. Some of the early recruits (April/May) will mature and grow fast during late spring and summer. These animals will be able to mate and spawn by the end of summer and contribute to increase the spawning activity and decrease the size at maturity in July and August. Two spawning peaks, with more than five months apart, were already reported in Marrocan waters (Faraj and Bez, 2007) and the Canary Islands (Hernández-García et al., 2002), although in those areas the peaks generally occur later (spring and autumn). On the other hand, a single spawning peak in late winter or spring was observed on the NW Spain by Fernández-Rueda and GarcíaFlórez (2007) and Otero et al. (2007), respectively. Two seasons of recruitment were detected on the SHT. The octopus recruited from March until May contribute for the single spawning peak in summer. The recruits from the main season appear from August until January with a maximum in November. If these recruits are ~6-7 month old, their females would be ready to spawn in late winter and spring. However, we observed that the spawning activity during that period is rather low. As we do not really know the age of these recruits we may hypothesise two explanations for this apparent mismatch

75


in recruitment and subsequent spawning seasons: (1) an early spawning peak exists but is not detected in our data because mature females migrate for spawning in locations outside the fisheries and cruise sampling range; (2) the late summer and autumn recruitment season are made of octopus hatched during late spring/early summer, which grow very fast under the high water temperature of summer/early autumn and recruit to the fishery, in higher numbers in November, as early as four months old. The females would spawn during next summer contributing for the observed single spawning peak in July/August, i.e. octopus from both recruitment seasons will spawn one year apart. Despite there is one argument in favour of the first hypothesis, which is the April and August spawning peaks detected by Silva et al. (2002) on the neighbouring Spanish waters, we find our second hypothesis more plausible. In Silva et al. (2002) only 1996 samples were analysed, which was a year of extraordinary high abundance, when seasonal patterns tend to be altered. Furthermore, the existence of two spawning peaks in the northern Gulf of Cádiz is not supported by Rodríguez-Rúa et al. (2005), who described a single summer peak similar to our data. A single summer spawning peak is also the pattern described for O. vulgaris in the western Mediterranean (Mangold, 1983b; Sanchez and Obarti, 1993). The differences in seasonal patterns observed between the NWT and SHT, as well as the different patterns observed in other areas of the Atlantic and Mediterranean reinforce the theory of a life cycle strategy tightly linked to the seasonal dynamics of the major local oceanographic regimes, as already suggested by Otero et al. (2007). He observed that the population living in Galician waters, subject to the influence of strongly seasonal coastal upwelling, shows a single spawning peak in April allowing the peak hatching of the planktonic paralarvae to be after the most advective summer months. Just a short distance south, O. vulgaris living on the northwestern Portuguese waters, also subject to the influence of coastal upwelling but within a highly retentive area (e.g. Relvas et

al., 2007), show two spawning peaks producing hatching in summer when zooplankton abundance is maximum and in autumn when zooplankton levels are still high and the water temperature over the shelf increased rapidly as a consequence of the end of the upwelling season. This emphasises the fact that within the same coastal upwelling region, different areas may exist where the

76


oceanography dynamics are specific and dependent on local aspects (Santos et

al., 2004). An extended spawning and an extended hatching season (throughout the year in the limit) is a life cycle strategy that enhances cephalopod great resilience to environmental change (Boyle and Boletzsky, 1996). We observed that

O. vulgaris, in the absence of limiting environmental factors, adjusts its reproductive season in order that prey availability and warmer temperature could maximize growth rates of paralarvae and juveniles and consequently increase recruitment success. These issues will be discussed further below under chapter 5.

77


78

Part 2 – Cephalopod early life stages: description and distribution patterns


_____________________________________________________________________________________________________________

3

Chapter 4 – Paralarvae description _____________________________________________________________________________________________________________

Chapter 4. Identification of cephalopod paralarvae from Portuguese and adjacent waters An identification key was developed to illustrate the early life stages found within the Portuguese and surrounding Spanish waters, because the early life stages of many species are virtually unknown, which makes the taxonomic investigation of cephalopods captured by plankton nets very difficult (Diekman et

al. 2002). The key was based on available information spread from several sources, namely Okutani and McGowan (1969), Young (1991), Hanlon et al. (1992), Hochberg et al. (1992), Sweeney et al. (1992), Voss et al. (1992), Wormuth et al. (1992), Young et al. (1992), Yau (1994), Bello (1995), Vechione et

al. (2001), Diekmann et al. (2002), Gowland et al. (2003). Illustrations and some original new descriptions of species are provided, as well of eggs and/or egg masses, where available. The key was subsequently used as an essential tool to describe distribution patterns (chapter 5).

4.1. Checklist of species Class Cephalopoda Subclass Coleoidea Order Sepiolida Family Sepiolidae Subfamily Heteroteuthinae

Heteroteuthis dispar (Rüppel, 1844) Subfamily Rossinae Rossia sp. Owen, 1834 Subfamily Sepiolinae Order Teuthida Suborder Myopsina Family Loliginidae Loligo vulgaris Lamarck, 1798 Loligo forbesii Steenstrup, 1856 Alloteuthis sp. Wülker, 1920 Suborder Oegopsina Family Ancistrocheiridae Ancistrocheirus lesueuri (Orbigny, 1842) Family Brachioteuthidae

81


Brachioteuthis riisei (Steenstrup, 1882)

Family Chiroteuthidae

Chiroteuthis sp. Orbigny, 1841

Family Chtenopterygidae

Chtenopteryx sicula (Verany, 1851)

Family Cranchiidae Subfamily Cranchiinae

Leachia atlantica (Degner, 1925)

Subfamily Taoninae

Bathothauma lyromma Chun, 1906 Helicocranchia pfefferi Massy, 1907 Liguriela podophthalma Issel, 1908 Taonius pavo (Lesueur, 1821) Teuthowenia megalops (Prosch, 1847)

Family Enoploteuthidae

Abralia veranyi (Rüppell, 1844) Abraliopsis pfefferi Joubin, 1896

Family Mastigoteuthidae

Mastigoteuthis sp. Verrill, 1881

Family Ommastrephidae Family Onychoteuthidae

Onychoteuthis banksii (Leach, 1817)

Family Pyroteuthidae

Pterygioteuthis sp. Fischer, 1896 Pyroteuthis margaritifera (Rüppell, 1844)

Order Octopoda Suborder Incirrina Family Octopodidae Subfamily Octopodinae Octopus salutii Verany, 1839 Octopus vulgaris Cuvier, 1797 Family Ocythoidae Ocythoe tuberculata Rafinesque, 1814

4.2. Identification key to family level of early life stages of neritic and oceanic cephalopods in the Iberian Atlantic waters 1.• mantle without fins, tentacles absent - Order Octopoda………………..……………………….….13 • mantle with fins or fin rudiments, one pair of tentacles or a proboscis ………….………………. 2

82


2.• mantle with lateral fins….…………………………………………….…..…………………..Sepiolidae • mantle with sub-terminal or terminal fins, sometimes dorsally attached - Order Teuthida..……. 3 3. • eye covered by a transparent membrane (cornea), tentacular clubs with 4 rows of suckers, no external photophores – Sub-Order Myopsida ……...……...……………...……..…. Loliginidae • eye in contact with seawater (no cornea), many species with external photophores – Sub-Order Oegopsida ………...………….…………………………………………………..……………..... 4 4. • tentacles fused into trunk like structure (proboscis)…………....................……. Ommastrephidae • pair of tentacles, no proboscis ………………..…………………..…………………...…………….. 5 5. • head with long neck………………………………………………........……………….…………….. 6 • head without long neck…………………………………………………….……………………….….. 7 6. • neck with dorsal hump, arm crown not stalked, mantle without conspicuously long tail………………………………………………..……………………….………. Brachioteuthidae • neck multiple chambered and without dorsal hump, long tail with secondary fin (often missing), arm crown stalked ……………………………………………………..…..……… Chiroteuthidae 7. • body elongated with long pointed tail, tentacles greatly enlarged/ stretched, funnel locking cartilage oval with small projection (tragus)……………………………….…. Mastigoteuthidae • other features than above, if body elongated and/ or tentacles enlarged the funnel locking cartilage is permanently fused with the mantle ……………………..……………….….…….. 8 8. • funnel locking cartilage and mantle permanently fused in nuchal region………....… Cranchiidae • mantle not fused to the head …………………………………………….…….………………....…. 9 9. • fins with muscular ribs; tentacular club in small larvae spatulated………..…… Chtenopterygidae • fins without ribs ……………………………………..………………………………..………………..10 10. • mantle sharply pointed posteriorly; funnel locking-cartilage straight; head often withdrawn into mantle up to eye lenses; arm pair IV rudimentary……..……………...……. Onychoteuthidae • features other than above, photophores on mantle, arms, head and/ or eyes and intestine “Enoploteuthid” group of families ……….…………………………….………………...……. 11 11.• no light organs on eyes……………………………………….…………………… Ancistrocheiridae

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• light organs on eyes, well defined even in youngest stages ……………..…………………… 12 12. • no light organs on viscera………………………….……………………..……….. Enoploteuthidae • light organs present on viscera but absent from surface of mantle, funnel, head and arms (not considering tentacles)…………………..………………………………………..… Pyroteuthidae 13. • mantle muscular, mantle locking apparatus absent; arms equal in length and generally short and compact…………………………………….……………………………………. Octopodidae • arm pairs I and IV greatly enlarged, in youngest stages not enclosed in brachial membrane; funnel elongated………………………….……………………………………………. Ocythoidae

4.3. Description and illustration of species Order Sepiolida 4.3.1. Family Sepiolidae This family is characterised by a short, broad mantle with large, round fins. The funnel locking-cartilage is simple and straight. The shell is reduced to a chitinous gladius or completely absent. Paralarvae of the sub-families Heterotheuthinae (Heteroteuthis dispar), Rossinae (Rossia macrosoma) and Sepiolinae appeared often in Portuguese and adjacent waters. Table 4.1 show the main characteristics to distinguish between the genera Heterotheuthis (Fig. 4.1) and Rossia (Fig. 4.2 and Fig. 4.3a) and the Sub-family Sepiolinae (Fig. 4.3b and Fig. 4.4).

Table 4.1. Key to the genera Heterotheuthis and Rossia and the sub-family Sepiolinae. Characters deep web joining the first three pairs of arms fins long, extending to the posterior end of the mantle fins short, not exceeding the mantle

Heterotheuthis

Rossia

Sepiolinae

+

-

-

+

-

-

-

+

+

-

-

+

dorsal edge of mantle fused with head

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(a)

(b)

Figure 4.1. Heterotheuthis dispar – ventral view of a 10.6 mm ML paralarvae captured in January 2001 at 36.24 ºN, 6.75 ºW (a) and dorsal view of a juvenile captured in July 1993 at 36.70 ºN, 8.07ºW (b). Arrows indicate the web joining the first three pairs of arms.

(a)

(b)

(c)

Figure 4.2. Rossia macrosoma – eggs collected with a bottom trawl on the south Portuguese coast at 111 m deep, during a survey cruise in March 2007 (a and b). Pre-hatchling after incubation (c). The arrow indicate the dorsal edge of mantle which is not fused with the head.

85


(a)

(b)

Figure 4.3. Dorsal view of a 2.72 mm ML Rossia sp. captured on November 2004 at 36.87 ºN, 7.96 ºW (a). Dorsal view of a 4.25 mm ML Sepiolinae paralarvae capture on January 2002 at 40.87 ºN, 8.83 ºW (b).

(b)

(a)

Figure 4.4. Dorsal (a) and ventral view (b) of a 5.69 mm ML sepiolinae paralarvae captured on November 2004 at 36.87 ºN, 7.92 ºW.

Order Teuthida Suborder Myopsina 4.3.2. Family Loliginidae Body form of hatchlings is bullet-shape with well-developed terminal fins, well developed ventral arms (arms IV > I) and tentacles. Fins are paddle-shaped, broad with short bases, each fin much wider than long. Tentacular clubs are broad and much wider than tentacular stalks. Head squarish. Young forms of Loligo and

Alloteuthis are so similar both between and within genera that is generally impossible to distinguish species from specimens preserved for a long time in formalin (Fig 4.5). In hatchlings of all species the number of chromatophores

86


decreases from the ventral to the dorsal side. The general chromatophore pattern is highly variable within each species and very similar between them. However, each species has a characteristic chromatophore arrangement in some body parts. The chromatophore pattern of red and yellow chromatophores in Alloteuthis sp., L. vulgaris and L. forbesi is described in table 4.2.

Figure 4.5. Ventral and dorsal view of 4.5 mm ML loliginidae paralarvae, preserved in formalin, captured on January 2004 at 36.92 ºN, 8.58 ºW.

Table 4.2. Key to distinguish between loliginid paralarvae of Portuguese and adjacent waters based on the chromatophore pattern (ML < 5 mm). The most frequent pattern observed on a large sample of L. vulgaris hatchlings is highlighted in bold (L. forbesi after Hanlon et al., 1989). Number of red/yellow

L. vulgaris

L. forbesi

Alloteuthis sp.

tentacle

5 large + 4 small /4 to 6

8 large + 9 small/?

4 large + 4 small/7

arm IV

2/2

3/0

2/0

below pair of arms IV

0/1

1/0

0/1

head

10 (8 to 12)/4

14/0

10 to 14 / 6

mantle

27 (18 to 38)/15

31 to 44/?

24 to 30 / 13 to 15

each fin

0/0

0/0

1/0

below pair of arms I

0/1

1/0

1/0

arm II

0/0

1/1

0/0

arm III

1/0

2/2

0/0

head

6 (4 to 9)/3

12/8

8/0

mantle

13 (9 to 19)/2

30/18

10 to 12/12

each fin

1/0

1/1

2/1

dorsal side

ventral side

chromatophores

87


Alloteuthis sp. Hatchlings measure between 2.0 to 2.8 mm ML. They last 15 to 30 days in the plankton. Juveniles have a bullet-shaped body coming to a point at the apex, which develops into a tail in the sub-adult stage. The median rows of suckers of the tentacle club is 3–4 times larger than marginal suckers, in early juveniles. However, in hatchlings this difference in sucker size is not noticeable. Similar to L.

vulgaris, the ventral arms IV show 2 red cromatophores. On the other hand, there is a red cromatophore located between the base of the pair of arms I on the dorsal side of the head (Figs. 4.6 and 4.7).

2 mm

Figure 4.6. Dorsal and ventral view of a 2.9 mm ML Alloteuthis sp. paralarvae captured on August 1995 at 37.90 ºN, 8.95 ºW.

(a)

(b)

Figure 4.7. Dorsal view of a 6.6 mm ML Alloteuthis sp. paralarvae, captured on August 1995 at 37.90 ºN, 8.95 ºW (a) and ventral view of a 4.9 mm ML Alloteuthis sp. paralarvae captured on August 1995 at 38.37ºN, 9.00 ºW (b).

Loligo vulgaris Live hatchlings measure 2.8 to 3.9 mm ML (Turk et al., 1986; Villanueva, 2000)

88


and are smaller (mean 2.52 ± 0.24 mm) when preserved in ethanol (2.1 to 2.8 mm) or formalin (1.6 to 3.0 mm). They last ~2 months in the plankton. Mantle broad, with few large dorsal chromatophores (average red = 13 and yellow = 2) and numerous ventral chromatophores (average red = 27 and yellow = 15). The arrangement of red cromatophores on the mantle is variable, but 5 to 6 are generally located on the ventral border and only one on the dorsal mantle border. On the ventral head 10 red cromatophores are arranged in two cheek patches of four posterior to eyes and a pair between the eyes. On the dorsal head two red cromataphores are located between the eyes and two above each eye. Below the eyes yellow cromatophores are present in variable numbers and one single yellow cromatophore is located between the base of arms I. The ventral arms have with two red chromatophores and two yellow cromatophores. Tentacles have 5 red aboral chromatophores and 4 smaller red chromatophores, and 4 to 6 yellow cromatophores between those (Figs. 4.8, 4.9, 4.10, 4.11 and 4.12).

Figure 4.8. Loligo vulgaris newly hatchlings, 2.6 mm ML, preserved in ethanol 70%.

Figure 4.9. L. vulgaris one day old, 2.9 mm ML, preserved in formalin 4%. Dorsal and ventral view.

89


Figure 4.10. L. vulgaris hatchlings, 2.4 mm ML (ventral view) and 2.7 mm ML (dorsal view), preserved in ethanol and a live hatchling 2.1 mm ML (ventral view).

1 mm

0.5 mm

Figure 4.11 – L. vulgaris detail of the tentacular club of a 2.6 mm ML and a 2.7 mm ML paralarvae and a 20.6 mm ML juvenile (from left to right).

Figure 4.12. Detail of the ventral head and posterior end of the dorsal mantle and fins of a L.

vulgaris hatchling.

90


Loligo forbesi Dorsal mantle length of live hatchlings measure 3.5 to 4.9 mm (mean 3.7 mm). Mantle broad, with few large dorsal chromatophores (average red = 13 and yellow = 2) and numerous ventral chromatophores (average red = 27 and yellow = 15). The arrangement of cromatophores is similar to L. vulgaris, but in higher numbers in each body part. Similar to Alloteuthis sp. and unlike L. vulgaris, L. forbesi have a red cromatophore located between the base of the pair of arms I on the dorsal side of the head. Three cromatophores are located on each arm IV (Fig. 4.13).

Figure 4.13. L. forbesi paralarvae hatched from an egg mass captured on the Baltic Sea, detail of the ventral head.

Loliginid egg masses

Alloteuthis eggs are enclosed in gelatinous capsules. Capsules measure ~ 3-5 cm and are usually attached in clusters to hard substrate.

50 mm

Figure 4.14. Alloteuthis subulata egg mass from Scotland (photo by Cyntia Yau).

Figure 4.15. Loligo forbesi egg mass from Scotland (photo by Cyntia Yau).

91


Loligo eggs are also encapsulated in gelatinous tissue, but eggs are arranged spirally. Capsules or “fingers” are larger and thus containing a larger number of eggs. The egg “fingers” of L. forbesi measure ~7-15 cm but length varies with the development stage and the egg is oval and measure 3.5 x 4.5 mm (Yau, 1994). The egg masses of L. vulgaris in Portuguese waters may very from small clusters of 20 “fingers” to very large clusters of 240 “fingers”. Usually the clusters are formed by ~60 “fingers”, each measuring ~7-14 cm (9.7 cm on average). A 14 cm finger contains ~174 eggs. The egg is oval and measure 3.22±0.12 x 4.25±0.26 mm in the early stages (Fig. 4.16) and 5.79±0.01 x 8.22±0.85 mm in the prehatching stages (Fig. 4.17).

10 mm

Figure 4.17. Loligo vulgaris egg mass in late stage and detail of eggs and pre-hatchlings. 10 mm

Figure 4.16. Loligo vulgaris egg mass in early stage of development and detail of eggs.

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Suborder Oegopsina 4.3.3. Family Ommastrephidae The Ommastrephidae or are an oceanic and neritic family. The hatchling is characterised by a distinctive paralarval form, the “rhynchoteuthion”, in which the tentacles are fused into a trunk-like structure, named proboscis. As the squid grows, the proboscis begins to divide with a splitting groove forming at its base. The separation into the two tentacles is completed at a mantle length of 6-10mm, depending on species. Three species of this family occur in the western Iberia:

Illex coindetii, Todarodes sagittatus and Todaropsis eblanae. The paralarvae of the last two were never described. We found some morphological differences which could split the smallest rynchoteuthions in three types. However, the morphometrics applied was not conclusive for larger specimens. Rynchoteuthion type A “Illex coindetii”? Paralarvae of type A have a slender and long proboscis with eight suckers of equal size. The proboscis is always longer than the longer arms and start splitting at ~ 5 mm ML. The proboscis is on average 46% (± 11.1) of mantle length in paralarvae < 5 mm. Tentacular index ranges between 0.28 and 0.73. Rynchoteuthion type A on our samples is probably Illex coindetii as it is similar to drawings by Salman et al. (2003) and the descriptions of I. illecebrosus (Roper and Lu 1979) and I. argentinus (Haimovici et al. 1995).

(a)

(b)

Figure 4.18 – Rynchoteuthion type A of a 2.25 mm ML paralarvae captured on July 1990 at 39.83 ºN, 9.22 ºW (a). Detail of the long and slender proboscis (1.21 mm) (b).

93


(a)

(b)

Figure 4.19. Rynchoteuthion type A – detail of the proboscis tip of a 2.86 mm ML paralarvae (a) and a 5.28 mm ML paralarvae captured on August 1987 at , showing the beginning of the proboscis division 40.08 ºN, 9.42º W (b).

Rynchoteuthion type B Paralarvae of type B have a thick and short proboscis with eight suckers of equal size. The proboscis start splitting in paralarvae > 4 mm ML and is on average 35% (± 8.7) of mantle length in paralarvae < 5 mm. Tentacular index ranges between 0.16 and 0.53. (b)

(a)

Figure 4.20 – Rynchoteuthion type B – 2.04 mm ML paralarvae captured on May 1994 at 40.25 ºN, 9.35º W.

Figure 4.21 – Rynchoteuthion type B – detail of the proboscis (1.09 mm) of a 3.42 mm ML paralarvae captured on January 1988 at 41.08 ºN, 9.25º W.

94


Rynchoteuthion type C The larvae of type C have a thick and short proboscis with 8 suckers, 6 of similar size and 2 lateral suckers larger than the other (Fig. 4.22). The proboscis measure on average 38% (± 7.8) of mantle length and is longer than the arms in paralarvae < 3 mm ML. Tentacular index ranges between 0.27 and 0.50. Only the arms II and III are formed at < 1.5 mm ML, each with one large sucker close to the base. Eyes are prominent, mantle is as wide as long and ends as a pointed apex. Fins are small. Fourteen red cromatophores were counted on the dorsal mantle (two isolated on the posterior end) and three on the dorsal head (one central and one above each eye). Sixteen chromatophores were counted on the ventral mantle, of which one isolated on the posterior end. (a)

(b)

(c)

(d)

Figure 4.22. Rynchoteuthion type C (1.43 mm ML) captured on May 2002 at 40.90 ºN, 9.35º W. Dorsal view (a), ventral view (b), detail of head and proboscis (c) and detail of arms (d).

Enoploteuthid group of families The Enoploteuthid group includes the families Enoploteuthidae, Ancistrocheiridae, and Pyroteuthidae. These squid are characterised by highly complex photophores and the paralarvae can be distinguished by their arrangement and numbers on

95


various body parts (Table 4.3). Table 4.3. Key to families of the enoploteuthid group based on photophore patterns (Dieckmann et

al., 2002). Photophores

Enoploteuthidae

Ancistrocheiridae

Pyroteuthidae

Mantle, head, arms

+ (in rows)

+

−

Tentacles

−

+

+ (embedded in stalk)

Eyes

+

−

+

Viscera

−

−

+

4.3.4. Family Enoploteuthidae The Enoploteuthidae are among the most abundant small squids of the open ocean and are especially numerous in the subtropical region (Nesis, 1987). Two of the four genera (Abralia and Abraliopsis) were identified in the western Iberia.

Abralia veranyi The arms I-III are long, but never as long or longer than mantle length. The arms IV are much less developed. At 2.1 mm ML they have 3 photophores on each eye. Absence of light organs on arm tips, which is a key characteristic to distinguish between Abralia and Abraliopsis. The club region is undifferentiated, with minute suckers along one fourth of tentacle (Fig. 4.23). The posterior end of mantle is sharp pointed.

Figure 4.23. Abralia veranyi , head detail of a 2.1 mm ML paralarvae captured on January 1998 at 36.12 ºN, 7.50 ºW. Arrow indicates the tentacle club with very small suckers.

96


Abraliopsis pfefferi Arms and tentacles are long and mostly exceed mantle length. Arm order III ~ II > I > IV. Tentacular club with > 4 rows of suckers and hooks visible at > 4 mm ML. Fins small and round. Funnel large extending until posterior level of eyes. The large photophores on tips of arms IV are absent at ML < 4 mm (Fig. 4.24)

Figure 4.24. Ventral view of a 2.5 mm, 3.0 mm and 4.0 mm ML Abraliopsis pfefferi paralarvae and details of tentacles, arms and fins. Paralarvae captured on March 1995 at 36.63 ºN, 8.75 ºW, January 1998 at 36.12 ºN, 8.50 ºW and February 1998 at 36.61 ºN, 8.30 ºW, respectively.

4.3.5. Family Ancistrocheiridae

Ancistrocheirus lesueuri The eyes are small and separated from the arm bases. The head tissue is gelatinous. Tentacular club bears a few but very large suckers and photophores. 4.3.6. Family Pyroteuthidae Two genera (Pyroteuthis, Pterygioteuthis) are comprised in this family. Pyroteuthids are mainly found in tropical to subtropical waters. Young specimens are characterised by very small tentacular clubs that generally curl at the tip and are covered with very small suckers. In specimens larger than ~ 5 mm ML the posterior end of the mantle is sharply pointed, the terminal conus of the gladius

97


becomes visible (equivalent to the adults) and the fins show their typical appearance (rounded with two free lobes).

Pterygioteuthis sp. Gill photophores present at 1.5 mm ML; gill photophores large as or larger than anal photophores, medial ocular photophores absent at anal photophores = 0.07 mm, tentacular club with 6 suckers, arm formula: III>>II>I>>IV. At 3.7 mm ML four ocular photophores are visible as well as the beginning of the formation of other two on a row (Fig. 4.26). At ~13 mm ML anal photophores large, half silvery, half black; gill photophores larger and silvery; seven large ocular photophores plus one larger and silvery, arms with hooks and tentacular club with one row of hooks (Fig. 4.27).

2 mm

Figure 4.25. Pterygioteuthis sp. dorsal and ventral view of a 2.7 mm ML paralarvae, captured on January 1989 at 38.00 ºN, 8.92 ºW

Figure 4.26. Pterygioteuthis sp. detail of the ocular photophores of a 3.71 mm ML paralarvae.

98


Figure 4.27. Dorsal and ventral view of a 13.3 mm ML Pterygioteuthis sp., captured on February 1998 at 36.25 ºN, 10.38 ºW. Arrows highlight gill photophores >> anal photophores.

Pyroteuthis margaritifera Gill photophores absent at < 4-5 mm ML; in specimens > 5 mm ML the gill photophores are smaller than anal photophores. In freshly caught specimens tentacle a pink patch is visible at the base of each tentacle and at the carpus. No photophores visible on eye of paralarvae < 2 mm ML; 1 dark and silver photophores and several tissue knobs on eye at 2-3 mm ML (Fig. 4.28); 4 aligned photophores on eye at 3.14 mm ML (Fig. 4.29) and at 9 mm ML 10 ocular photophores of various sizes and not aligned (Fig. 4.30). Mantle tip blunt, almost rounded and fins small, round and broadly separated in paralarvae < 5 mm ML; mantle and gladius tip elongated and pointed in specimens > 9 mm ML.

(a)

(b)

2 mm

Figure 4.28. Pyroteuthis margaritifera ventral view of a 2.92 mm ML paralarvae, captured on March 2001 at 36.25 ºN, 10.38 ºW (a). Detail of eye with a single formed photophores and

99


2 mm

2 mm

Figure 4.29. Pyroteuthis margaritifera dorsal and ventral view 3.14 mm ML, captured on February 2001 at 36.49 ºN, 8.25 ºW.

10 mm

Figure 4.30. Pyroteuthis margaritifera ventral view of a 9.38 mm ML paralarvae, captured on March 2001 at 36.24 ºN, 6.75 ºW.

4.3.7. Family Onychoteuthidae

Onychoteuthis banksii The paralarvae can be easily identified by their muscular body and their visible, sharply pointed gladius (Fig. 4.31). The head of small paralarvae < 10 mm ML is generally retracted inside mantle, with only arms and tentacles outside of a constricted mantle opening. Fins broadly heart-shaped.

100


(a)

(b)

(c)

Figure 4.31. Onychoteuthis banksii dorsal view of a 6.8 mm ML paralarvae (a), ventral view of a 7.59 mm ML paralarvae (b) and dorsal view of a 10.34 mm ML paralarvae (c), captured respectively on August 1993 at 36.80 ºN, 8.28 ºW, on March 2001 at 36.24 ºN, 8.25 ºW and on May 1994 at 36.6 ºN, 11.24 ºW.

4.3.8. Family Chtenopterygidae

Chtenopteryx sicula The Chtenopterygidae are a monotypic family with the single species

Chtenopteryx sicula. The species is easily identifiable at all developmental stages by the typical ribbed fins made of muscular supports joined by a thin membrane. At 2 mm ML the fins are only one terminal flap and the head is very short and the funnel large (Fig. 4.32a). Tentacles are short and the club broad and round. The club suckers form a distinct circular pad (Fig. 4.32b). (a)

(b)

Figure 4.32 – Lateral view of a 2.1 mm ML Chtenopteryx sicula paralarvae with a small fin of only one “rib” (a) captured on April 1995 at 36.00 ºN, 8.40 ºW. Detail of the tentacle and tentacular club (b).

101


4.3.9. Family Brachioteuthidae

Brachioteuthis riisei The paralarvae have long mantle and long neck with dorsal hump (Fig. 4.33). The neck contains a fluid-filled sac that extends as a reservoir into the body. Contraction of the reservoir can greatly increase the length of the neck, thereby extending the head from the mantle. Fins are paddle-shape and separated. Even young specimens show a distinctive swelling or hump on the dorsal surface of the head. Tentacles are prominent and robust. In paralarvae ~3 mm ML clubs have suckers in two to three rows, arms I and II are very short and arms III and four are just small papillae.

2 mm

Figure 4.33. Brachioteuthis riisei 3.18 mm ML paralarvae, captured on February 2001 at 36.24ºN, 7.75 ºW.

4.3.10. Family Mastigoteuthidae

Mastigoteuthis sp. Paralarvae have long mantle, long gladius projecting posterior to the fins as a long pointed tail, protruding eyes and tentacular stalks thicker than the arms. The fins are transversely oval. Tentacle stalks with two rows of suckers along its entire length and tentacular clubs with four rows of suckers in paralarvae ~5 mm ML (Fig. 4.34). Tentacular clubs with more than four rows in the larger paralarvae. Arm formula II>I>IV>>III, arm III papilla-like in paralarvae < 10 mm ML. One light organ on ventral surface of each eye. Gladius extends posterior to fins (Fig. 4.35). There are 15 species described from specimens in poor condition thus the genus is in

102


need for revision. The specimens found in Portuguese waters differ from

Idioteuthis c.f. hjorti (formerly M. hjorti) by the smaller gladius tail and the presence of tentacle stalk suckers. (a)

(b)

2 mm

2 mm

Figure 4.34. Mastigoteuthis sp. ventral view of a 4.92 mm ML paralarvae, captured on March 1995 at 37.25 ºN, 9.50 ºW (a) and a 7.83 mm ML paralarvae (without the arm crown), captured on April 1995 at 36.25 ºN, 9.75 ºW (b).

(b)

(a)

Figure 4.35. Mastigoteuthis sp. details of the arm crown and tentacles and fins of the 7.83 mm ML paralarvae.

4.3.11. Family Chiroteuthidae

Chiroteuthis sp. The “doratopsis” paralarvae of Chiroteuthis sp. is characterized by the elongated chambered neck, a gladius extending beyond the fins, a long, slender and spindle shape mantle, a short arm-crown stalk relative to neck length and by the presence of suckers on the oral surface of the tentacular stalks (Fig. 4.36). At ~17 mm ML arm IV (with numerous suckers) measure about ¼ of tentacle length, arm formula

103


IV>>II>III>I, tentacle with suckers only on distal half of stalk and club with more and larger suckers than on stalk.

77 Figure 4.36. Chiroteuthis sp. dorso-lateral view of a 16.8 mm ML paralarvae, captured on February 2001 at 36.25 ºN, 10.38 ºW.

4.3.12. Family Cranchiidae The paralarvae are characterised by a thin walled mantle (often semigelatinous), fused with the head in the nuchal region and to the funnel locking-cartilage. Short head and tentacular club with 4 rows of suckers. The main distinctive characters between the genera of cranchiids found in Portuguese and surrounding Spanish waters are summarized in Table 4.4. Sub-fam. Cranchiinae

Leachia atlantica The mantle is spindle-shaped and elongates with growth. Gladius ends in a sharp spike. Fins are transversely elliptical. The head have a long and narrow arm-crown stalk and tubular transparent large eye stalks (Fig. 4.37a). A single tubercular cartilaginous strip extends from each funnel-mantle fusion point with a species specific tubercle arrangement: ~7-8 large rosette-shaped tubercles with small simple tubercles between them (Fig. 4.37b).

(a)

(b)

Figure 4.37. Leachia atlantica ventral view of a 42 mm ML paralarvae, captured on January 2001 at 36.24 ºN, 8.75 ºW (a), detail of the tubercular strip (b).

104


Table 4.4. Key to the genera of the family Cranchiidae found in Portuguese and surrounding Spanish waters, based on Diekmann et al. (2002) and updated from Voss et al. (1992). mantle

gladius/lanceola

fins

cartilaginous strips on ventral mantle

arm crown stalk

eyes

other features

moderately stout, spindleshaped, but elongates with growth

gladious spine projects between fins

transversely elliptical, solid gladial spine projecting between

Single strip extends from each funnelmantel fusion

long narrow stalk

on long stalks, with 5-21 oval photophores

details of tubercular strips important for species identification

elongated, sac-shaped, rounded posteriorly

gladius expanded at right angle to mantle

small, paddle-shaped, widely set apart (on gladius)

--------

long stalk

on long stalks, with ventral rostrum

tentacles short and robust in early juveniles

Helicocranchia

elongated, cylindrical, often with mucous outer layer

gladius projects dorsally free of mantle

small, paddle-shaped, insert on posterior tip of gladius

--------

short stalk

nearly sessile, with pronounced ventral rostrum

very large funnel

Liguriella

firm, stout, spindle-shaped

blunt-pointed, moderately broad, diamond-shaped delicate lanceola

paddle-shaped, become oval with growth,

--------

medium to long stalk

on long stalks, with distinct short ventral rostrum

tentacles moderately long in paralarvae < 15 mm ML, distal heavier than proximal

Taonius

elongated, narrow, coneshaped

very elongated, narrow, diamond-shaped lanceola

small, paddle-shape but with growth extending along the lanceola

---------

moderately long stalk

on very long stalks

specimens appear "stretched"

Teuthowenia

stout, saccular (< ~11 mm ML), conical with growth

lanceola of medium width, diamond-shaped, sharppointed end

small, paddle-shaped, insert on posterior tip of gladius

--------

short stalk

on short stalks, with short ventral rostrum

only genus with 4 rows of suckers extending nearly entire length of tentacular stalk

Sub-fam. Cranchiinae Leachia

Sub-family Taoninae Bathothauma

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The arms III are disproportionately elongated, very long robust tentacles with no enlarged club (Fig. 4.38). The eyes have 5-6 photophores.

Figure 4.38. Leachia atlantica ventral view of a 81 mm ML paralarvae.

Sub-fam. Taoninae

Bathothauma lyromma Mantle is sac-shaped and rounded posteriorly, the eyes are oval with a ventral rostrum on very long eye stalks and the arm-crown is also very long. The tentacles are stout in early stages (Figs. 4.39a) and long narrow in bigger paralarvae (Fig. 4.39b). The fins are small, paddle-shaped and widely separated (Fig. 4.39c). The paralarvae reaches a very large size (~10 cm ML).

Helicocranchia pfefferi The large funnel extending to level of buccal mass makes generic identification of paralarvae easy. The mantle is elongated, cylindrical, bluntly rounded at tip and often with a mucous outer layer. There is a near absence of eye stalks making the eyes nearly sessile. Eyes oval with pronounced ventral rostrum. Head with short arm-crown, arms short (Figs. 4.40, 4.41, 4.42). Fins small, wide and paddle-

106


shaped, inserted on tip of gladius (Fig. 4.43). Gladius with small to elongate narrow rostrum projecting free of end of mantle. No very enlarged suckers on arms III or tentacular clubs (~ 7 mm ML). Tentacles robust and < 100% ML, with minute suckers along entire stalk.

(a)

(b)

(c)

Figure 4.39. Bathothauma lyromma, a 7.0 mm ML paralarvae, captured on January 2001 at 36.25 ºN, 10.38 ºW (a), a 24.3 mm ML paralarvae, captured on February 2008 at 36.25 ºN, 9.88 ºW (b) and detail the posterior mantle with the wide separate fins (c).

Figure 4.40. Helicocranchia pfefferi dorsal and ventral view of a 2.35 mm ML paralarvae, captured on June 1994 at 36.34 ºN, 9.74 ºW.

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Figure 4.41. Helicocranchia pfefferi dorsal and ventral view of a 4.4 mm ML paralarvae, captured on June 1994 at 36.34 ºN, 9.74 ºW.

Figure 4.42. Helicocranchia pfefferi dorsal view of a 8.25 mm ML paralarvae captured on June 1994 at 36.34 ºN, 9.74 ºW.

Figure 4.43. Helicocranchia pfefferi growth series of posterior mantle, gladius and fins: 2.35 mm ML, 5.76 mm ML and 8.25 mm ML (from left to right).

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Liguriella podophthalma The mantle is stout with paddle-shaped fins in paralarvae < ~15 mm ML, inserted on narrow and delicate, diamond-shaped lanceola (Figs. 4.44, 4.45a). Head have moderately long arm-crown stalk. The eyes are oval, with short ventral rostrum, on long stalks (Fig. 4.45b). Tentacles long, with 2 rows of carpal suckers on basal half and 4 rows on distal part (Fig. 4.45).

(a)

(c)

(b)

Figure 4.44. Liguriella podophthalma dorsal dorsal view of a 5.53 mm ML paralarvae (a), dorsal view of a 9.6 mm ML paralarvae (b) and ventral view of a 11.75 mm ML paralarvae (c). Paralarvae were captured respectively on February 1998 at 36.17 ºN, 8.37 ºW and at 36.37 ºN, 7.50 ºW and on February 2001 at 36.25 ºN, 9.88 ºW.

(c)

(b)

(a)

Figure 4.45. Liguriella podophthalma detail of fins (a), head (b) and tentacle (c).

Taonius pavo The mantle is elongated and cone-shaped. The fins are paddle-shaped in paralarvae < ~18 mm ML and inserted on elongated diamond-shaped lanceola. Head with moderately long arm-crown stalk. The eyes are elliptical on long stalks (Figs.4.46).

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(a)

(b)

(c)

Figure 4.46. Tanis pavo dorsal view of a 3.89 mm ML, captured on January 2001 at 37.25 ºN, 9.42ºW (a), ventral view of a 7.48 mm ML (b) and dorsal view of a 12.0 mm ML paralarvae (c), both captured on January 1998 at 36.25 ºN, 9.75 ºW.

(a)

(c)

(b)

Figure 4.47. Taonius pavo detail of head and tentacles (a), and fins of a 7.5 mm ML (b) and 12 mm ML (c) paralarvae.

Teuthowenia megalops The mantle is stout and sac-like at < 11 mm ML and becomes increasingly conical with growth. The head have a short arm-crown stalk with very small arms. Eyes are oval with a slight ventral rostrum, on short stout stalks and funnel large (Fig. 4.48). Tentacles are moderately large with a small part of the stalk with two rows of suckers, followed by four rows of suckers extending nearly entire length of tentacle (the only genus with this feature). The paralarval period is prolonged and ends when the eyes become sessile, between sizes of 75 and 95 mm.

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Figure 4.48. Teuthowenia megalops paralarvae growth series: 8.18 mm ML, 12.5 mm ML, 15.2 mm ML and 28 mm ML, captured at 40.6-41.08ºN, 8.83-9.50ºW.

Order Octopoda 4.3.13. Family Ocythoidae

Ocythoe tuberculata Mantle without fins. Arms I and IV greatly enlarged evident already in hatchlings. Head and arms of smallest paralarvae stages not enclosed in cuff-shape brachial membrane. Funnel long extending anterior to the base of arms (Fig. 4.49).

Figure 4.49. Ocythoe tuberculata 6 mm ML captured on June 1994 at 35.32 ºN, 14.37 ºW.

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4.3.14. Family Octopodidae, sub-family Octopodinae The hatchlings measure 2.0-8.0 mm ML and are covered with characteristic Koelliker’s bristles. The eyes are large and prominent. Typically only 3-4 suckers are present in a single straight row on the short arms. Mantle short and rounded. These bristles are lost and arms elongate during the growth in plankton.

Octopus salutti Short arms, with 4 suckers on subequal arms. Cromatophores on arms in two rows and uniformly distributed over entire body surface (Fig. 4.50).

Figure 4.50. Octopus saluti dorsal and ventral view of a 3.08 mm ML captured on June 1995 at 40.17 ºN, 9.75 ºW.

Octopus vulgaris Mantle elongate and conical without fins. Arms subequal with 2 cromatophores in 1 row and 3 suckers until ~3.5 mm ML. After that, the number of suckers and chromatophores on arms increases. Funnel with 2 + 2 cromatophores (Figs. 4.51, 4.52).

Figure 4.51. Octopus vulgaris dorsal and ventral view of a 2.7 mm ML paralarvae, captured on December 2004 at 36.93 ºN, 8.81 ºW.

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Figure 4.52. Octopus vulgaris dorsal and ventral view of a 5 day, 10 day and 14 day paralarvae, hatched and reared at the laboratory.

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Octopus vulgaris eggs The female spawns ~100000-500000 eggs and remain with them during the development period, after which the female die. Spawning events of a single female may differ at least 4-5 days. (Fig. 4.53). Loose fishery pots are a suitable spawning site. The female uses a broken shell “glued” to her own suckers to block the entrance of the pot.

Figure 4.53. Octopus vulgaris female inside a pot taking care of her brood, collected with a bottom trawl on the southwest Portuguese coast, during a survey cruise in September 2007. Detail of the egg mass, which was in two development stages: stage XIII deep inside the pot and stage IX at the entrance.

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The eggs are sausage-shaped capsules with a stalk to attachment in clusters to the substrate (Fig. 4.54).

stage IV

stage VIII

stage XIII

stage XVI

stage V

stage IV

stage IX

stages VII to XII

stage XIII

stage XIII

stage XVIII

stage XVI

Figure 4.54. Octopus vulgaris embryonic development in captivity.

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Chapter 5 – Distribution and seasonality of paralarvae _____________________________________________________________________________________________________________

Chapter 5. Distribution and seasonality of cephalopod paralarvae off Portugal based on 19 years of historical data

5.1. Introduction The Portuguese and adjacent Spanish waters are the northern part of the important Canary Current coastal upwelling system that stretches from Cape Finisterra (NW Spain) to Cape Vert (Senegal) and are characterized by optimum conditions for phytoplankton blooms and consequent zooplankton richness (Cunha, 2001; Moita, 2001; Aristegui et al., 2006). Differences in the main oceanographic features between the Western Iberia and the Gulf of Cádiz induce quite different environmental conditions between the western and the southern Portuguese waters, which may affect differently cephalopod paralarvae distribution and seasonality in the west and southern Portuguese waters, with significant implications on population structure. Cephalopods represent a major fishery resource in Europe, specifically in Portugal and Spain. The most important cephalopod species as fisheries resource, which have planktonic early life stages, thereafter called paralarvae (Young and Harman, 1988), are Octopus vulgaris, Loligo vulgaris, L. forbesi, Illex coindetii and

Todaropsis eblanae. These are neritic species, whose adults and juveniles occur mainly in the middle-shelf (O. vulgaris and Loligo spp.) or in the outer-shelf region (I. coindetii and T. eblanae). O. vulgaris is presently the fourth most important fishery resource in Portuguese waters with landings of about 7000 tons and a commercial value of 28.7 million € in 2006 (DGPA, 2007), which support many local fishing communities. The neritic loliginid, octopus and sepiolid females lay their eggs in capsules/clusters attached to hard substratum or branched sessile organisms on the sea bottom, while in ommastrephids and most other oceanic squids the eggs are laid into large masses that drift submerged in the open sea (Jereb et al., 2005). Embryonic development lasts from few weeks to few months, depending on water temperature (Villanueva et al., 2003). Soon after hatching cephalopod

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paralarvae are active predators of other zooplankton and active swimmers by jet propulsion, however during this life stage their distribution is essentially dependent on the oceanic circulation (Hanlon et al., 1985). Information on the distribution of paralarvae and the knowledge of the spawning grounds of the most important European cephalopod resources are scarce. However its knowledge is of major relevance for the understanding of the dispersal behaviour of paralarvae stage with important implications to recruitment success and variability. Several studies have analysed the oceanographic

influences on cephalopod paralarvae

distribution in the northwest Atlantic coastal area (e.g. Goldman, 1993; Zeidberg and Hamner, 2002) or in the open Atlantic Ocean (e.g. Diekmann and Piatkowski, 2002; 2004). Little research has been undertaken in the north-eastern Atlantic besides studies in Galicia (NW Spain), that relates the distribution of cephalopod paralarvae and the circulation associated to coastal upwelling events (Rocha et

al., 1999; González et al., 2005). Thus cephalopods early life-history dynamics in coastal upwelling systems are poorly understood. Furthermore, information about the vertical distribution of cephalopod paralarvae are even scarcer, being almost related to pelagic oceanic squid species in non-European waters (e.g. Hatanaka et

al., 1985; Roepke et al., 1993; Filippova and Pakhomov, 1994). The present study aims to identify the environmental variables and mesoscale oceanographic features, which have the main influence on the distribution and seasonality patterns of paralarvae within the Iberian upwelling system and the northern Gulf of Cádiz. Since cephalopod paralarvae are rare in plankton samples (Vechione, 1987), the analysis is based on information from 19 years of plankton sampling (1986 to 2004) off the Portuguese and adjacent Spanish waters.

5.2. Material and methods 5.2.1. Sampling Cephalopod paralarvae distribution and seasonality was analysed from plankton samples carried out during 57 survey cruises between October 1986 and

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December 2004 in the Portuguese waters, and occasionally in adjacent Spanish waters (Fig.5.1). Table 5.1 summarise the fieldwork and sampling methodologies used in this study. The sampling area covers latitude 33.23°N to 42.75°N and longitude 6.15°W to 14.37°W in the NE Atlantic. The majority of cruises were performed at a monthly or seasonal basis on board the Portuguese research vessels “Noruega”, “Capricórnio” and “Mestre Costeiro”, under sampling research programmes targeting for fish eggs and larvae. The main gear was a bongo net with a 60 cm mouth aperture diameter fitted with 335 and 500 µm mesh size nets. The net was towed on depth-integrated oblique hauls at ~2 knots from surface to 10 m above the bottom or until 200 m when the bottom was deeper. Filtered water volumes were estimated using calibrated flowmeters mounted on both net mouth apertures. In the cruises targeting for cephalopod paralarvae on board RV “Mestre Costeiro” and the German RV “Poseidon” the bongo net was towed horizontally during 10 min near bottom between double oblique tows to surface (Piatkowski and Petersen, 1995; Moreno, 1998). Most vertical distribution data was obtained from a survey targeting crustacean larvae (May 2002), in which a Pro-LHPR system and neuston net were used. The Pro-LHPR system collected samples at approximately 5 m depth intervals in the first 25 m and at 10 m depth intervals down to near bottom. Neuston net samples were collected every 2 hours during a 69 hours period in a fixed point station (for more complete description of this cruise see Santos et al. 2006). Scattered data on vertical distribution were obtained from depth stratified sampling during several cruises, with a WP-2 and a MOCNESS multiple net sampler (e.g. Piatkowski and Wieland, 1994; Farinha and Lopes, 1996). Hydrological data, when collected, were obtained from CTD casts. All samples were preserved in 4% borax-buffered formaldehyde, prepared using seawater. A total of 4156 samples were examined and 914 cephalopod paralarvae identified to the lowest taxonomic level possible, and the dorsal mantle length (ML) was measured as defined in Sweeney et al. (1992).

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Galician Bank

43 ºN

Spain Vigo

NE Atlantic 41 Portugal

39

Lisbon

Ampere Bank

37 Gorringe Bank Gulf of Cadiz

Josephine Bank

35 14 ºW

12

10

8

6

Figure 5.1. Sampling stations. Box covers the main sampling area. Stations outside the box were undertaken only once.

5.2.2. Data analysis Sea surface temperature (SST) data were extracted from CTD temperature profiles. To fill in gaps, SST data was also extracted from the integrated Global Ocean Services System – Meteorological Center “IGOSS nmc” database (Reynolds and Smith, 1994). The Pacific Fisheries Environmental Laboratory (ERD) of NOAA provided the upwelling index (UI) and the University of East Anglia (CRU) provided the North Atlantic Oscillation (NAO) index.

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Table 5.1. Plankton sampling summary. Sampling excluded in the horizontal distribution analyses of neritic species is marked with *.

Date

Target

Area

Nº of samples

CTD

Haul type

Net type

Mesh size

Oblique

Bongo 60 cm φ

335 and 500 µm

Horizontal and Oblique

Bongo 60 cm φ

335 and 500 µm

Hauls towing 10’ near bottom and oblique to surface

Stratified hauls in 3 to 8 depth layers from near bottom to surface or from 200 m to surface, where the ocean floor > 200 m

Oct 1986 to Jan 1989 (monthly)

Fish eggs and larvae

West coast: 3 transects at 41º05’N, 40º05’N, 38º00’N from shoreline to 9º35’W South coast: 1 transect at 8º35’W, from shoreline to 36º50’N

506

Yes

Feb/Mar 1992/93;

Fish eggs and larvae

Along the coast: 36º07’ to 42º45’N and 7º30’ to 10º45’W

1756

No

Jun/Jul 1990/92 Oct/Nov 1990/91/92

Hauls from near bottom to surface, or from 200 m to surface, where the ocean floor > 200 m

No

Jun/Jul 1993, Oct/Nov 1993

Yes

May 1994; Mar/Apr 1995;

No

Jan/Feb/Mar 1998/2001/04

Yes

Aug 1993

Crustacean larvae

Jun 1994

Cephalopods

Feb 2000

Fish larvae

North coast: 40º24’N to 41º36’N and 8º45’W to 10º00’W

111

No

Jun 1995

South coast: 33º14’ to 37º17’N and 7º25’ to 14º22’W

62

No

Cephalopods

North coast: 39º45’ to 41º50’N and 8º44’ to 9º45’W

160

Yes

Yes

Nov 1996; Aug 1996;

No

Aug/Sep 1995; Nov 1995

Cephalopods

Dec 2004

Fish eggs

Feb/Mar 1996 (WP2)

Fish eggs/larvae

WP2

200 µm

May 1996 (WP2)

Cephalopods

No

LHPR

280 µm

May 2002 (LHPR)

Crustacean larvae

Yes

or

or

Jun 1994 (Mocness)

Cephalopods

Yes

Mocness

335 µm

Mar/Apr 1995 (WP2)

Fish larvae

Nov 2002/03 (WP2) *

Fish larvae

Nov/Dec 1999/00/01; *

Fish eggs

Calvet

150 µm

Jan 2002 *

Method

SW and south coast: 36º48’ to 38º38’N and 7º48’ to 9º56’W NW coast: 38º17’ to 41º31’N and 8º34’ to 11º30’W

97

No Yes

1010

SW and south coast: 33º14’ to 38º45’ºN and 6º20’ to 14º22’W

314

Along the coast: 36º07’ to 41º52’N and 6º09’ to 10º00’W

140

Yes

Oblique

Yes No No No

Vertical

Hauls from near bottom to surface, or from 200 m to surface, where the ocean floor > 200 m

Catches of the neritic species were standardised to number per 100 m-3 using flowmeter information to study their distribution and seasonality. The effects of temporal and physical variables on paralarvae densities were analysed with GLM models, using R software. The GLM analysis was conducted in two steps procedures, because of the very high proportion of null samples (e.g. 83% for loliginids) and to account for both the probability of occurrence and the density by sampling station (Sousa et al., 2007): (1) a logistic regression model with the logit link (Hosmer and Lemeshow, 1989) was used to estimate the probability of a positive capture due to a given predictor, assuming that the presence/absence of paralarvae in the samples follows a binomial distribution; and (2) the gamma regression model with a log link (McCullagh and Nelder, 1989) was used to

121


estimate the expected value of positive captures (densities), assuming that the predictors interact in a multiplicative way. The occurrence/density was analysed as a response to the following continuous explanatory variables (predictors): year, month, latitude, longitude, depth, NAO, UI, and SST. First order interactions between predictors were also tested. Knowing that oceanographic features associated to upwelling events are determinant in the distribution of many zooplankton groups off the west Portuguese coast (e.g. Santos et al., 2004; Queiroga et al., 2005; dos Santos et

al., 2007), the bathymetric distribution was evaluate in more detail by testing the differences in densities by season and depth range with a factorial ANOVA. For each species, the categorical predictor season grouped samples carried out during two distinct periods (or density peaks), which showed opposite average UI. All depth-stratified samples were pooled together to provide data on loliginid and octopus vertical distribution and diel vertical migrations. Further analysis of their location in the water column and vertical migration evidence, was done by examining relative numbers and densities between sampling strategies (methods). For this, a pool of samples were selected and categorized in 4 sampling strategies: sampling by oblique tows from >15 m above the ocean floor until the surface, performed during the day (including dusk) or during the night (including dawn), and horizontal tows close to the bottom performed during the day (including dusk) or during the night (including dawn). To reduce null samples, only sampling with bongo nets carried out between June and December over the continental shelf (< 250 m) was considered in this analysis. The effect of the period of the day (day vs. night) and sampling method (water column vs. close to bottom) on numbers and densities were analyzed by factorial ANOVA. Additionally, those effects on the presence/absence data were analysed with GLM (assuming binomial distribution and using a logit function). Catches during the day include sampling one hour after sunrise until astronomic twilight and catches during the night include sampling after astronomic twilight until one hour after sunrise.

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5.3. Results 5.3.1. Neritic species The most abundant cephalopod paralarvae off the Portuguese coast belong to the neritic species (~90%) of the families Loliginidae (40.6%), Octopodidae

(Octopus

vulgaris)

(27.8%),

Sepiolidae

(11.2%)

and

Ommastrephidae (9.6%). Table 5.2 presents a summary of the spatial and temporal distribution of the different taxa found, as well as additional information about paralarvae size, total number caught, bottom depth and SST range where they were found. Table 5.2. List of paralarvae of neritic species (taxa) collected in 57 research cruises (1986 -2004) in Portuguese and adjacent waters. Summary of the spatial and temporal distribution, size range and total number caught.

Loliginidae

Loliginidae indet.

36.13 to 42.75

Bottom depth range (m) 15 to 500

13.0 to 22.7

all

ML range (mm) 1.5 to 7.5

Octopodidae

Octopus vulgaris

35.06 to 41.83

14 to 1378

13.9 to 22.7

all

1.2 to 4.2

254

Sepiolidae

Sepiolidae indet.

36.24 to 41.86

21 to 740

13.2 to 20.8

all

1.2 to 9.5

102

Ommastrephidae

Ommastrephidae indet.

33.23 to 42.75

20 to 4142

13.2 to 20.8

all

0.7 to 8.7

91

Family

Species

Latitude range (ºN)

SST range (ºC)

Seasonality (month)

5.3.1.1. Loliginids Loliginid paralarvae, mainly hatchlings (Fig. 5.2), were the most abundant group. They were found year round over the shelf, with two distinct hatching seasons: a main season in winter/early spring and a secondary season in late spring/summer, with highest densities in March and August, respectively (Fig. 5.3). In general, higher densities were found along the northwest coast of Portugal (between 39.5º N and 41.5º N). The paralarvae were found within the adult distribution over the continental shelf, particularly between the 50 and 125 m isobaths (Fig. 5.4a), and in areas with lower SST, namely 13 to 15 ºC (Fig. 5.4b). The seasonal distribution is displayed in figure 5.5.

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N 371


Number of paralarvae

70 60 50 40 30 20 10 0 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7 7.5 ML class (mm)

Figure 5.2. Length frequency of loliginid paralarvae.

Mean density (ind.100 m-3)

0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 J

F

M

A

M

J

J

A

S

O

N

D

Month

Figure 5.3. Mean monthly densities of loliginid paralarvae within their distribution area (depth < 200 m). Vertical bars denote 0.95 confidence intervals.

(a)

0.3 0.2 0.1

(b)

0.4 0.3 0.2 0.1 0.0

250_275

225_250

200_225

175_200

150_175

125_150

100_125

75_100

50_75

25_50

15_25

0.0

0.5 Density (ind.100 m-3)

Density (ind.100 m-3)

0.4

11 12 13 14 15 16 17 18 19 20 21 22 23 SST (ºC)

Depth range (m)

Figure 5.4. Mean densities of loliginid paralarvae by bottom depth range (a) and by surface temperature (SST) (b).

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GLM results (table 5.3) support the significant role of month, latitude and depth but also the importance of low temperatures and high upwelling in loliginid distribution. Moreover, the analysis indicates that there was a significant influence of the interactions month vs. latitude and SST vs. latitude (Fig. 5.6a,b). These interactions result in a spread distribution from north to south in winter, when average SST is relatively low throughout the area. In opposition, they concentrate mainly on the northwest shelf, located where SST is lower, in spring and summer (Fig. 5.5). On the other hand, the gamma model (Table 5.4) indicated that the oceanographic conditions alone had the main influence on loliginid density. This model reflects essentially seasonality rather than the spatial distribution, i.e. higher densities associated with lower SST and UI, which are the prevailing conditions during the main hatching peak (winter).

Table 5.3. Deviance tables for loliginid paralarvae logistic models (probability of positive capture). Total of variation explained by the significant variables. Estimates

Source of variation

Deviance %

βi

SE

year

0.0

-0.009

0.016

p-value 0.558

ns

month

0.8

-0.062

0.023

0.006

**

latitude

0.8

0.144

0.050

0.004

**

longitude

0.1

-0.177

0.152

0.243

ns

depth

1.7

-0.006

0.001

0.000

***

NAO

0.0

-0.008

0.079

0.917

ns

UI

1.3

0.007

0.002

0.001

***

SST

0.6

-0.097

0.038

0.012

*

month x latitude

1.4

0.029

0.014

0.041

*

month x depth

2.5

-0.001

0.000

0.211

ns

month x UI

2.6

0.000

0.001

0.877

ns

month x SST

1.0

-0.013

0.014

0.372

ns

latitude x depth

2.3

0.000

0.001

0.745

ns

latitude x UI

2.4

0.002

0.001

0.153

ns

latitude x SST

1.8

0.074

0.027

0.007

**

depth x UI

3.1

0.000

0.000

0.429

ns

depth x SST

2.4

-0.001

0.001

0.098

.

UI x SST

2.8

0.002

0.001

0.060

.

Total explained

8.4%

125


43 ºN

43

(a) winter

20 10 0 0m m

ºN

42

42

41

41

40

40

ind. 100 m-3

-

(b) spring

20 10 0 0m m

0

- 12

39

39

38

38

37

37

36

36 11 ºW

10

9

8

43 ºN

11ºW

7

ºN

42

42

41

41

40

40

39

39

38

38

37

37

36

36 11 ºW

10

9

8

13

8

15

17

19

21

10

7

(d) autumn

20 10 0 0m m

11 ºW

7

11

9

43

(c) summer

20 10 0 0m m

10

9

8

7

23 ºC

Figure 5.5. Distribution of loliginid paralarvae in Portuguese and adjacent waters in winter (a), spring (b), summer (c) and autumn (d). Overlay of seasonal SST.

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Nevertheless, the logistic model fitted to presence/absence of loliginids explained only about 8.4% and the gamma model 12.4% of total variability for the whole area. Thus, an additional analysis was carried out for the west coast to

43

43

42

42

41

41

40

40

Latitude

Latitude

highlight the role of oceanography on the loliginid distribution.

39

39

38

38

37

37

36

(a)

36 1

2

3

4

5

6

7

8

9

10

11

12

Month

(b)

12

13

14

15

16

17

18

19

20

21

22

23

SST (ºC)

Figure 5.6. Interaction of latitude and month (a) and interaction of latitude and SST (b) in loliginid paralarvae distribution. The size of dots represents densities of 1 up to 12 ind. 100 m-3.

Table 5.4. Deviance tables for loliginid paralarvae gamma models (density in positive captures). Source of variation

Deviance

Estimates

%

βi

SE

year

2.7

-0.011

0.015

p-value 0.474

ns

month

4.2

-0.036

0.023

0.122

ns

latitude

2.2

0.011

0.054

0.843

ns

longitude

2.4

-0.098

0.205

0.634

ns

depth

2.9

-0.002

0.002

0.435

ns

NAO

2.8

-0.085

0.090

0.350

ns

UI

5.0

-0.004

0.002

0.038

*

SST

7.4

-0.097

0.036

0.008

**

UI x SST

8.8

-0.001

0.001

0.536

ns

Total explained

12.4%

The spatial distribution on the west coast displayed differences between seasons of contrasting oceanographic conditions. Significantly higher densities

127


were observed offshore (75 m to 125 m isobaths) between December and March (Fig. 5.7a), corresponding to the winter coastal convergence period, and close inshore (15 m to 75 m isobaths) between June and September (Fig. 5.7b), during the summer upwelling season (ANOVA season vs. depth range effect, F(4, 613) = 2.924, p < 0.05). These differences were particularly noticeable between 40.1 ºN and 41.5 ºN on the northwest shelf (ANOVA season vs. depth range effect, F(4, 275) = 3.558, p < 0.05). A particular exception to this pattern was detected in an area located at 40.08ºN, where loliginid paralarvae could be found year round, without significant season, depth or, season*depth effect (ANOVA, F(3, 82) = 0.72261, p = 0.541). In figure 5.8 is highlighted the monthly variation on the crossshelf distribution in the west coast (interaction month vs. bottom depth).

(a)

(b)

December to March

June to September

41

41

ºN

ºN

40

40

ind. 100 m-3

12 10 ºW

10 ºW

9

9

Figure 5.7. Horizontal distribution of loliginid paralarvae in the northwest Portuguese waters during December to March (a) and June to September (b) plankton surveys. The 100 m isobath is also presented.

125

Bottom depth (m)

100

75

50

25

1

2

3

4

5

6

7

8

9

10 11 12

Month

Figure 5.8. Interaction of month and bottom depth in the loliginid densities on the west coast.

128


The results on vertical distribution have to be considered as preliminary since they are based in few numbers of paralarvae. Nevertheless, loliginid paralarvae evidenced a consistent diel vertical migration (Fig. 5.9). They may be found in surface layers (5-20 m) after sunset and the following 4 to 6 hours and are deeper during daylight. No paralarvae were found in the neuston layer at any time.

0

2

4

6

8

Time (hour) 10 12 14 16 18 20 22 24

0 -10 -20

Depth (m)

-30 -40 -50 -60 -70 -80 -90 -100

Figure 5.9. Diel vertical distribution of loliginid paralarvae. Big dots (LHPR sampling) and triangles (WP2 and MOCNESS sampling) represent paralarvae presence, small dots represent absences. Real depth sampling standardized to 100 m water column. Sampling at -1 m indicates the neuston net sampling (first 20 cm).

In face of the few data from vertically stratified sampling, the vertical distribution and vertical migration of loliginids was also evaluated by day–night differences in density, mean numbers and presence vs. absence close to the bottom and in the water column 15 m above the floor (Table 5.5). The higher density and numbers of loliginids was detected close to the bottom during the day (Fig. 5.10). However, the variability is high and we could only find significant differences in numbers caught between sampling strategies (ANOVA, F(1, 375) = 5.55, p < 0.05), but not densities (ANOVA, F(1, 375) = 1.31, p > 0.05). The percentage of samples with loliginid paralarvae was also much higher in horizontal sampling close to bottom during the day. GLM applied to presence/absence data also indicated that the highest probability of finding loliginids is during the day

129


close to the ocean floor (Wald X²(1) = 7.7640, p < 0.01). Therefore, we may conclude that the horizontal sampling close to floor is the most effective sampling strategy for loliginid paralarvae and that there is a reasonable confidence that these results also show that loliginid paralarvae are located mainly close to the ocean floor during daylight, which is also an indication of a diel vertical migration behaviour. Table 5.5. Vertical distribution of Loliginid paralarvae evaluated by sampling strategy with bongo nets in stations over the continental shelf (depth < 250 m), se = standard error. mean N (se)

Sampling strategy Water column, 15 m above floor (day) N stations = 118 Water column, 15 m above floor (night) N stations = 73 Close to floor, 0-10 m above floor (night) N stations = 65 Close to floor, horizontal 0-10 m above floor (day) N stations = 123

positive stations

0.27 (0.14)

0.11 (0.08)

10.2 %

0.10 (0.18)

0.08 (0.10)

9.6 %

0.08 (0.19)

0.10 (0.10)

7.8 %

1.01 (0.14)

0.35 (0.08)

39.8 %

1.4

(a)

(b)

1.2

0.4

Mean numbers

-3

Mean density (ind.100 m )

0.5

mean ind. 100 m-3 (se)

0.3

0.2

1 0.8 0.6 0.4

0.1

0.2 0

0 close bottom day

water column day

close bottom night

close bottom day

water column night

water column day

close bottom night

water column night

Figure 5.10. Variation in density (a) and numbers (b) of loliginid paralarvae captured by sampling strategy with bongo nets in stations over the continental shelf (depth < 250 m).Vertical bars denote 0.95 confidence intervals.

5.3.1.2. Octopus vulgaris Most octopus paralarvae (ca. 95%) were of small size (Fig. 5.11), with 3 suckers in the subequal arms. The number of suckers in each arm begins to

130


increase in paralarvae > 3 mm ML. The seasonality of octopus paralarvae is more pronounced than in loliginids. Higher densities occurred mainly in the second half of the year, with peaks in July and November (Fig. 5.12). Only eight specimens were found during

Number of paralarvae

winter months.

100 90 80 70 60 50 40 30 20 10 0 1

1.5

2

2.5 3 3.5 ML class (mm)

4

4.5

5

Figure 5.11. Length frequency of O. vulgaris paralarvae.


0.5

0.4

0.3

0.2

0.1

0.0 J

F

M

A

M

J

J

A

S

O

N

D

Month

Figure 5.12. Monthly mean densities of O. vulgaris paralarvae within their distribution area (bottom depth < 1500 m). Vertical bars denote 0.95 confidence intervals.

The two distinct peaks, a minor peak in summer and a major peak in autumn, were present throughout the sampled area, i.e. on the west and south regions. Paralarvae hatching in spring and summer (Figs. 5.13a,b) were

131


distributed over the shelf and slope between the 14 m and 1400 m isobaths, mainly between 50 and 400 m, and at the Gorringe and Ampere Banks (in June). During autumn paralarvae were found more inshore, over the continental shelf mainly between the 25 m and 150 m isobaths (Fig. 5.13c).

43

43

ºN

(a) spring

(b) summer

ºN

42

42

41

41 40

40 39

39 38

38

37

37

36

35

36 13 ºW

12

11

10

9

8

11 ºW

7

10

9

8

7

43 ºN

(c) autumn

42

11

13

15

17

19

21

23 ºC

41

40

ind. 100 m-3 -0 -6

39

Figure

5.13.

Distribution

of

O.

vulgaris

paralarvae in Portuguese and adjacent waters

38

in spring (a), summer (b) and autumn (c). Overlay of seasonal SST.

37

36 11 ºW

10

9

8

7

6

132

6


The GLM analysis revealed an important contribution of several variables and interactions between them to explain the occurrence of octopus paralarvae (total explained = 59.2 %, Table 5.6). The variables month and its interaction with depth, and SST and its interaction with UI, depth or latitude were the most significant contributors to explain octopus distribution. Overall, the probability of finding paralarvae increased along the year (higher in autumn), with increasing SST and upwelling, and decreasing latitude (higher in the south) and depth (higher inshore). Table 5.6. Deviance tables for O. vulgaris paralarvae logistic models (probability of positive capture). Total of variation explained by the significant variables. Source of variation

Estimates

Deviance

p-value

%

Βi

SE

year

0.000

-0.002

0.017

0.920

ns

month

10.309

0.248

0.026

0.05) and the higher densities for low UI (Fig. 5.15a) likely reflect the autumn non-upwelling peak. In spite of the gamma model did not show any significant influence of the interaction between month and depth on the whole area distribution (Table 5.7),

134


this interaction is significant on the west coast (Table 5.8).

1.2

0.4 west

1.0

Mean density (ind. 100 m-3)


west south

0.8 0.6 0.4 0.2

south

0.35 0.3 0.25 0.2 0.15 0.1 0.05

0.0

0

1

2

3

4

5

6

7

8

9

10

11 12

11 12 13 14 15 16 17 18 19 20 21 22 23

Month

SST (ºC)

Figure 5.14. Variation in mean densities of O. vulgaris paralarvae in the west and south Portuguese waters with month (a) and SST (thin line = west and thick line = south moving average) (b).

Table 5.8. Deviance table for O. vulgaris paralarvae logistic and gamma models for the west coast. Total of variation explained by the significant variables (the only ones displayed in the table).

Model

Estimates

Source of

Deviance

variation

%

βi

SE

SST

8.56

0.381

0.051

1.16E-13

***

month

7.8

0.212

0.031

6.76E-12

***

logistic

p-value

UI

2.7

0.010

0.003

9.47E-05

***

NAO

0.98

-0.466

0.185

0.012

*

11.78

-0.007

0.002

5.24E-05

***

UI * SST Total explained

33.9 % year

10.29

-0.060

0.020

0.003

**

depth

10.15

-0.001

0.001

0.016

*

gamma

UI

7.11

0.006

0.003

0.021

*

month

5.24

0.082

0.039

0.035

*

year * depth

33.62

5.18E-04

1.29E-04

0.000

***

month * depth

22.76

-0.001

0.000

0.000

***

Total explained

89.2 %

On this area, the cross-shore distribution is significantly different between seasons (ANOVA season vs. depth range effect, F(3, 769) = 2.852, p < 0.05): during the spring/summer upwelling season the density is significantly higher offshore than in the autumn/winter coastal convergence period, when the higher

135


density is observed close inshore. On the south coast, the difference of the bathymetric distribution between hatching seasons was not significant, but it may be observed a larger bathymetric range during the months of higher density (Fig. 5.16).

Table 5.9. Deviance table for O. vulgaris paralarvae logistic and gamma models for the south coast. Total of variation explained by the significant variables.

logistic

Estimates

Deviance

Source of variation

%

βi

month

16.18

0.333

0.053

2.60E-10

***

longitude

2.69

-0.613

0.213

0.004

**

depth

4.78

-0.002

0.001

0.0005

***

UI

1.79

-0.011

0.005

0.015

*

SST

1.80

0.167

0.068

0.014

*

month x depth

19.55

-0.001

0.0002

0.028

*

longitude * UI

7.60

0.018

0.007

0.007

**

UI * SST

7.64

-0.012

0.004

0.005

**

-0.062

0.021

0.005

**

Total explained Gamma

62.0 % year

15.70

Total explained

15.7 %

0.25 south

0.2

Upwelling index


west

0.15 0.1 0.05 0 -100-25

p-value

SE

-25-0

0-25

25-100

Upwelling Index (m3/s/100m coastline)

100 80 60 40 20 0 -20 -40 -60 -80 -100

(m3/s/100m coastline)

Model

1 2 3 4 5 6 7 8 9 10 11 12 Month

Figure 5.15. Variation in mean densities of O. vulgaris paralarvae in the west and south Portuguese waters in relation to the upwelling index (a). Month and upwelling/downwelling interaction on presence (large dots) and absence (open circles) of paralarvae on the west coast (b).

136


West

South

450 400 350 300 250 200 150 100 50 0

450 400 350 300 250 200 150 100 50 0

Bottom depth (m)

> 500

Bottom depth (m)

> 500

1 2 3 4 5 6 7 8 9 101112 Month

1 2 3 4 5 6 7 8 9 101112 Month

Figure 5.16. Monthly bathymetric distribution of O. vulgaris paralarvae on the west and south Portuguese waters.

The diel vertical distribution pattern of octopus is not clear from the depth stratified sampling, compiled from different stations, seasons and areas (Fig. 5.17). No paralarvae were found in the neuston layer at any time.

0

2

4

6

8

Time (hour) 10 12 14 16 18 20 22 24

0 -10 -20

Depth (m)

-30 -40 -50 -60 -70 -80 -90 -100

Figure 5.17. Diel vertical distribution of O. vulgaris paralarvae. Big triangles represent paralarvae presence (WP2 and MOCNESS sampling), small dots represent absences. Real depth sampling standardized to 100 m water column. Sampling at -1 m indicates the neuston net sampling (first 20 cm).

Due to the few data from vertically stratified sampling, as in loliginids, the vertical distribution and vertical migration of O. vulgaris was also evaluated by

137


day–night differences in density, mean numbers and presence vs. absence close to the bottom and in the water column 15 m above the floor (Table 5.10). A significantly higher density of paralarvae is located close to the bottom at night (ANOVA location vs. time effect: F(1, 375) = 5.29, p < 0.05). The percentage of samples with octopus paralarvae and the higher numbers were captured in the water column during the day, however with no significant differences (ANOVA: F(1, 375) = 1.44, p >0.05) between sampling strategies (Fig. 5.18). These results seem a good indication that the diel distribution in the water column of O. vulgaris is opposite to loliginids, or at least that each species display distinct behaviours.

Table 5.10. Vertical distribution of O. vulgaris paralarvae evaluated by sampling strategy with bongo nets in stations over the continental shelf (depth < 250 m), se = standard error. mean N (se)

Sampling strategy Water column, 15 m above floor (day) N stations = 118 Water column, 15 m above floor (night) N stations = 73 Close to floor, 0-10 m above floor (night) N stations = 65 Close to floor, horizontal 0-10 m above floor (day) N stations = 123

positive stations

0.52 (0.06)

0.17 (0.03)

23.7 %

0.21 (0.07)

0.16 (0.03)

16.4 %

0.25 (0.08)

0.34 (0.03)

16.9 %

0.29 (0.05)

0.05 (0.02)

17.1 %

0.8

(a)

(b)

0.7

0.4 0.6 Mean numbers


0.5

mean ind. 100 m-3 (se)

0.3

0.2

0.5 0.4 0.3 0.2

0.1 0.1 0

0 close bottom day

water column day

close bottom night

close bottom day

water column night

water column day

close bottom night

water column night

Figure 5.18. Variation in density (a) and numbers (b) of O. vulgaris paralarvae by sampling strategy with bongo nets in stations over the continental shelf (depth < 250 m).Vertical bars denote 0.95 confidence intervals.

138


5.3.1.3. Sepiolids Sepiolids were found over the continental shelf (only 3 specimens deeper than 200 m), located in two separate areas (Fig. 5.19 and Fig. 5.20): on the northwestern shelf between 40º and 42º N, occurring mainly in winter and spring, inshore of the 100 m isobath and on the southwestern and southern shelves, south to 38º N, between summer and winter, mainly offshore of the 100 m isobath. 43

43

ºN

20

0 100 m m

(a) winter

ºN

42

42

41

41

40

40

39

39

38

38

37

37

36

36

43

11 ºW

10

9

8

20 1 0 00 m m

11ºW

7

10

(b) spring

9

8

7

43

ºN

20

0 100 m m

(c) summer

ºN

42

42

41

41

40

40

39

39

20

0 100 m m

(d) autumn

ind. 100-3 - 0 - 6 11

38

38

37

37

36

13

15

17

19

21

23

36 11 ºW

10

9

8

11ºW

7

10

9

8

7

Figure 5.19. Horizontal distribution of sepiolid paralarvae in Portuguese waters and adjacent Spanish regions during winter (a), spring (b), summer (c) and autumn (d) plankton surveys. Overlay of seasonal SST.

139

ºC


The variables included in the GLM modelling poorly explain the distribution of these paralarvae for the whole area (2.8%), with year and depth being the only significant contributors (Table 5.11), reflecting mainly the higher occurrences in 2002 and 2004 and generally offshore of the 80 m isobath. At the same time, the gamma model explained 23.7% of the total variance, with month and SST as the major contributors. Density was significantly higher during the first months of the year (Fig. 5.20) when the average SST is lower throughout the whole sampling area and this could explain the inverse relationship with this variable. Nevertheless, temperature shows a clear influence on distribution, independently of season, with paralarvae occurring associate to the lower SST range of every season. Table 5.11. Deviance table for sepiolid paralarvae logistic and gamma models. Total of variation explained by the significant variables. Model

depth

logistic

year Total explained

gamma

p-value

%

βi

SE

1.83

0.009

0.003

0.002

**

0.98

0.051

0.022

0.021

*

15.40

-0.103

0.030

0.001

**

8.28

-0.114

0.052

0.031

*

2.8 %

month SST

23.7 %


Total explained


Estimates

Deviance

Source of variation

0.6

0.4

0.2

0.0

0.6

0.4

0.2

0.0 J

F M A M

J

J

A

S O N D

J

Month

F M A M

J

J

A

S O N D

Month

Figure 5.20. Monthly mean densities of sepiolid paralarvae within their distribution area (bottom depth < 200 m) on the northwest region (a) and on the southwest and south regions (b). Vertical bars denote 0.95 confidence intervals.

140


A detailed analysis separately for the northwestern shelf and the southwestern/southern shelf showed no seasonal depth range differences within each area (ANOVA, F(3, 689) = 0.118, p > 0.05, F(3, 425) = 0.351, p > 0.05, respectively in the north and south).

5.3.1.4. Ommastrephids Ommastrephids were mostly in the rhyncoteuthion stage (only 7 specimens presented some proboscis division, DML > 5.3 mm). Many paralarvae had the head, arms and proboscis inside the mantle cavity, which may be a result of retraction at time of preservation. Paralarvae were found year round, with three distinct peaks in January, April/May and October (Figure 5.21) and distributed mainly in the northwestern shelf and shelf break north of 40º N, between the 50 m


and 300 m isobaths (Fig. 5.22).

0.2

0.1

0.0

J F M A M J J A S O N D Month

Figure 5.21. Monthly mean densities of ommastrephid paralarvae within their distribution area (bottom depth < 1500 m). Vertical bars denote 0.95 confidence intervals.

GLM results (Table 5.12) significantly highlighted the higher probability of capture ommastrephid paralarvae in northern latitudes. The interaction latitude vs. month was also significant, reflecting the seasonal variation in the spatial distribution: a spread to the north and south of the main distribution area was detected in autumn/winter (Fig. 5.22a) and during spring/summer most paralarvae

141


occurred in the northern shelf (Fig. 5.22b). During winter some specimens occurred in oceanic waters, namely between the continental shelf-break and oceanic seamounts (Galicia and Gorringe Banks). Table 5.12. Deviance table for ommastrephid paralarvae logistic model. Total of variation explained by the significant variables (total explained in the gamma model = 0%). Source of variation

Estimates

Deviance %

βi

SE

year

4.25

-0.131

0.030

latitude

2.76

0.291

depth

0.94

-0.0004 0.062

0.035

p-value 0.000

***

0.080

0.000

***

0.0002

0.052

.

0.075

.

month

0.58

year x month

5.68

-0.026

0.010

0.008

**

year x depth

5.35

1.54E-04

6.82E-05

0.024

*

month x latitude

5.39

0.0683

0.024

0.004

**

Total explained

20.7 %

43

43

ºN

ºN

(a) October to March

42

(b) April to September

42

41

41

40

40

39

39

38

38

37

37

ind. 100 m-3 -0 -6

36

10

11 ºW

10

9

8

00

10 0 20 m 0 m

36

10 00

m

11 ºW

7

11

13

15

17

19

21

10

9

8

10 0 20 m 0 m m

7

23 ºC

Figure 5.22. Horizontal distribution of ommastrephid paralarvae in Portuguese waters and adjacent Spanish regions during October to March (a) and April to September (b) plankton surveys. Overlay of seasonal SST.

142


There is also a significant role of year and the interactions: year vs. month and year vs. depth, suggesting high interannual variability. A more detailed analysis revealed higher densities offshore (100-300 m) between April and September under the summer upwelling conditions and close inshore (50-100 m) between October and January, during the autumn/winter coastal convergence (ANOVA, season vs. depth range effect, F(5, 868) = 3.9273, p < 0.05). The paralarvae distribution was limited to SST between 13 and 20 ºC.

5.3.2. Oceanic species Ninety-six paralarvae and early juveniles of 19 different taxa of oceanic cephalopod species occurred in the sampling area. The majority of them belonged to the enoploteuthid group and the family Cranchiidae. Details concerning distribution, seasonality and size for each of the taxa are summarized in Table 5.13. Paralarvae were grouped according to the main species distribution in tropical and sub-tropical (TST), sub-tropical to south temperate (STST), tropical and temperate (TT) and temperate to sub-artic species (TSA), after Nesis (1982) and Clarke (2006). The occurrence of oceanic paralarvae peaked during January and decreased until August. No oceanic paralarvae were found between September and December, despite the offshore sampling (over bottom depths > 200 m) undertaken during those months (Fig. 5.23).

Paralarvae frequency

0.14 TST

0.12

STST

TT

TSA

0.1 0.08 0.06 0.04 0.02 0 1

2

3

4

5

6

7

8

9

10

11

12

Month

Figure 5.23. Monthly frequency of oceanic paralarvae grouped as mostly tropical and sub-tropical species (TST), sub-tropical to south temperate (STST), tropical and temperate (TT) and temperate to sub-artic (TSA).

143


Table 5.13. List of paralarvae of oceanic species (taxa) collected in 57 research cruises (1986 2004) in Portuguese and adjacent waters. Summary of the spatial and temporal distribution, size range and total number caught. Paralarvae group = tropical and sub-tropical (TST), sub-tropical to south temperate (STST), tropical and temperate (TT) and temperate to sub-artic species (TSA).

B. depth range (m)

SST range (ºC)

ML range (mm)

N

1, 7

10.6

2

1, 2, 4, 6, 7

1.9 - 13.3

9

1, 2, 3

2.1 - 9.4

5

17.0 - 19.4

1, 3

1.5 - 4.4

6

17.7

1

2.1

1

745 - 3681

17.2 - 17.3

1, 2, 3, 6

2.5 - 7.8

5

36.24 - 37.06

20 - 2400

15.6 - 17.2

1, 3

3.0 - 5.3

2

36.12 - 36.99

63 - 900

17.1 - 17.7

1, 5

1.5 - 2.5

5

Species

Sepiolidae

Heteroteuthis dispar

TT

36.24 - 36.70

587 - 750

17.8 - 20.9

Pterygioteuthis sp.

TST

35.75 - 38.00

65 - 2000

16.0 - 17.3

Pyroteuthis margaritifera

TST

36.24 - 36.49

614 - 4788

17.3 - 19.4

Pyroteuthidae indet.

TST

36.25 - 36.87

132 - 4788

Abralia cf. veranyi

TST

36.12

310

Abraliopsis atlantica

TST

36.12 - 36.69

Ancistrocheirus lesueuri

STST

Eno. group indet.

TT

Pyroteuthidae

Enoploteuthidae Ancistrocheiridae Enoploteuthid group

Cranchiidae

Mastigoteuthidae Onychoteuthidae

Group

Latitude range (ºN)

Family

Seasonality (month)

Bathothauma lyromma

TST

36.25 - 37.75

3000 - 4765

16.2 - 18.1

1, 2

7.0 - 24.3

2

Helicocranchia pfefferi

STST

36.34 - 36.72

742 - 3681

-

5, 6

2.4 - 8.3

5

Leachia sp.

TST

36.24 - 36.75

2043 - 3400

17.0 - 17.3

1

26.8 - 52

4

Megalocranchia sp.

TST

36.17 - 36.75

800 - 3000

16.9 - 19.1

2, 3

5.5 - 11.8

Taonius pavo

STST

36.25 - 36.57

800 - 4000

17.2 - 19.5

1, 2

2.5 - 15.6

Teuthowenia megalops

TSA

40.25 - 41.08

45 - 3850

13.8 - 15.0

2, 3

4.4 - 28

5 1 1 5

Taoninae indet.

TT

34.93 - 37.71

228 - 1290

18.3

3, 6

2.2 - 4.1

5

Mastigoteuthis sp.

TT

36.12 - 40.75

310 - 3460

15.6 - 18.8

1, 2, 3, 4

4.9 - 9.9

9

Onychoteuthis banksii

STST

36.24 - 40.75

230 - 3000

15.0 - 18.8

2, 3, 5, 6, 8

6.8 - 11.2

6

Onychoteuthidae indet.

STST

39.75 - 40.30

162 - 1030

15.4 - 16.9

2, 5

2.7 - 3.7

2 4

Chiroteuthidae

Chiroteuthis veranyi

STST

36.25 - 37.25

210 - 3000

16.0 - 19.4

1, 2, 3

4.8 - 16.8

Brachioteuthidae

Brachioteuthis reesei

TT

36.24

968

17.8

2

3.2

1

Chtenopterygidae

Ctenopterix siculus

STST

36.00

2000

-

4

2.1

1

Ocythoidae

Ocythoe tuberculata

TST

35.32

4318

-

6

6

1

Most taxa were found only during winter months (Chiroteuthis sp.,

Pyroteuthis margaritifera, Abralia cf. veranyi, Ancistrocheirus lesueuri, Leachia sp., Taonius pavo, Bathothauma lyromma, Megalocranchia sp., Teuthowenia megalops and Brachioteuthis reesei), while others were found during winter and spring (Abraliopsis atlantica, Mastigoteuthis sp.), only in spring (Helicocranchia

pfefferi, Ctenopterix siculus, Ocythoe tuberculata) or throughout winter to summer (Pterygioteuthis sp., Onychoteuthis banksii, Heteroteuthis dispar).

Teuthowenia megalops, the only species whose main distribution is in north temperate to sub-artic waters in the Atlantic, was captured on the western Iberia only in winter, north of 40 ºN and SST below 15º C. During this season, only

Mastigoteuthis sp. and Onychoteuthis banksii paralarvae occurred also north of 38

144


ºN. Most oceanic paralarvae (89%) were distributed in the southern part of the sampling area, in the warmer oceanic stations and few on the colder continental shelf. Subtropical and tropical species were restricted to the southern area, south of the Gulf of Cádiz northern recirculation front and mostly within SST ~17 ºC (Fig. 5.24).

43 ºN 42

19

IPC

PoC

18 17

PoC

16

41

15 14

40

13

IPC 12º C

39 WIWiF

38 e cent t. Vi S e Cap

IPC?

37 36

Gulf of Cádiz

AC

35

AC

14ºW

13

12

11

10

9

8

7

6

Figure 5.24. Distribution of paralarvae of oceanic species during winter months. Filled triangles represent the temperate to sub-artic species, open triangles the tropical to temperate species, stars the sub-tropical to south temperate species, and open circles represent the tropical/sub-tropical species records. Dots represent the sampling stations. Overlay of winter sea surface temperature (SST) and major winter surface circulation features, after Peliz et al. (2005): PoC = Portugal Current, IPC = Iberian Poleward Current, AC = Azores current eastern branch (arrows); WIWiF = Western Iberia Winter front, Gulf of Cádiz northern re-circulation and STF/AC frontal systems (thick lines).

145


Fewer oceanic species were captured during spring-summer months. During this season most paralarvae occurred on the southern slope and close to seamounts, distributed mainly at SST ~17-18º C (Fig. 5.25).

43 ºN 42

20

IPC

PoC

19 18

PoC

Uj

17

41 16 15

40

14 º

39

C

IPC

38 te icen St. V e p Ca

IPC?

37 Gulf of Cádiz

36 AC

35

AC

14 ºW 13

12

11

10

9

8

7

6

Figure 5.25. Distribution of paralarvae of oceanic species during spring-summer months. Open triangles represent the tropical to temperate species, stars the sub-tropical to south temperate species, and open circles represent the tropical/sub-tropical species records. Dots represent the sampling stations. Overlay of spring-summer sea surface temperature (SST) and major summer surface circulation features, after Mason et al. (2005): PoC = Portugal Current, IPC = Iberian Poleward Current, AC = Azores current eastern branch, Uj = upwelling jet (arrows); Gulf of Cádiz northern re-circulation and STF/AC frontal systems (thick lines).

146


5.4. Discussion The Portuguese waters are an important area for the spawning of numerous neritic and oceanic species, which is reflected in the high biodiversity found. This study was based in plankton sampling from several cruises and different programmes, throughout a 19 years period. Sampling methodology bias was avoided by the standardisation of catches, and the adjustment of the analysis to the data available (e.g. high number of zero catches). 5.4.1. Loligo vulgaris Loliginid paralarvae are very similar in shape and thus difficult to identify to species level, especially when cromatophore pattern is absent, as it is the case of most old preserved plankton samples. However, the relatively low abundance of

Loligo forbesi off the Portuguese coast (Chen et al., 2006); the occasional recoveries of loliginid egg masses, all identified as being L. vulgaris (e.g. Cunha et

al., 1995; Villa et al., 1997), and the size at hatching measured in reference collections of preserved specimens, lead us to assume that the loliginid paralarvae caught were mainly L. vulgaris, with a small percentage of Alloteuthis subulata. Furthermore, the hatching period inferred from loliginid paralarvae densities matches the spawning season of L. vulgaris. The spawning peaks in December/January and June/July (Moreno et al., 2002; Chapter 1 in this volume), followed by an embryonic development of 40-47 days on average (Villanueva et

al., 2003), would produce two seasons of higher densities of hatchlings with peaks around March and August, as detected in our analysis. SST revealed to be the most important environmental factor, enough to be determinant of species seasonality and distribution, in agreement to other studies that put in evidence the role of temperature on L. vulgaris life strategies and population dynamics (e.g. Moreno et al., 2005). Therefore, higher densities and a broader distribution were found during the main hatching peak, when average SST is relatively low throughout the area, whereas in the warm season, the higher densities were located in areas with lower temperature, namely associated to cold upwelled waters. Therefore, despite the location of an important spawning ground at the southern area (9 to 8 ºW) in summer (Cunha et al., 1995), we found low

147


density of L. vulgaris paralarvae, when temperatures were quite high. This indicates that the upwelling relaxation lead to favourable conditions for larval advection from the hatching sites in this area. It is observed that during this time of the year, a coastal warm countercurrent is formed extending westwards and turning northwards along the western coast after reaching Cape St. Vincent (Relvas and Barton, 2005). This inshore counterflow is a potential mechanism for the northwards advection of L. vulgaris hatchlings from their southern spawning grounds, located at lower depths during summer months (Villa et al., 1997). Furthermore, this drifting expose squid paralarvae to the influence of colder and more productive upwelled waters of the west coast and thus enhance their survival. The distribution and seasonality of L. vulgaris paralarvae on the northwest shelf were quite distinct and reflect well the oceanography of the western Iberia. Therefore in summer, although paralarvae are under the influence of upwelling conditions and consequently cross shelf transport in the Ekman surface layer is expected to advect them towards the open ocean, the higher densities were found mainly in the middle shelf, broadly located in the vicinity of the main northern spawning ground (Cunha et al., 1995). However, our data suggest that L. vulgaris paralarvae perform diel vertical migrations, similar to other cephalopod paralarvae (Piatkowski et al., 1993). Thus, the cross-shelf net transport associated to upwelling dynamics coupled to larval diel migration patterns could result in favourable condition for their retention over the spawning grounds during summer as hypothesised by observations and models for crustacean larvae in the same geographic area (Marta-Almeida et al., 2006; dos Santos et al., in press). The positive influence of upwelling events in the abundance of L. vulgaris paralarvae was previously observed during summer in the vicinity of Ria of Vigo (Rocha et al., 1999; González et al., 2005). In winter, when paralarvae density is higher, a part of the new generation is able to spread offshore as a result of the cross shelf downwelling dynamics, which promote net offshore transport for paralarvae that occupy the bottom layers during most part of the day/night period. Nevertheless, they will be retained over the shelf break by the blocking effect of the IPC which in the long run could promote also a net poleward advection (Santos et al., 2004; Peliz et al., 2005), as

148


indicated by the spread to the north observed in Fig. 5.5a. At the same time, the absence of paralarvae close to the shore in the northwestern coast during winter is likely to avoid the less saline coastal waters derived from intense river runoff (Ribeiro et al., 2005). 5.4.2. Octopus vulgaris

O. vulgaris is widely spread over mainland shelf waters, as well as in distant oceanic islands and seamounts. The length of embryonic development has an inverse relationship with temperature and it may take from 1.5 to 4 months until hatching (Mangold and Boletzky, 1973) under the temperature range the eggs may experience within Portuguese waters at depths < 100 m. Year round spawning is observed in fisheries and survey data off northwest Portugal with two distinct peaks in February/March and July/August (see chapter 3). The average duration of egg development may take ~110 and ~95 days, respectively, based on the degree-day model of Katsanevakis and Verriopoulos (2006) and the average bottom temperatures estimated at depth < 100 m during the months following each spawning peak (IPIMAR cruzdem database). Therefore, two density peaks of paralarvae would be expected in June/July and in October/November, which matches well with our observations. The autumn hatching peak could be magnified as a result of faster development of the eggs laid by the end of the summer spawning season, since with the end of the upwelling season bottom temperatures rise abruptly in shallow depths. In the north-west coast, the seasonal distribution of octopus seems to agree well with the Ekman dynamics of cross-shelf transport, showing higher densities offshore during the upwelling season and near the shore during the convergence period, in opposition to L. vulgaris paralarvae. Despite the more offshore distribution of octopus paralarvae in summer, the double frontal system on the wide continental shelf north of 40º N turns this area in a major retention area, preventing massive larvae advection and consequent loss into the open ocean (Peliz et al., 2002). This different summer distribution of L. vulgaris and O.

vulgaris paralarvae, may be related to their distinct diel vertical migration behaviour. However, this knowledge is still very scarce and further investigation about the vertical distribution and behaviour is necessary.

149


The two octopus hatching peaks on the west Portuguese coast mirror the octopus strategy described by Demarcq and Faure (Demarcq and Faure, 2000) in the Canary Current upwelling system off NW Africa. In our study we give further evidence that the reproductive strategy of O. vulgaris follows the seasonal dynamics of the major local processes. Similar to the Arguin bank and the South Senegalese coast (Demarcq and Faure, 2000), O. vulgaris in the northwest Portugal is able to adjust their population dynamics in terms of spatial and temporal optimisation of enrichment and retention processes for the planktonic paralarvae, by having two spawning/hatching peaks. On the contrary, in high upwelling but weak retention areas, the hatching season is narrowed out of the more advective months, which is a common reproductive strategy in other groups of marine species within the coastal upwelling ecosystems (Shanks and Eckert, 2005). Accordingly, just further north, in Galician waters, a unique peak of early hatched octopus occurs at the end of summer and autumn months (Otero, 2006). On the other hand, on the southern Portuguese waters the spawning season extends throughout the year with higher intensity in summer, which is very similar to the reproductive strategy on the north-eastern Gulf of Cádiz (RodriguézRúa et al., 2005) and on the western Mediterranean (Mangold 1963, Sanchez and Obarti 1993). A single paralarvae peak would be expected on the southern Portuguese waters ~80 days later (Katsanevakis and Verriopoulos 2006), taking into account the mean local bottom temperature (~15 ºC) that follows the main spawning season (IPIMAR cruzdem database). This is in agreement to the observed dominant autumn peak in paralarvae density. However, it does not explain well the existence of the summer peak in our data. A plausible explanation is a drift of the newly hatchlings during June-July within the equatorward flow of relatively cool water associated with the upwelling regime of the west coast, which in part turns eastwards around Cape St. Vincent and then flows along the southern coast mixing with the locally upwelled waters (Sánchez and Relvas, 2003). This water mass with SST below 19ºC flows eastward until ~8º W (Relvas et al., 2007) and coincides with the distribution of paralarvae along the southern shelf break. As the swimming capacity of newly hatchlings (< 3 cm s–1) is very weak, (Villanueva et al., 1995), some may be carried as far as ~190 km within the upwelling jet (~16-22 cm s–1) (Sanchez and

150


Relvas, 2003), from the west to the south coast in 10 days. This should be enough to reveal a paralarvae density peak in July in the south coast. Following this oceanic circulation a few specimens could also be advected offshore by the long upwelling filament that protrudes close to Cape St. Vincent (Relvas et al., 2007), and be caught in June at the Gorringe and Ampere seamounts. Nevertheless, we do not exclude the possibility that the paralarvae on the banks result from resident populations. The drift hypothesis from the west to the south coast is supported by the significant influence of SST and upwelling on O. vulgaris paralarvae distribution that was demonstrated by our study, which denotes a strong association of these paralarvae and water masses properties, namely the 18-19ºC upwelled waters. This peak on distribution of paralarvae during summer on the southern coast may also be an indication that a significant part of the summer spawning would occur in shallow waters, at areas with high bottom temperatures, producing significant offspring within a month time. 5.4.3. Sepiolids The poor correlation observed between paralarval sepiolid distribution and environmental variables is caused by the occurrence of several species with different distributions and spawning seasonality. Indeed, the paralarvae found, which were not identified to the species level, may include a mixture of Rossia

macrosoma, Sepietta oweniana, and Rondeletiola minor that are the most abundant species within the surveyed area (Guerra, 1992). Some paralarvae caught could belong also to the less abundant species: Sepietta neglecta, Sepiola

atlantica, and Sepiola rondeleti. Nevertheless, our observations are consistent with the knowledge that all those species undergo spawning all year round (Jereb and Roper, 2005). The most interesting finding was that paralarvae were retained on the continental shelf, in spite of adult distribution range spreads far offshore (until 500 m or even 1000 m depth). This could be and indication that these species migrate inshore for spawning in Atlantic waters, as observed for many species in the Mediterranean Sea (Jereb and Roper, 2005). Unlike the other cephalopod paralarvae, no seasonal oceanographic effects on paralarvae dispersal were

151


observed. Thus, the distinct depth distribution detected between the northern and southern areas may be more related to the actual geographic differences between those areas. Namely, in the northern area the shelf is much wider (~ 60 km) than in the southern area (~ 25 km) (Peliz et al., 2005), and distinct depth range distributions suggest similar distances from the coast. 5.4.4. Ommastrephids Some morphological differences were detected among ommastrephids, however, as there were no paralarvae descriptions for some species, all specimens were analysed as a single group. Although the most abundant species,

Illex coindetii and Todaropsis eblanae spawn all year round throughout Atlantic European waters, I. coindetii have a main spawning season between spring and summer (González and Guerra, 1996; Arvanitidis et al., 2002; Hernández-García, 2002; chapter 2 in this volume) and T. eblanae spawns mainly during summer in northern waters (Hastie et al., 1994; Robin et al., 2002; Zumholtz and Piatkowsky, 2005) and south of 44ºN have two spawning seasons, in early spring and early autumn (González et al., 1994; Arkipkin and Laptikovsky, 2000). The high paralarvae density in spring matches well the spawning peak of both species, giving ~ 15 days for egg development (Sakai et al., 1998). On the other hand, the paralarvae of the October peak may represent mainly the T. eblanae second spawning season. Paralarvae of Todarodes sagittatus could be considered negligible as a component of this group since the spawning females that approach the Portuguese continental waters are in few numbers from May until December (IPIMAR cruise data). Nevertheless, T. sagittatus, in spite of having an extended spawning season, show a well-pronounced winter peak in the northwestern African waters (Arkhipkin et al., 1999) and thus the January peak of ommastrephids in our samples could correspond to T. sagittatus paralarvae, including those specimens found between the continental shelf-break and oceanic seamounts. Ommastrephid spawning grounds in the northeast Atlantic are unknown but it is possible to suggest their location based on the occurrence of females in spawning condition, namely regarding T. eblanae, which is less migratory than the

152


sympatrics I. coindetii and T. sagitattus (Lordan, 2001). I. coindetii and T. eblanae spawning females may be found mainly in the southwest and southern areas during spring and summer months (IPIMAR cruise data). During this season there is a clear mismatch between the spatial distribution of spawning females and paralarvae, which were found mainly confined to the continental shelf between 42 and 40 ºN. Although paralarvae may be rapidly transported within water masses (Trites, 1983), it is more likely that the mature fast swim ommastrephids migrate northwards, namely by taking advantage of the subsurface Iberian Poleward Current (IPC) in the vicinity of the shelf-break (Peliz et al., 2005). This northwards migration

in

spring/summer

months

allow

females

to

meet

favourable

environments for spawning in more productive areas with moderate temperatures, because eggs and paralarvae fail to develop at temperatures >20 ºC (Boletzky et

al., 1973; Brunetti and Ivanovic, 1992). The area of higher density of ommastrephid paralarvae was at all seasons within the one already described as retentive for biogenic material in northwestern Iberia (Relvas et al., 2007). These results emphasises the importance of the productive upwelling areas for the reproduction and early growth of migratory pelagic species, thus the lack of significant influence of temperature or upwelling in the statistical analysis of distribution and abundance was hide by the mixture of species. 5.4.5. Oceanic species The oceanic species composition in the Portuguese waters was similar to other sub-tropical eastern Atlantic areas. In spite of histioteuthids being fairly more common in this region (Nixon and Young, 2003; Clarke, 2006; 2007), their early young stages were not found, and the mesopelagic enoploteuthids and cranchiids, whose hatchlings occur in near-surface waters (e.g. Gibbs and Roper, 1970), dominated the catches. The adults of most of the paralarvae identified may be found in the northwest Africa (Adam, 1983) and in the Madeiran waters (Rees and Maul, 1956; Clarke and Lu, 1995) towards the mid-Atlantic ridge, in the vicinity of seamounts and in the Azores waters (Dieckmann et al., 2002; Clarke 2006). Those species have their northernmost range of distribution in Portuguese waters, when approaching for spawning, between January and June. They take advantage

153


of the major circulation regimes, illustrated in figures 5.24 and 5.25, such as the eastern branch of the Azores current (AC) and the Gulf of Cadiz northern recirculation, which transports warm sub-tropical water, as well as the flow associated to the Western Iberia Winter Front (WIWiF) formed around 39-40ºN in winter (Peliz et al., 2005). On the contrary, the cranchiid Teuthowenia megalops, which is a common species west of British Islands (Collins et al., 2002), extends its spawning ground further south in winter and its paralarvae will reach the northwest Portuguese coastal waters. For the northern species, warmer temperatures are likely to be a major boundary to equatorward dispersal. T. megalops specimens were all found in the same geographic area, and are a good example of adult or larval drift equatorwards by the broad southward-flowing Portugal Current (Pérez et al., 2001) and inshoreward advection under the prevailing winter convergence in northwest Portuguese waters. Despite the wide geographic sampling coverage, the oceanic paralarvae were mainly concentrated in the Gulf of Cádiz system, including many cosmopolitan

species

with

wide

latitudinal

distribution

range,

such

as

Brachioteuthis reesei and Heteroteuthis dispar. The persistent thermal and thermohalin fronts between the shelf and deep waters close to Cape S. Vicente associated with the northward recirculation of the AC (Sanchez and Relvas, 2003; Peliz et al., 2005), represent a major boundary to poleward dispersal, which would result in the concentration of oceanic cephalopod paralarvae in the southwestern Iberian Peninsula. For tropical to sub-tropical species favourable temperature for paralarvae development clearly restrained the spatial distribution, which was almost restricted to 17-18 ªC water masses.

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Concluding Remarks _____________________________________________________________________________________________________________

Concluding Remarks

155


_____________________________________________________________________________________________________________

156


Concluding Remarks and Perspectives for Future Research It is clear that the cephalopod species analysed have a high degree of biological variation across their geographic distribution. Most of the biological indices analysed showed a geographic trend implying species adaptation to largescale environmental trends. Under favourable environmental conditions, squids and octopus adjust their reproductive season in order that prey availability and temperature could enable the maximisation of growth rates of paralarvae and juveniles and consequently increase recruitment success.

L. vulgaris living at different water temperature regimes evidenced geographic variability in reproductive and growth-related parameters and those living in areas which differ in the oceanographic regimes showed distinct spawning/recruitment patterns and consequent population complexity (north France~Greek Seas vs. northwest Portugal~Saharan Bank). Length-weight relationship slopes increased from the north to the south in the Atlantic and from Atlantic to the Mediterranean. Full maturity occurred at smaller size in northwest Portugal than in other areas of the Atlantic, and at similar size as Mediterranean squid. Illex coindetii, which performs extensive migrations, showed less pronounced differences in life-cycle parameters between the geographic populations studied than L. vulgaris. Nevertheless, I.

coindetii males from the Portuguese waters showed also significantly higher lengthweight slopes than those from northern areas. Additionally, ML50% was also lower in the Portuguese waters than on the Southern Celtic Sea and Bay of Biscay and similar to the values on the Greek Seas. The seasonality of reproduction and recruitment of Octopus vulgaris were also the main differences found between the populations living on the northwest and south Portuguese waters, closely related with the oceanography of the western Iberia upwelling and the Gulf of Cadiz ecosystems. Several studies suggest that significant migrations of O. vulgaris, when they exist, are only bathymetric and linked to reproduction (Mangold-Wirz, 1963; Quetglas et al., 1998). Therefore, latitudinal movements from the west to the south

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_____________________________________________________________________________________________________________

Portuguese waters may depend on the dispersal during the planktonic phase associated to the shelf circulation. These movements were inferred by combining both fisheries data on spawning peaks and paralarvae abundance from plankton sampling. Nevertheless, the hypothesis of migration out of fishing grounds deserves to be subject of future directed research. The paralarvae identification key and illustrations, gathering disperse available information and new descriptions of specimens, egg and egg masses found within the Portuguese and surrounding Spanish waters, proved to be an essential tool to describe the distribution patterns of paralarvae. Nevertheless, the taxonomy of cephalopods captured by plankton nets is still difficult because the early life stages of many species are virtually unknown. Future efforts should be made to attempt the description of some abundant species in Portuguese waters, e.g. the short-finned squid Todaropsis eblanae, by artificial fertilization on research cruises during the spawning season. The analyses of paralarvae distributions showed that temperature along with oceanographic mesoscale processes and features, including currents, thermal fronts, coastal upwelling and related features play a crucial role in modulating population dynamics for cephalopod planktonic paralarvae, as they are for other plankton communities (e.g. Bakun, 1996; dos Santos et al., 2007; Santos

et al., 2007). The direct influence and interaction between several variables result in a spread distribution of loliginid paralarvae from north to south in winter, when average SST is relatively low throughout the area. In opposition, they concentrate mainly on the northwest shelf, located where SST is lower, in spring and summer. The influence of the physical environment is specially pronounced for the paralarvae of O. vulgaris, following distinct patterns related to the regional oceanography of the western Iberia and the Gulf of Cádiz. The probability of finding octopus paralarvae increase along the year (higher in autumn), with increasing SST (higher at 18-19 ºC), decreasing latitude (higher in the south) and decreasing depth (higher inshore). When modelling data separately for the west and south areas we conclude that the influence of SST independently of season is more pronounced on the west coast and octopus paralarvae distribution is highly

158


correlated with upwelling, independently of hatching season and only in this area. Additionally, on the west there is a significant influence of the interaction between month and depth, which results from seasonal differences in the cross-shelf transport linked to the upwelling conditions. Differences in distribution within the northwest shelf between loliginids and octopus lead to the hypothesis that they have distinct diel vertical behaviour. Although, this is relatively evident for loliginids, it is not very clear in the case of O.

vulgaris taking into account the few data available. Thus, the design of directed experiments and more adequate sampling devices are required to clarify the vertical distribution of these species. The analysis of the distribution of all neritic species highlighted higher paralarvae densities within the most retentive area for biogenic material in the northwestern Iberia upwelling system (Relvas et al., 2007), emphasising the importance of this particular geographic area (~40 - 41.5ºN) for the reproduction and early growth of the most important cephalopod fishery resources. While discussing the results, our interpretations were supported with studies made in other areas and in captivity. To obtain a more refined model of the life cycle of squid and octopus from Portuguese waters there are still some important data missing. A good knowledge of the spawning areas, associated physical variables (namely bottom temperature) and paralarvae behaviour in the water column are mandatory studies to infer the duration of embryonic development, paralarvae advection from spawning sites and predict recruitment to other geographic areas. New technologies for tag and track paralarval cephalopods may be one of the most promising approaches to address this question, as pointed out in Semmens et al. (2007). Along with the existing fisheries monitoring, a good monitoring of the physical variables would help also the marine resources population modelling. The collection of biological parameters across a range of fishing grounds by similar methods and temporally coincident (part I) was an important step towards

159


_____________________________________________________________________________________________________________

the understanding of the plasticity of life-traits of cephalopod species. Furthermore, the analysis of plankton samples, presented in part II, revealed to be an essential contribution for the interpretation of the population dynamics of those species. However, more in-depth studies relating life history strategies to environmental conditions are desirable to achieve a better understanding of the population dynamics within climate changing scenarios and provide adequate background for the establishment /improve of conservation regulation.

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References __________________________________________________________________________________________________________

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Fotografias da capa da esquerda para a direita: 1. Fêmea de polvo-comum, Octopus vulgaris, a tomar conta da sua postura dentro de um alcatruz de plástico abandonado, recolhido no NE “Noruega” durante um cruzeiro demersal em Setembro 2007 (foto de Ana Moreno), 2. Paralarva de polvo-comum Octopus vulgaris, eclodida da postura da fotografia 1, no laboratório de aquacultura do L-IPIMAR, após algumas semanas de incubação (foto de Ana Moreno obtida a partir de uma sequência de vídeo), 3. Paralarva de lula-vulgar, Loligo vulgaris, eclodida no laboratório de zooplâncton do LIPIMAR, após alguns dias de incubação (foto de Ana Moreno), 4. Exemplar adulto de lula-vulgar, Loligo vulgaris, recolhido à toneira no NE “Noruega” durante um cruzeiro demersal em Setembro 2007 (retocada a partir de foto de Paulo Oliveira, www.paulofotos.com).

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