How climate change may influence loliginid squid populations

GLOBAL OCEAN ECOSYSTEM DYNAMICS GLOBEC Report 24: The Role of Squid in Open Ocean Ecosystems GLOBEC Report No.24 THE ROLE OF SQUID IN OPEN OCEAN ECOSYSTEMS Report of a GLOBEC-CLIOTOP/PFRP workshop, 16-17 November 2006, Honolulu, Hawaii, USA Robert J. Olson and Jock W. Young (Eds.) GLOBAL OCEAN ECOSYSTEM DYNAMICS GLOBEC Report No. 24 THE ROLE OF SQUID IN OPEN OCEAN ECOSYSTEMS Report of a GLOBEC-CLIOTOP/PFRP workshop, 16-17 November 2006, Honolulu, Hawaii, USA Robert J. Olson and Jock W. Young (Eds.) The GLOBEC Report Series (Ed. Manuel Barange) is published by the GLOBEC International Project Ofice and includes the following: No. 1. Towards the development of the GLOBEC Core Programme. A report of the irst International GLOBEC planning meeting. Ravello, Italy, 31 March - 2 April 1992. No. 2. Report of the irst meeting of an International GLOBEC working group on Population Dynamics and Physical Variability. Cambridge, United Kingdom, 1-5 February 1993. No. 3. Report of the irst meeting of the International GLOBEC working group on Sampling and Observation Systems. Paris, France, 30 March - 2 April 1993. No. 4. Report of the irst meeting of the ICES/International GLOBEC working group on Cod and Climate Change. Lowestoft, England, 7-11 June 1993. No. 5. Report of the irst meeting of the International GLOBEC working group on Development of an International GLOBEC Southern Ocean Program. Norfolk, Virginia, USA, 15-17 June 1993. No. 6. Report of the irst meeting of the International GLOBEC working group on Numerical Modelling. Villefranche-sur-Mer, France, 12-14 July 1993. No. 7. Southern Ocean Implementation Plan. Bremerhaven, Germany, 6-8 June 1994. No. 7a. Report of the meeting of the Southern Ocean Planning Group, San Diego, California, 1-3 August 1997. No. 8. Report of the irst planning meeting on Small Pelagic Fishes and Climate Change Programme. La Paz, Mexico, 20-24 June 1994. No. 9. IGBP Report No. 40. Global Ocean Ecosystem Dynamics Science Plan. No. 11. Small Pelagic Fishes and Climate Change Programme Implementation Plan. No. 12. Report of the irst SPACC Modelling workshop. Ispra, Italy, 14-16 October 1996. No. 13. IGBP Report No. 47. Global Ocean Ecosystem Dynamics Implementation Plan. No. 14. Report of a Workshop on the Use of the Continuous Underway Fish Egg Sampler (CUFES) for Mapping Spawning Habitats of Pelagic Fish. No. 15. Report of a GLOBEC-SPACC/APN Workshop on the Causes and Consequences of Climateinduced Changes in Pelagic Fish Productivity in East Asia, 25-27 October 2001, Kobe, Japan. No. 16. Report of a GLOBEC-SPACC/IDYLE/ENVIFish Workshop on Spatial Approaches to the Dynamics of Coastal Pelagic Resources and their Environment in Upwelling Areas, 6-8 September 2001, Cape Town, South Africa. No. 17. Report of the GLOBEC Workshop on Optical Plankton Counters, 17-20 June 2001, Tromsø, Norway. No. 18. CLimate Impacts on Oceanic TOp Predators (CLIOTOP). Science Plan and Implementation Strategy, 2005. No. 19 Ecosystem Studies of Sub-Arctic Seas (ESSAS) Science Plan, 2005. Hunt, G.L., Jr and K.F. Drinkwater (Eds.). No. 20 Background on the Climatology, Physical Oceanography and Ecosystems of the Sub-Arctic Seas. Appendix to the ESSAS Science Plan, 2005. Hunt, G.L., Jr and Drinkwater, K.F. (Eds.). No. 21 Report of a GLOBEC/SPACC Workshop on Characterizing and Comparing the Spawning Habitats of Small Pelagic Fish, 12-13 January 2004, Concepción, Chile. van der Lingen, C.D., L. Castro, L. Drapeau and D. Checkley (Eds.). No. 22 Report of a GLOBEC/SPACC Meeting on Characterizing and Comparing the Spawning Habitats of Small Pelagic Fish, 14-16 January 2004, Concepción, Chile. Castro L.R., P. Fréon, C.D. van der Lingen and A. Uriarte (Eds.). No. 23 BASIN. Basin-scale Analysis, Synthesis, and INtegration. Wiebe, P.H., R.P. Harris, M.A. St John, F.E. Werner and B. de Young (Eds.). No. 24 The role of squid in open ocean ecosystems. Report of a GLOBEC-CLIOTOP/PFRP workshop, 16-17 November 2006, Honolulu, Hawaii, USA. R.J. Olson and J.W. Young (Eds.). GLOBEC Special Contributions No. 1. Predicting and Monitoring of the Physical-Biological-Chemical Ocean. A.R. Robinson (Ed.). No. 2. An Advanced Modeling/Observation System (AMOS) For Physical-Biological-Chemical Ecosystem Research and Monitoring (Concepts and Methodology). GLOBEC International Working Groups on Numerical Modeling and Sampling Observational Systems. No. 3. GLOBEC Workshop on the Assimilation of Biological Data in Coupled Physical/ Ecosystems Models. A.R. Robinson and P.F.J. Lermusiaux (Eds.). No. 4. Report on the GLOBEC National, Multinational and Regional Programme Activities 2001. H. Willson (Ed.). No. 5. Report of the irst meeting of the SPACC/IOC Study Group on ‘Use of environmental indices in the management of pelagic ish populations’, 3-5 September 2001, Cape Town, South Africa. No. 6. Report of the second meeting of the SPACC/IOC Study Group on ‘Use of environmental indices in the management of pelagic ish populations’, 9-11 November 2002, Paris, France. No. 7. Update of the GLOBEC National, Multinational and Regional Programme Activities, 2004. D.M. Ashby (Ed.). Additional copies of these reports are available from: GLOBEC International Project Ofice Plymouth Marine Laboratory Prospect Place Plymouth PL1 3DH United Kingdom Tel: +44 (0)1752 633401 Fax: +44 (0)1752 633101 e-mail: [email protected] Homepage: www.globec.org The GLOBEC Report Series is partially supported by the US National Science Foundation under grant OCE-0608600. Any opinions, indings and conclusions or recommendations expressed in these reports are those of the authors and do not necessarily relect the views of the US National Science Foundation. GLOBEC is a Programme Element of the International Geosphere-Biosphere Programme (IGBP). It is co-sponsored by the Scientiic Committee on Oceanic Research (SCOR) and the Intergovernmental Oceanographic Commission (IOC). The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA PREFACE This report documents a workshop that was held under the auspices of CLIOTOP Working Group 3: Trophic Pathways in Open Ocean Ecosystems. The workshop was co-sponsored by GLOBEC, the Pelagic Fisheries Research Program (PFRP) of the University of Hawaii, USA; the Inter-American Tropical Tuna Commission (IATTC), California, USA; and the Commonwealth Scientiic and Industrial Research Organisation (CSIRO), Tasmania, Australia, and hosted by the PFRP. The workshop was held on 16-17 November 2006. It aimed to summarise relevant information on pelagic squid, and address how changing oceanographic conditions may affect squid’s central role as prey and predator in open-ocean ecosystems. This report should be cited as: Robert J. Olson and Jock W. Young (Eds.). 2007. The role of squid in open ocean ecosystems. Report of a GLOBEC-CLIOTOP/PFRP workshop, 16-17 November 2006, Honolulu, Hawaii, USA. GLOBEC Report 24: vi, 94pp. i The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA TABLE OF CONTENTS PREFACE ............................................................................................................................... i TABLE OF CONTENTS..........................................................................................................ii LIST OF ABBREVIATIONS AND ACRONYMS .....................................................................iv ABSTRACT ........................................................................................................................... v ACKNOWLEDGEMENTS......................................................................................................vi INTRODUCTION ................................................................................................................... 1 BIOLOGY AND ECOLOGY ................................................................................................... 3 Horizontal and vertical migrations of Dosidicus gigas in the Gulf of California revealed by electronic tagging W.F. Gilly ...................................................................................................................... 3 Distribution of Dosidicus gigas paralarvae off the west coast of the Baja California peninsula, Mexico S. Camarillo-Coop, R. De Silva-Dávila, M.E. Hernández-Rivas and R. Durazo-Arvizu.... 7 Cephalopod metabolism as a function of body size B.A. Seibel, R. Rosa and L.A. Trueblood .................................................................... 9 Metabolism of jumbo squid Dosidicus gigas as a function of CO2 concentrations R. Rosa and B.A. Seibel .............................................................................................11 Prey size-predator size relationships of squid and their predators in the Northwest Atlantic M.D. Staudinger, F. Juanes and J. Link ..................................................................... 13 Comparing squid optimal cost of transport speeds to actual ield migrations: new data from 40-g Loligo opalescens J. Payne and R. O’Dor............................................................................................... 16 Fin laps: key adaptation for habitat expansion in the squid, Dosidicus gigas? R. O’Dor, J. Stewart and W. Gilly .............................................................................. 19 Epiplanktonic squid from the west coast of the Baja California Peninsula, Mexico J. Granados-Amores, R. De Silva-Dávila and M.E. Hernández-Rivas ...................... 22 Post-spawning egg-care in the squid, Gonatus onyx: implications for diving mammals B.A. Seibel ................................................................................................................. 25 CLIMATE IMPACTS ............................................................................................................ 28 How climate change may inluence loliginid squid populations G.T. Pecl and G.D. Jackson ...................................................................................... 28 Long-term changes in the stock abundance of neon lying squid, Ommastrephes bartramii, in relation to climate change, the squid ishery, and interspecies interactions in the north Paciic T. Ichii, K. Mahapatra, M. Sakai and D. Inagake ....................................................... 31 How climate change might impact squid populations and the ecosystems: A case study of the Japanese common squid, Todarodes paciicus Y. Sakurai .................................................................................................................. 33 ii The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Studies of the jumbo squid (Dosidicus gigas d´Orbigny, 1835) in Mexico: Fishery, ecology and climate C.A. Salinas-Zavala, S. Camarillo-Coop, A. Mejia-Rebollo, R. Rosas-Luis, J. RamosCastillejos, R. Ramírez-Rojo, D. Arizmendi, G. Bazzino, N. Dimaté-Velasquez and U. Markaida-Aburto.................................................................................................... 35 TROPHIC LINKS ................................................................................................................. 42 Contribution of cephalopod prey to large pelagic ish diet in the central north Atlantic Ocean J. Logan, R. Toppin, S. Smith, J. Porter and M. Lutcavage ...................................... 42 Cephalopod prey of the apex predator guild in the epipelagic eastern Paciic Ocean F. Galván-Magaña, R.J. Olson, N. Bocanegra-Castillo and V.G. Alatorre-Ramirez .. 45 New information from predator diets on the importance of two Ommastrephidae: Sthenoteuthis oualaniensis in the Indian Ocean and Hyaloteuthis pelagica in the Atlantic Ocean F. Ménard, M. Potier, E. Romanov, S. Jaquemet, R. Sabatié and Y. Cherel ............. 49 Trophic ecology of jumbo squid, Dosidicus gigas, in the Gulf of California and adjacent waters U. Markaida, R. Rosas, C. Salinas and W. Gilly........................................................ 53 The jumbo squid, Dosidicus gigas, a new groundish predator in the California Current? J.C. Field and K.A. Baltz............................................................................................ 55 Artisanal catches of jumbo squid Dosidicus gigas off Coquimbo, Chile and their relation to environmental variables E. Acuña, L. Cid, J.C. Villarroel and M. Andrade ....................................................... 57 Use of stable isotopes to examine foraging ecology of jumbo squid (Dosidicus gigas) R.I. Ruiz-Cooley and U. Markaida ............................................................................. 62 Signature fatty acids: a robust method for evaluating trophic relationships in open ocean ecosystems C.F. Phleger, J.W. Young, M. Guest, M. Lansdell and P.D. Nichols .......................... 64 MODELLING ....................................................................................................................... 68 Assessing the potential role of predation by jumbo squid (Dosidicus gigas) and ishing on small pelagics (common sardine Strangomera bentincki and anchovy Engraulis ringens) and common hake (Merluccius gayi) in central Chile, 33-39°S H. Arancibia and S. Neira .......................................................................................... 68 The direct and indirect contributions of cephalopods to global marine isheries M.E. Hunsicker, T.E. Essington, R. Watson and R. Sumaila ..................................... 71 Modelling environmental inluences on squid life history, distribution, and abundance G.J. Pierce, M.B. Santos, C.D. MacLeod, J. Wang, V. Valavanis and A.F. Zuur ....... 73 PERSPECTIVES AND DISCUSSIONS............................................................................... 78 Squid - the new ecosystem indicators G.D. Jackson and R.K O’Dor..................................................................................... 78 Perspectives on Dosidicus gigas in a changing world W.F. Gilly and U. Markaida ........................................................................................ 81 WORKSHOP PARTICIPANTS............................................................................................. 91 iii The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA LIST OF ABBREvIATIONS AND ACRONYMS ARIMA Autoregressive Integrated Moving Average Models ARMA Autoregressive-Moving Average AVHRR Advanced Very High Resolution Radiometer BSR Body Size Relationship CalCOFI California Cooperative Oceanic Fisheries Investigations CLIOTOP CLimate Impacts on Oceanic TOp Predators DFA Dynamic Factor Analysis DHA Docosahexaenoic Acid ENFA Ecological Niche Factor Analysis ENSO El Niño Southern Oscillation EPA Eicosapentaenoic Acid FMSY Fishing Mortality at MSY GAM Generalised Additive Model GAMM Generalised Additive Mixed Modelling GIS Geographic Information System GLM Generalised Linear Model GLOBEC Global Ocean Ecosystem Dynamics IATTC Inter-American Tropical Tuna Commission ICPMS Inductively Coupled Plasma Mass Spectrometry IPO International Project Ofice IRI Index of Relative Importance LME Large Marine Ecosystem LRL Lower Rostral Lengths MDS Multi-Dimensional Scaling ML Mantle Length MSY Maximum Sustainable Yield NAO North Atlantic Oscillation OML Oxygen Minimum Layer OTN Ocean Tracking Network PFRP Pelagic Fisheries Research Program POST Paciic Ocean Shelf Tracking PSAT Pop-up Satellite Archival Tags PUFA Polyunsaturated Fatty Acid RAPD Random Ampliication of Polymorphic DNA SST Sea Surface Temperature STFZ Sub-tropical Frontal Zone STL Seasonal and Trend decomposition using Loess TZCF Transition Zone Chlorophyll Front iv The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA ABSTRACT This report summarises, via a series of extended abstracts, a workshop to examine current research on the ecological role of squid in ocean ecosystems worldwide. The workshop was held at the University of Hawaii, Honolulu, 16-17 November 2006. The workshop was sponsored by GLOBEC/CLIOTOP and the Pelagic Fisheries Research Program (PFRP), University of Hawaii, and was organised as a contribution from CLIOTOP Working Group 3 (Trophic Pathways in Open Ocean Ecosystems). The workshop was attended by 37 participants from 9 countries. Twenty one talks and ive posters were presented. Four themes, biology and ecology, climate impacts, trophic links, and modelling, were addressed in a series of presentations followed by theme discussions moderated by a nominated specialist in that theme. The workshop concluded with a combined session which attempted to identify the major outcomes, challenges, and areas for future research, particularly in relation to climate change. Because of the dramatic rise in the biomass of the jumbo squid, Dosidicus gigas, since 2000, there was a signiicant focus on this species during the workshop, particularly on its role as an indicator species in relation to potential scenarios of ocean warming. Research on other species, particularly from the families Ommastrephidae and Loliginidae, was also presented. Topics included distribution and abundance, isheries, trophic relationships, laboratory studies, and modelling. The workshop identiied a number of research gaps, particularly the lack of long term data sets, and the paucity of research in the Indian and Atlantic Oceans. One of the central points to emerge was that the dificulty of capturing squid generally was a major impediment to understanding their role and importance in ocean ecosystems. As such, new methodologies are needed to develop a better understanding of this fauna. To this end, a number of new methodologies were detailed. In particular, research showing the value of satellite and archival tagging in understanding the movement and behaviour of these animals was presented. A variety of biochemical techniques, including fatty acid and stable isotope analysis showed promise in identifying the ecological role of squid in a broader spatial and temporal context. The workshop ended with a number of recommendations for future research, which are summarised at the end of the report. v The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA ACkNOWLEDGEMENTS The convenors and editors thank Dr Manuel Barange (GLOBEC IPO) and Dr John Sibert (PFRP, University of Hawaii) for their encouragement and sponsorship of this workshop. We also thank Ms Dodie Lau and Mr Johnoel Ancheta (PFRP), for their assistance in organising and running the workshop; Mrs Lotty Dunbar (GLOBEC IPO) for organising travel for participants, and Miss Dawn Ashby (GLOBEC IPO) for her assistance in publishing this report. Funding from GLOBEC and PFRP and support from IATTC and CSIRO are gratefully acknowledged. Finally, we are grateful to the enthusiasm of the attendees and their willingness to provide the very informative extended abstracts of which this report is comprised. vi The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA INTRODUCTION The GLOBEC regional programme CLIOTOP (Climate Impacts on Oceanic Top Predators) has the central aim to identify, characterise, and model the key processes governing the dynamics of oceanic pelagic ecosystems leading to “top” predators, such as tunas, billishes, mammals, and seabirds. The goal is to develop an improved understanding of the impact of climate variability and ishing on the upper trophic levels, and a reliable predictive capability for single species and ecosystem dynamics at short-, medium-, and long-term scales (Maury and Lehodey, 2005). Prerequisite for this goal is an understanding of the components and structure of pelagic ecosystems, and an appreciation of how changes in the pelagic environment will affect what we consider to be the status quo. CLIOTOP Working Group 3 (Trophic Pathways in Open Ocean Ecosystems) developed a number of objectives to understand the trophic pathways that underlie the production of tunas and other oceanic predators, including 1) the characterisation of the main trophic pathways of oceanic top predators and how they differ among and within oceans, and 2) identifying evidence for changes in trophic pathways over time and space, while considering seasonal and spatial variability. The traditional pelagic food web model on which much of our understanding of ecosystem interactions is based is a conceptual pyramid, with large pelagic ishes at the top and preying on increasingly complex groups of organisms at lower trophic levels, and supported by primary production at the base. Cephalopods play a central role in many, if not most, marine pelagic food webs by linking the massive biomass of micronekton, particularly myctophid ishes, to many oceanic predators. Given the high trophic lux passing through the squid community, a concerted research effort on squid is critical to advancing our understanding of their role as key prey and predators. Renewed interest in squid-ecosystem dynamics is motivated by recent remarkable range expansions of Humboldt or jumbo squid (Dosidicus gigas) in the eastern Paciic Ocean (e.g. Field and Baltz, p.55 this volume; Arancibia and Neira, p.68 this volume; Zeidberg and Robison, 2007), and speculation whether climate variability and/or ishing on squid predators could have promoted the increase. Characterised by short life spans and fast growth rates, squid may respond more readily to changes in the environment and in the trophic structure than perhaps any other mid-trophic-level organism in the open ocean. In spite of their importance in pelagic ecosystems, squid are not well understood. In part, this is because of their ability to largely avoid capture by conventional marine sampling techniques. Other factors, such as their complex taxonomy compounded by their relatively fast digestion in predator stomachs, have meant that detailed information on their role in many ocean ecosystems is lacking. New technologies, including those able to track squid movements (e.g. archival and satellite tags) and new biochemical techniques capable of identifying squid presence in the tissues of their predators (e.g. stable isotope and fatty acid analysis), are helping to resolve some of the questions surrounding squid. With encouragement and sponsorship from GLOBEC-CLIOTOP and the Pelagic Fisheries Research Program (PFRP)1 of the University of Hawaii, a workshop was held on 16-17 November 2006 at the Hawaii Imin International Conference Center at the University of Hawaii immediately following the PFRP Principal Investigators Meeting. This workshop brought together squid ecologists working in diverse ecosystems and oceanographic regions from the Paciic, Atlantic, and Indian Oceans. It The Pelagic Fisheries Research Program (PFRP) was established in 1992 after the Magnuson Fishery Conservation and Management Act (1976) was amended to include “highly migratory ish.” This amendment greatly increased the responsibilities of the Western Paciic Regional Fishery Management Council, which is mandated to manage isheries in the Western Paciic region. The PFRP was created to provide scientiic information on pelagic isheries to the Council for use in development of isheries management policies. For further information on PFRP visit http://www.soest.hawaii.edu/PFRP/pfrp1.html. 1 1 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA aimed to summarise relevant information on pelagic squid - addressing how changing oceanographic conditions may affect squid’s role as prey and predator. Workshop topics included: • • • • consideration of the role of squid in pelagic ecosystems supporting tunas and other upper-level predators; consideration of how climate change might impact squid populations and the ecosystem; consideration of the recent range expansions of D. gigas in the eastern Paciic Ocean, especially in terms of the effects of such expansions on the various ecosystems; identiication of the research needs addressing pelagic squid required to meet the goals of GLOBEC-CLIOTOP, and the identiication of potential research proposals. The workshop was attended by 37 participants from 9 countries. Twenty-one oral and ive poster presentations were made by researchers from numerous countries, including: Australia, Canada, Chile, France, Great Britain (including the Falkland Islands), Japan, Mexico, Portugal and the USA (both east and west coasts). The workshop featured four main themes: biology and ecology, climate impacts, trophic links, and modelling. A inal session, led by the moderators from each theme, reviewed the outcomes from each theme and highlighted potential future research. This report provides extended abstracts from most of the presentations and contains summaries of the discussions and conclusions at the workshop. References Maury O. and P. Lehodey (Eds.). 2005. Climate impacts on oceanic top predators (CLIOTOP). Science Plan and Implementation Strategy. GLOBEC Report 18: 42pp. Zeidberg L.D. and B.H. Robison. 2007. Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Paciic. Proceedings of the National Academy of Sciences 104(31): 12948-12950. 2 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA BIOLOGY AND ECOLOGY Horizontal and vertical migrations of Dosidicus gigas in the Gulf of California revealed by electronic tagging William F. Gilly Hopkins Marine Station, Department of Biological Sciences, Stanford University, Paciic Grove, CA 93950, USA ([email protected]). Squid of the family Ommastrephidae, migratory predators of the open seas, are ecologically and economically important on a global scale. Dosidicus gigas (jumbo or Humboldt squid), the largest ommastrephid (up to 50 kg mass and mantle length of 1.2 m), is endemic to the productive waters of the eastern Paciic, particularly those of the California Current, Peru Current and Costa Rica Dome (Nigmatullin et al., 2001; Waluda and Rodhouse, 2006). This species is the target of the world’s largest cephalopod ishery, with landings of 800,000 tonnes in 2004 (ftp://ftp.fao.org/i/stat/summary/a1e.pdf). Despite the commercial importance of D. gigas, relatively little is known of its natural behaviour. This squid grows extremely rapidly, increasing from 1 mm mantle length at birth to 1 m in a life-span of only 1-2 years (Nigmatullin et al., 2001; Markaida et al., 2004). Such a high growth rate requires a correspondingly large dietary intake, and the squid standing stock in the Guaymas Basin in the Gulf of California (Fig. 1), probably consumes ~107 kg (104 tons) per day (Gilly et al., 2006a). In this region, prey consists of mostly small mesopelagic ishes, crustaceans and other squid (Markaida and Sosa-Nishizaki, 2003). Dosidicus gigas is also a vital prey species. As juveniles, these squid are preyed on by numerous pelagic ishes (particularly tunas) and birds throughout the eastern Paciic, as described by several papers in this volume. In the Gulf of California, adult D. gigas serves as prey for both very large ishes (Klimley et al., 1993; Abitia-Cardenas et al., 2002; Rosas-Aloya et al., 2002) and marine mammals, particularly pilot and sperm whales (Ruiz-Cooley et al., 2004; 2006). Thus, jumbo squid provide an important trophic link between small mesopelagic organisms and vertebrate apex predators. 28°N 27°N 26°N 25°N 24°N 23°N 113°W 112°W 111°W 110°W 109°W 3 Figure 1. Tagging locations of Dosidicus gigas. Black triangle off Santa Rosalia marks deployment site for PSAT’s G1G7 (Wildlife Computer PSAT 3.0); pop-up locations are shown in yellow (October 2004) and green (November 2005) circles. Other tags deployed off Magdalena Bay in June 2005 (P1-P3) are denoted by red triangle and individual red circles. Data from these tags are not discussed in this report. The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Commercial ishing operations for D. gigas began in the late 1970s and have since increased dramatically in both the northern and southern hemispheres. The bulk of the Mexican ishery (~100,000 tonnes or 20% of the world total) is located in the Guaymas Basin of the Gulf of California (Fig. 1), a relatively small area where commercial ishing is centred around the ports of Santa Rosalia (June-November), and Guaymas (Markaida and Sosa-Nishizaki, 2001). Conventional tag-and-recapture studies (Markaida et al., 2005) demonstrated a seasonal migration from Santa Rosalia to Guaymas in November, and a reciprocal migration in May, but routes and rates of migration remain poorly understood. As a way of addressing migratory behaviour of D. gigas in the Guaymas Basin, we have utilised electronic archiving tagging methods, primarily pop-up satellite archival tags (PSAT). In September 2001, we deployed the irst PSAT off Santa Rosalia (G1, Fig. 1), and 3 additional tags were deployed in October 2004 (G2-G4). Pop-up positions of the 2004 tags revealed that squid could migrate at least 200 km in one week, 3-4 times faster than the speed previously estimated (Markaida et al., 2005). Secondly, the direction of migration was to the southeast (G2, G4) or east (G3). Although the direction of squid G3 seems appropriate for a migration to the Guaymas ishing grounds, the direction taken by G2 and G4 does not. This south-westward movement may represent a migration out of the Gulf and into the Paciic, or to regions of the Gulf that are presently not subject to commercial ishing. Squid G1, tagged earlier in the autumn, remained in the vicinity of Santa Rosalia. Three squid tagged in 2005 migrated to the north (G6) or northeast (G5), covering distances of ~100 km in 3 days. The end-point of squid G7 was ambiguous. Migration speeds were thus comparable to those observed in 2004, but the direction was essentially opposite to that seen previously. If squid G5-G7 were making a Santa Rosalia to Guaymas migration, it would appear that the route passes through the San Pedro Martir Basin and then turns south. A seasonal current in this part of the Gulf shows similar directionality and timing (Alvarez-Borrego, 2002), and the current switches back to a counter clockwise circulation in late spring, roughly in phase with the May migration from Guaymas to Santa Rosalia. This current could thus serve to both guide and ease migrations. Alternatively, some squid may migrate from Santa Rosalia in November to the San Pedro Martir Basin and remain there (Gilly et al., 2006b). Time-at-depth data from the PSATs consistently showed that D. gigas spent daytime hours at depths of ~300 m, whereas night-time hours tended to be spent at much shallower depths (<150 m) (Fig. 2). A night-time component was also evident at typical daytime depths. One month of time-series data from an archival tag deployed in September 2004 directly revealed frequent rapid excursions between the shallow night time zone and deep daytime zone (Fig. 3). In addition, rhythmic episodes of diving activity were prominent during both day and night at both deep and shallow depths. We believe that these excursions are related to foraging activity in at least two ways. Firstly, squid appear to forage (i.e. rhythmic diving) at night both in the shallow zone and at depth (as well as in the daytime). Secondly, they may also make deep night-time dives to recover from thermal stress encountered while foraging in warm surface waters. These ideas are discussed elsewhere in greater detail (Gilly et al., 2006a; Davis et al., 2007). 0.4 0.3 150 Night 0.2 100 0.1 50 0.0 0 0 100 200 300 400 Oxygen concentration (µM) Fraction of time Figure 2. Diel change in vertical distribution of D. gigas as revealed by PSAT tags. Time-at-depth histograms are illustrated for mean data from tags G5-G7 (November 2005). Open bars are daytime hours (local sunrise to sunset); grey bars are night-time hours. Fraction of time was computed separately for day and night. Data were collected in 1 hour bins. The blue curve represents the dissolved oxygen proile recorded at the site of tag deployment one day later. Dotted blue line represents upper boundary of the OML (~20 μM concentration). 200 Day 500 Depth (m) 4 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 0 Depth (m) 10/1 100 200 300 Quarter moon 400 430 440 450 460 Time (hours) 470 480 Figure 3. Complex diving behaviours from a squid carrying an archival tag (Lotek 1100) deployed at the same site as that for PSAT’s (September - October 2004, sampling time was 2-4 min). The plotted hour refers to cumulative time after release. Night-time hours are indicated by shaded areas; lunar phase is indicated. The 200-300 m zone bounded by dotted lines represents the upper boundary of the OML. Much high-frequency diving occurs in this hypoxic zone both day and night. Daytime depths revealed by tagging in the Santa Rosalia area are associated with a midwater hypoxic environment, the oxygen minimum layer (OML). Mean vertical distributions (day and night) computed for Tags G5-G7 are compared in Figure 2 with an oxygen proile taken 1-2 days later in the same area after deploying the tags. The dotted blue line indicates an oxygen concentration of 20 μM, our operational deinition of the upper boundary of the OML. These squid regularly inhabited depths with a lower oxygen content, i.e. deeper than ~175 m. These initial tagging experiments have increased our understanding of fundamental aspects of the biology of D. gigas concerning both horizontal migrations and daily vertical movements into the hypoxic environment of the OML. The apparent ability of this squid to maintain high levels of muscular activity at hypoxic depths while foraging and/or migrating is remarkable and is dificult to reconcile with what is known about the respiratory physiology of other active squid, including ommastrephids (Pörtner, 2002). Efforts are now underway to investigate this phenomenon in more detail, including relevant physiological and biochemical mechanisms. Tagging has also yielded insights into horizontal migrations. The inding that the November migration (Tags G5-G7) from Santa Rosalia to Guaymas may involve passage through the San Pedro Martir Basin, or perhaps to this spot as a terminal destination, is particularly interesting. This area is essentially unexplored with regard to squid and is not commercially ished (Gilly et al., 2006b). Although many questions about long-distance migrations remain unanswered, the application of PSAT methods is clearly feasible and should be more extensively applied, both in the Gulf of California and in the Paciic Ocean. Choice of times and places for tagging will be important. Our results show that D. gigas utilises the hypoxic OML to an unexpected extent. Foraging probably occurs day and night, shallow and deep. Vertical migrations are likely to represent essentially continuous searching for patches of abundant prey, with rhythmic bouts of diving activity relecting active foraging on myctophids and other members of the mesopelagic community associated with the deep acoustic scattering layer and the OML. Although the mechanisms underlying the ability to withstand hypoxic stress remain to be elucidated, the fact remains that this squid spends much time in an environment that is hostile to predatory pelagic ishes. Inhabiting the OML may protect juvenile or smaller D. gigas from predation by these ishes, but penetration of this habitat by the largest adults is likely to be the portal to foraging grounds from which pelagic predators like tunas are essentially excluded. Physiological adaptations and lexible behaviour of D. gigas must also underlie its apparent ability to rapidly exploit environmental perturbations resulting from ENSO events and other thermal anomalies, as well as hypoxia anomalies (Grantham et al., 2004). Such events alter productivity and may create transient windows of opportunity for D. gigas to expand its range (Bakun and Broad, 2003). If an area into which expansion occurs remains highly productive, the squid are likely to remain there and eventually make another excursion from the new starting point. If the area is not productive enough to support D. gigas, the squid will retract or ind another ephemeral hot spot. Because of its extremely fast growth and migratory nature, D. gigas provides an extremely rapid indicator of environmental changes. 5 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA References Abitia-Cárdenas L., A. Muhlia-Melo, V. Cruz-Escalona and F. Galván-Magaña. 2002. Trophic dynamics and seasonal energetics of striped marlin Tetrapturus audax in the southern Gulf of California, Mexico. Fisheries Research 57: 287-295. Alvarez-Borrego S. 2002. Physical oceanography. p.41-59. In: T.J. Case, M.L. Cody and E. Ezcurra (Eds.). A new island biogeography of the Sea of Cortes, Oxford University Press. Bakun A. and K. Broad. 2003. Environmental ‘loopholes’ and ish population dynamics: comparative pattern recognition with focus on El Niño effects in the Paciic. Fisheries Oceanography 13: 458-473. Davis R.W., N. Jaquet, D. Gendron, U. Markaida, G. Bazzino and W. Gilly. 2007. Diving behavior of sperm whales in relation to behavior of a major prey-species, the jumbo squid, in the Gulf of California, Mexico. Marine Ecology Progress Series 333: 291-302. Gilly W.F., U. Markaida, C.H. Baxter, B.A. Block, A. Boustany, L. Zeidberg, K. Reisenbichler, B. Robison, G. Bazzino and C. Salinas. 2006a. Vertical and horizontal migrations by jumbo squid, Dosidicus gigas, revealed by electronic tagging. Marine Ecology Progress Series 324: 1-17. Gilly W.F., C.A. Elliger, C.A. Salinas, S. Camarillo-Coop, G. Bazzino and M. Beman. 2006b. Spawning by jumbo squid Dosidicus gigas in the San Pedro Martir Basin, Gulf of California, Mexico. Marine Ecology Progress Series 313: 125-133, Grantham B.A., F. Chan, K.J. Nielsen, D.S. Fox, J.A. Barth, A. Huyer, J. Lubchenco and B.A. Menge. 2004. Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Paciic. Nature 429: 749-754. Klimley A.P., I. Caberera-Mancilla and J.L. Castillo-Geniz. 1993. Horizontal and vertical movements of the scalloped hammerhead shark, Sphyrna lewini, in the southern Gulf of California, Mexico. Ciencias Marinas 19: 95-115. Markaida U. and O. Sosa-Nishizaki. 2003. Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. Journal of the Marine Biological Association of the United Kingdom 83: 507-522. Markaida U., C. Quiñónez-Velázquez and O. Sosa-Nishizaki. 2004. Age, growth and maturation of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. Fisheries Research 66: 31-47. Markaida U., J.J.C. Rosenthal and W.F. Gilly. 2005. Tagging studies on the jumbo squid (Dosidicus gigas) in the Gulf of California, Mexico. Fishery Bulletin 103: 219-226. Nigmatullin C.M., K.N. Nesis and A.I. Arkhipkin. 2001. A review on the biology of the jumbo squid Dosidicus gigas. Fisheries Research 54: 9-19. Pörtner H.O. 2002. Environmental and functional limits to muscular exercise and body size in marine invertebrate athletes. Comparative Biochemistry and Physiology 133A: 303-321. Rosas-Aloya J., A. Hernández-Herrera, F. Galván-Magaña, L. Abitia-Cárdenas and A. Muhlia-Melo. 2002. Diet composition of sailish (Istiophorus platypterus) from the southern Gulf of California, Mexico. Fisheries Research 57: 185-195. Ruiz-Cooley R.I., D. Gendron, S. Aguíñiga, S. Mesnick and J.D. Carriquiry. 2004. Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Marine Ecology Progress Series 277: 275-283. Ruiz-Cooley R.I., U. Markaida, D. Gendron and S. Aguíñiga. 2006. Stable isotopes in jumbo squid (Dosidicus gigas) beaks to estimate its trophic position: comparison between stomach contents and stable isotopes. Journal of the Marine Biological Association of the United Kingdom 86: 437-445. Waluda C.M. and P.G. Rodhouse. 2006. Remotely sensed mesoscale oceanography of the Central Eastern Paciic and recruitment variability in Dosidicus gigas. Marine Ecology Progress Series 310: 25-32. 6 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Distribution of Dosidicus gigas paralarvae off the west coast of the Baja California peninsula, Mexico Susana Camarillo-Coop1,3, Roxana De Silva-Dávila1*, Martín E. Hernández-Rivas1 and Reginaldo Durazo-Arvizu2 Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Departamento de Plancton y Ecología Marina, Av. IPN s/n, Aptdo. 592, CP 23000, La Paz, BCS, Mexico ([email protected]). 2 UABC Facultad de Ciencias Marinas, Apdo. 453, Ensenada, BC, Mexico. 3 Current address: CIBNOR Unidad Sonora, Centenario Norte 53, Col Prados del Centenario, CP 83260, Hermosillo, Sonora, Mexico. *EDI and COFAA grant recipient 1 Squid from the Ommastrephidae family represent an important component in marine ecosystems, and are targeted by commercial isheries in many coastal and pelagic waters of the world (Yatsu, 2000). This family also contributes substantially as a food item in the diet of predators, such as procellariiform seabirds, tunas, sharks, and over 80% of the odontocete species (Weimerskirch, 1995; Clarke, 1996). In Mexico, a single species of this family, the jumbo lying squid Dosidicus gigas, is the main component of the commercial squid catches. In spite of the social and economic value of this resource in our country, the identiication of the early life stages of these squid still represents an acute problem. One of the objectives of our study was to identify the paralarvae of this species, and their distribution and abundance off the west coast of the Baja California Peninsula. All cephalopod paralarvae were sorted from zooplankton samples collected with standard Bongo net tows in September 1997 (9709) and January, July and October 1998 (9801, 9807, and 9809, respectively) as part of the IMECOCAL programme, which covered the area from Ensenada, BC to Punta Abreojos BCS, Mexico (Fig. 1). The ommastrephid paralarvae (Pl) were sorted from the samples and identiied based on the characteristic proboscis of the family. Ommastrephid Pl constituted about 1.3% in September 1997 to 82.5% in July 1998 of the total abundance of cephalopods in the study area (Fig. 2a), and were represented by four species identiied for the irst time along the west coast of Baja California, Mexico: Dosidicus gigas, Sthenoteuthis oualaniensis, Eucleoteuthis luminosa, Hyaloteuthis pelagica, two morphotypes (A and B), and a group of very small (<3 mm mantle length) Pl of D. gigas and/or S. oualaniensis from a recent spawning event (“S-D group”). Among these ommastrephids, D. gigas dominated in abundance by far during the study period (756 Pl/1000 m3). The highest abundance of this species was found during July 1998, with 32°N 55 60 100 40 35 30 ENSENADA MEXICO LF PUNTA BANDA 103 OF 107 CA 110 119 IA PUNTA EUGENIA RN FO BAHIA VICAINO 113 28°N LI Latitude Figure 1. Study area and location of sampling stations. GU 30°N 50 45 117 PUNTA ABREOJOS 120 26°N 123 127 GOLFO DE ULLOA 130 IMECOCAL 1997 - 1998 24°N 118°W 116°W 114°W 112°W Longitude 7 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 32°N ENSENADA MEXICO 1.3% 12.7% GU 30°N LF PUNTA BANDA CA 119 BAHIA VICAINO IA PUNTA EUGENIA RN 28°N PUNTA ABREOJOS 85.6% 26°N 9709 FO LI Latitude OF 32.9% IMECOCAL Cruises 9801 9807 1-15 GOLFO DE ULLOA 16 - 63 9809 64 - 255 256 - 1023 PI/1000 m3 Figure 2a. Relative abundance of the Ommastrephidae paralarvae collected during the study period (cruise 9709 was in September 1997 and cruises 9801, 9807 and 9809 were in January, July and September 1998). 24°N 118°W 116°W 114°W 112°W Longitude Figure 2b. Distribution and abundance of Dosidicus gigas paralavae during July 1998 (cruise 9807), along the west coast of the Baja California peninsula, Mexico. more than 90% of the paralarvae distributed within 50 km of the coast off Punta Eugenia (Fig. 2b). Paralarvae of D. gigas, as well as those of the S-D group, consistently were present in the south region of the study area and were collected at stations sampled at sunrise (0600 h). Dosidicus gigas paralarvae were captured at stations where the temperature at 10 m depth ranged between 19.5° and 22°C, with a peak at 20.5°C, while the S-D group was captured at temperatures ranging from 18.5° to 22.5°C, with a peak also at 20.5°C. During the study period, the 1997-1998 El Niño event, the most intense in history, was recorded in Mexican waters (Durazo and Baumgartner, 2002). Two different water masses were recognised by these authors according to their spiciness (π) values: Subarctic Water mass (SAW) (π<0.6), and Transitional-Subtropical Surface Water mass (TrStSW) (π>1.5). The paralarvae of the D. gigas and S-D group were associated with the TrStSW, and with the boundary between both water masses (π=1). References Clarke M. 1996. The role of cephalopods in the world´s oceans. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 351(343): 1053-1065. Durazo R. and T. Baumgartner. 2002. Evolution of oceanographic conditions off Baja California: 19971999. Progress in Oceanography 54: 7-31. Weimerskirch H.Ch.Y. 1995. Seabirds as indicators of marine resources: black-browed albatrosses feeding on ommastrephid squids in Kerguelen waters. Marine Ecology Progress Series 129: 295-300. Yatsu A. 2000. Age estimation of four oceanic squids, Ommastrephes bartramii, Dosidicus gigas, Sthenoteuthis oualaniensis, and Illex argentinus (Cephalopoda, Ommastrephidae) based on statolith microstructure. Japan Agricultural Research Quarterly 34(1): 1-3. Acknowledgements Funding for sample collection was provided by the following research projects: CONACyT No. G0041T and CGPI 2005-0673. We thank the Programa Institucional de Formación de Investigadores (PIFI) of the IPN, and Drs F.G. Hochberg, C.A. Salinas-Zavala and F. García-Domínguez. 8 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Cephalopod metabolism as a function of body size Brad A. Seibel, Rui Rosa and Lloyd A. Trueblood Biological Sciences Center, University of Rhode Island, 100 Flagg Road, Kingston, RI 02881, USA ([email protected]). The inverse relationship between mass-speciic metabolic rates and body mass, most famously illustrated by the ‘mouse to elephant curve’ for mammals, covering six orders of magnitude size range, is among the most established in all of biology (Schmidt-Nielsen, 1984; Calder, 1984). Metabolic rate (B) typically decreases with increasing mass (M) according to: B = b0Mb where b0 is a normalisation constant independent of mass and the exponent, b, is a scaling coeficient. Both b0 and b are reportedly highly conserved, such that metabolic rates can be modelled from only mass and temperature. However, here we show wide variation in both parameters within the class Cephalopoda related to geometrical and ecological attributes of individual species (Table 1; Fig. 1). Ommastrephid and loliginid squid (Fig. 1), including the jumbo squid, Dosidicus gigas, are highly active species with metabolic rates that fall closely along a single scaling curve. The rates of larger squid are unmatched by any organisms of similar size. Metabolic rates decline with depth in pelagic cephalopods such that deep-sea species (e.g. Vampyroteuthis infernalis) have rates similar to gelatinous zooplankton (Seibel et al., 1997; Seibel, 2007). Deep-sea hypometabolism can be explained, not by constraints associated with a seemingly inhospitable environment (hypoxia, low temperature, high pressure or food limitation), but rather by strong selection for locomotory capacity in well-lit surface waters and a relaxation of such selection in the light-limited deep-sea (Seibel et al., 1997; Seibel, 2007). The variation in scaling coeficients (b) may arise from the unique geometric allometry in tube-shaped oceanic squid. Mantle diameter increases faster than thickness with consequent growth in surface area with size (O’Dor and Hoar, 2001). Increasing surface area supports extensive cutaneous oxygen uptake, as is required to meet even resting oxygen demand (~60%; Pörtner, 2002). Also of importance, cost of transport for jet-propelled squid may not decrease as fast as that for other forms of locomotion (e.g. in swimming ishes, O’Dor and Webber, 1986). High sustained energetic requirements (to grow and reproduce) during all stages of the squid’s short life cycle is another trait unique to squid that increases relative cost at large sizes (for more discussion see Glazier, 2006; Seibel, 2007). These three factors all reduce the potential energy savings associated with large size that we believe results in the commonly reported negative allometry of mass-speciic metabolism in animals. Table 1. Oxygen consumption rates (B; µmoles O2 g-1 h-1, 5°C) in cephalopods as a function of body mass (M) (B = b0Mb) b (SE) b0 r2 n Loliginidae -0.084 (0.010) 8.20 0.56 51 Ommastrephidae -0.077 (0.015) 7.60 0.60 20 -0.02 (n.s.) 4.57 n.s. 24 Octopodidae -0.27 (0.054) 3.35 0.90 15 Histioteuthidae -0.24 (0.083) 1.36 0.58 26 Cranchidae -0.19 (0.089) 0.53 0.31 33 Bolitaenidae -0.25 (0.072) 0.27 0.66 32 Vampyroteuthidae -0.23 (0.115) 0.14 0.56 17 Family Gonatidae 9 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Oxygen Consumption (µmole O2g-1h-1) 10 Histioteuthidae Cranchidae Bolitaenidae Vampyroteuthidae Gonatidae Loliginidae Ommastrephidae Octopodidae 1 0.1 10 -3 10 -2 10 -1 10 0 10 1 10 2 10 3 10 4 Mass (g) Figure 1. Oxygen consumption rates of cephalopod families as a function of body mass. References Calder W.A. 1984. Size, function, and life history. Harvard University Press, Cambridge, Massachusetts, USA. Glazier D.S. 2006. The 3/4-power law is not universal: evolution of isometric, ontogenetic metabolic scaling in pelagic animals. Bioscience 56: 325-332. O’Dor R.K. and J.A. Hoar. 2000. Does geometry limit squid growth? ICES Journal of Marine Science 57: 8-14. O’Dor R.K. and D.M. Webber. 1986. The constraints on cephalopods: why squid aren’t ish. Canadian Journal of Zoology 64: 1591-1605. Pörtner H.O. 2002. Environmental and functional limits to muscular exercise and body size in marine invertebrate athletes. Comparative Biochemistry and Physiology A 133: 303-321. Schmidt-Nielsen K. 1984. Scaling: why is animal size so important? Cambridge University Press, Cambridge, UK. Seibel B.A. 2007. On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the class Cephalopoda (Mollusca). Journal of Experimental Biology 210: 1-11. Seibel B.A., E.V. Thuesen, J.J. Childress and L.A. Gorodezky. 1997. Decline in pelagic cephalopod metabolism with habitat depth relects differences in locomotory eficiency. Biological Bulletin 192: 262-278. 10 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Metabolism of jumbo squid Dosidicus gigas as a function of CO2 concentrations Rui Rosa and Brad A. Seibel Biological Sciences Center, University of Rhode Island, 100 Flagg Road, Kingston, RI 02881, USA ([email protected]). The absorption of atmospheric carbon dioxide (CO2) causes ocean acidiication, i.e. decreasing pH. Business as usual emission scenarios are expected to cause a reduction in global ocean pH by more than 0.3 units by the year 2100. This constitutes a doubling of the hydrogen ion concentration (Caldeira and Wickett, 2003) and is expected to have severe consequences for calcifying organisms, among others. Squid are hypothesized to be sensitive to elevated CO2, as their respiratory protein is often characterised by a pronounced Bohr coeficient (Pörtner, 2002). That is, a small decrease in pH will impair oxygen transport. However, the effects of environmentally-relevant pH reduction on the marine biota are still poorly understood (Seibel and Fabry, 2003). We investigated the impact of short-term hypercapnia (0.1% CO2, up to 24 hours), equivalent to a tripling of pre-industrial levels, on the oxygen consumption rates of juvenile squid, Dosidicus gigas. We also measured massspeciic rates of oxygen consumption under normoxic and normocapnic conditions (MO2; µmoles O2 g-1h-1) in D. gigas. The rates we measured were similar to rates reported for other ommastrephids and to the coastal loliginids (Seibel, 2007). However, they were higher than those of ishes and even mammals (at comparable size and temperature), a fact that relects the low eficiency of jet propulsion relative to other forms of locomotion (Webber and O’Dor, 1986). After acidifying seawater by bubbling an air mix with 0.1% CO2 (the concentration Standard Metabolic Rate (SMR) expected to be attained in the oceans in 100 100 years), the standard (SMR; between 4 Normal CO and 21 µmol h-1 g-1), routine (RMR, between High CO 5 and 26 µmol h-1 g-1) and active (AMR; 10 between 7 and 38 µmol h-1 g-1) metabolic rates (Fig. 1) showed a steady decrease of approximately 10-25% with high CO 2 1 levels. However, these effects were not Routine Metabolic Rate (RMR) signiicant (ANCOVA, P > 0.05). 100 2 O2 consumption (µmol h-1 g-1) 2 Normal CO2 High CO2 10 1 Active Metabolic Rate (AMR) 100 Normal CO2 High CO2 10 1 1 10 100 Weight (g) Figure 1. Effect of high CO2 (0.1%) on standard (SMR), routine (RMR) and active (AMR) metabolic rates of Dosidicus gigas. 11 The lowering of the jumbo squid’s metabolism was also evident by the reduction in the number of intervals of elevated activity (as indicated by peaks in oxygen consumption rate) per hour (Nc h-1) and the scope for activity (AMR/ SMR) (Fig. 2). This short-term sublethal effect (metabolic depression and reduced scope for activity) may have serious impact on its ability to catch prey and escape predators. Blood oxygen binding experiments in other ommastrephid squid demonstrated lowered blood oxygen binding afinity caused by elevated CO2 (Pörtner and Reipschläger, 1996) and on-going enzymatic analysis of octopine production may show a premature switch to anaerobic energy production under these conditions. The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 2.6 30 2.4 25 2.2 2.0 AMR/SMR Nc h-1 20 15 10 1.8 1.6 1.4 1.2 1.0 5 0.8 0 Normal CO2 - 1 High CO2 - 1 Normal CO2 - 2 0.6 High CO2 - 2 Normal CO2 - 1 High CO2 - 1 Normal CO2 - 2 High CO2 - 2 Figure 2. Effect of high CO2 (0.1%) on the number of active cycles per hour (Nc h-1) and scope for activity (AMR/SMR) of Dosidicus gigas. D. gigas undergoes diurnal migrations, spending the daytime in deep, cold and oxygen-depleted water (oxygen minimum layer - OML; 10°C at around 300 m) and migrates at night to shallow, warm (up to 30°C) and oxygenated surface waters. Under the low oxygen conditions of the OML (only a fraction of a kilopascal) in addition to elevated CO2 levels (pH drops to 7.5), D. gigas may reduce total energy expenditure by shutting down expensive cellular processes (e.g. protein synthesis). Although CO2 or pH are common triggers of metabolic suppression, our results indicate that slightly elevated CO2 itself does not cause a substantial metabolic suppression while in the OML. In conclusion, elevated environmental carbon dioxide and the consequent acidiication seemed to interfere with the jumbo squid’s respiratory physiology, which may have cascading and long-term impacts on its ecology. While the effects reported here are subtle, much larger impacts are expected in ongoing studies as carbon dioxide exposure coincides with higher temperatures consistent with D. gigas’ night-time depth distribution. References Caldeira K. and M.E. Wicket. 2003. Anthropogenic carbon and ocean pH. Nature 425: p.365. Pörtner H.O. 2002. Environmental and functional limits to muscular exercise and body size in marine invertebrates athletes. Comparative Biochemistry and Physiology A 133: 303-221. Pörtner H.O. and A. Reipschläger. 1996. Ocean disposal of anthropogenic CO2: physiological effects on tolerant and intolerant animals. p.57-81. In: B. Ormerod and M. Angel (Eds.). Ocean storage of CO2: environmental impacts. MIT and International Energy Agency, Greenhouse Gas R&D Programme, Cheltenham/Boston. Seibel B.A. 2007. On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the class Cephalopoda (Mollusca). Journal of Experimental Biology 210: 1-11. Seibel B.A. and V.J. Fabry. 2003. Marine biotic response to elevated carbon dioxide. Advance in Applied Biodiversity Science 4: 59-67. Webber D.M. and R.K. O’Dor. 1986. Monitoring the metabolic rate and activity of free-swimming squid with telemetered jet pressure. Journal of Experimental Biology 126: 205-224. 12 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Prey size-predator size relationships of squid and their predators in the Northwest Atlantic Michelle D. Staudinger1, Francis Juanes1 and Jason Link2 1 University of Massachusetts Amherst, Department of Natural Resources Conservation, Amherst, MA 01003-9285, USA ([email protected]). 2 National Marine Fisheries Service, Northeast Fisheries Science Center, Woods Hole MA 02543, USA. Quantile regression analysis was used to evaluate absolute and relative body size relationships (BSR) between squid and ten predators in the Northwest Atlantic. Minimum (lower bound), median, and maximum (upper bound) slopes were estimated using scatter plots of absolute body lengths. Relative BSRs were compared using trophic niche breadth, deined as the range of relative prey sizes consumed ontogenetically by a predator (Scharf et al., 2000). Differences in size-based predation on squid were contrasted with predation on ishes to determine if the two prey resources are functionally similar, as has been previously suggested (Packard, 1972). Predator and prey length data were compiled from the National Marine Fisheries Service long-term ecosystem monitoring programme, the Apex Predators programme of the Massachusetts Division of Marine Fisheries, and from several other independent surveys conducted regionally from 1977 to 2004. Atlantic mackerel 10 Bluefish 40 Fourspot flounder 20 15 10 20 5 5 0 0 10 20 30 40 Goosefish 50 0 0 20 60 80 Silver hake 40 40 40 10 20 30 40 50 Smooth dogfish 30 30 20 30 20 20 Prey length (cm) 10 10 10 0 0 0 0 40 80 120 Spiny dogfish 40 0 20 40 40 60 Spotted hake 15 60 80 100 120 140 Summer flounder 40 30 10 20 20 5 0 10 0 0 10 30 50 70 90 0 110 10 20 30 40 50 10 30 50 70 90 Winter skate 30 20 10 0 10 30 50 70 90 Predator length (cm) 110 Figure 1. Relationships between the absolute body sizes of prey and predators: squid prey (dashed lines) and ish prey (solid lines) versus various predators collected in Northwest Atlantic waters. Regression slopes represent the lower (25th, 10th, 5th), median (50th), and upper (75th, 90th, 95th) quantiles (depending on sample size). Individual points of original scatter plots are not shown. 13 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 1.0 1.0 Trophic niche breadth A 0.56 B 0.8 0.8 0.6 0.6 0.35 0.30 0.25 0.20 0.15 0.13 0.2 0.23 0.18 0.15 0.15 0.9 0.15 0.10 0.22 ke r sp Blu el ot ef flo ish u G nd oo e r S se Sm ilv fis e h oo r h th a Sp do ke in gf y i Sp do sh Su o g f m tte ish m d er ha k f W lou e in nd te er rs ka te ac ur m ic nt At la Fo ke r sp Blu el ot ef flo ish u G nd oo e r S se Sm ilv fis e h oo r h th a Sp do ke in gf y i S d sh Su po og f m tte ish m d er ha k f W lou e in nd te er rs ka te ac ur m 0.22 0.0 Fo ic nt 0.28 0.25 0.30 0.2 0.0 At la 0.26 0.4 0.4 Predator species Figure 2. Box plots of relative body size relationships between a) squid b) prey ishes and ten predator species. Noted values indicate mean trophic niche breadth respective to each predator. Box boundaries represent 25th and 75th percentiles, lines within boxes mark the median. Error bars indicate the 90th and 10th percentiles. Circles show outliers in the 5th and 95th percentiles. Upper and lower bound slopes for absolute squid–predator BSRs ranged from negative (i.e. gooseish) to positive (i.e. fourspot lounder) and spanned orders of magnitude among predators (Fig. 1). Squid slopes were less steep in comparison to prey ish slopes; also, total ranges of squid sizes consumed were smaller than ishes. The majority of predators exhibited expanding ranges of prey ish sizes consumed with increasing predator size (all except Atlantic mackerel, smooth and spiny dogish). Conversely, when feeding on squid, the majority of predators (all except fourspot lounder, silver hake, and summer lounder) exhibited no change in range with increasing predator size (lower and upper bound slopes were parallel). Evaluation of relative BSRs revealed that squid occupied narrower trophic niche breadths in comparison to prey ishes for all predators (Fig. 2). Results indicate both the upper limit and total range of size-based predation on squid is more moderate in comparison to prey ishes. Gape limitation has often been cited as a limiting factor in size-based predation. However, for the majority of predators analysed here, other factors are clearly inluencing predator-prey size relationships. Predators were physically capable of consuming broader ranges of squid sizes evidenced by steeper upper bound slopes and broader trophic niche breadths found respective to prey ishes. A greater number of ish species were included in analyses and likely relect a greater range of available prey sizes in comparison to squid. Predator–prey behaviour, predator mobility, and habitat overlap are potential factors inluencing size-based predation on squid and are responsible for the different patterns in prey resource utilisation seen between squid and ishes. Loligo pealeii is the cephalopod that is most frequently found in predator diets in the northwest Atlantic, and a highly-valued commercial resource. Consequently, it is important to assess whether ishers are competing with predators for similar squid resources regionally. Lengths of L. pealeii recovered from the diets of 31 predators, including marine mammals, inishes, elasmobranchs and large pelagics, were compared to the lengths of squid harvested by the commercial ishing industry to evaluate the degree of overlap between squid user groups. A Kolmogorov Smirnov test detected signiicant differences (D = 0.69, p < 0.001) between the lengths of squid consumed by predators and harvested by the ishery (Predator mode = 4 cm, median = 7 cm; Fishery mode = 12 cm, median = 16 cm). 14 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 15 Modepredators Lengths consumed by predators Commercially harvested lengths Relative frequency Meanpredators ModeCommercial 10 MeanCommercial 5 16% 0 0 5 10 R 15 20 25 30 35 40 Mantle length (cm) Figure 3. Relative frequencies of mantle lengths of Loligo pealeii consumed by 31 predators (solid line) and harvested by the commercial ishing industry (dashed line) in the Northwest Atlantic. The overlapping area under the two curves totalled 16%. Arrows point to the mode and mean mantle lengths of the squid consumed by predators and harvested by commercial ishermen. “R” indicates the size (> 8 cm) at which L. pealeii are recruited into the ishery. Commercial data were provided by the National Marine Fisheries Service. The overlapping area under the two curves (Fig. 3) totalled 16% with the greatest peak at 10 cm mantle length. It appears that predators are targeting smaller squid in comparison to the commercial ishing industry. However, many of the predator stocks included in the above analyses have experienced severe age-truncation over recent decades, and data on the largest individuals are scarce. Therefore, as management efforts seek to recover predator populations and increase biomass in larger size classes, it will be important to monitor how size–based predation changes as a result of shifts in predator population size-structure. References Packard A. 1972. Cephalopods and ish: the limits of convergence. Biological Reviews 47: 241-307. Scharf F.S., F. Juanes and R.A. Rountree. 2000. Predator size-prey size relationships of marine ish predators: interspeciic variation and effects of ontogeny and body size on trophic niche breadth. Marine Ecology Progress Series 208: 229-248. 15 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Comparing squid optimal cost of transport speeds to actual ield migrations: new data from 40-g Loligo opalescens John Payne1 and Ron O’Dor2 1 Paciic Ocean Shelf Tracking (POST) Project, 13639 SW 224th St., Vashon, WA 98070, USA ([email protected]). 2 Census of Marine Life Secretariat, Consortium for Oceanographic Research and Education, Suite 420, 1201 New York Avenue NW, Washington, DC 20036, USA ([email protected]). Introduction We took advantage of an extensive array of over 100 acoustic receivers that are used collaboratively for a variety of projects inside Puget Sound, Washington, to monitor the movements of the California market squid, Loligo opalescens. The squid population in the Sound appears to luctuate strongly, and although squid are abundant during some years, there has not been enough stability to support a signiicant commercial ishery. Little is known about what these squid are doing there, or how the Puget Sound population might interact with oceanic populations of the same species. Methods Between 16 September and 14 December 2005, we tagged 35 squid with 9 mm diameter VEMCO V9 coded acoustic tags, using a custom-designed tool to insert the tags into the small mantle cavity (Fig. 1). The V9 tag has been extensively used for tagging salmon smolts by the Paciic Ocean Shelf Tracking (POST) project (Welch et al., 2003). One squid was tagged in northern Puget Sound; 34 others were tagged from a ishing dock on Vashon Island in the middle of the Sound. The Vashon site was desirable because, if squid were migrating out of the Sound, the tags would be detected by the POST project, which maintains curtains of receivers across the Strait of Juan de Fuca and around Vancouver Island. If the squid were migrating into the Sound, they would be detected by an array of receivers operated by the Squaxin Tribe south of the Tacoma Narrows. Figure 1. VEMCO V9 coded tag and tool designed to insert tag into mantle cavity. Results One third of the 34 squid tagged between 16 September 2005 and 14 December 2005 were detected on at least one of the receivers in the Sound (Table 1 and Fig. 2). The predominant direction of movement was south into the Sound over the entire period. Average rates of travel were signiicantly higher to the south than to the north (4.0 vs. 2.5 km/d), suggesting directed movement south, independent of tidal currents. There were no detections outside the Sound, even though the average detected tag continued to be detected for nearly two weeks and one was detected after six weeks. The squid were tracked at up to 6.9 cm/s or 6.0 km/d, and at that speed the maximum range could have been up to 300 km, certainly adequate to take them through the POST curtains, to many other receivers in the north, or for them to be detected by a sizeable array in the inner 16 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Figure 2. Movements of 10 Loligo opalescens in Puget Sound, Washington. All squid, except one further north (See Table 1, Tag 3636), were tagged on Vashon Island (circle) and detected at stationary receivers (stars). The track lines are hand-drawn and represent minimum distances moved. The heavy line shows a route taken by 4 squid. Four receivers (unilled stars) were removed on 27 September when the season for another project ended, illustrating the need for current efforts to co-ordinate and fund receiver arrays in the region as a permanent, shared multi-user system. The bathymetric map was produced by David Finlayson at the University of Washington, Seattle. 122°30’ W 47°30’ N Vashon Island Sound to the south. The tentative conclusion is that the squid are moving deeper into the Sound to breed, as they do in Monterey Bay, California and Bamield, British Columbia. Alternatively, Puget Sound may have a resident population, but it will take many more tags deployed over more of the season and in more areas to conirm this. 1 km It is exciting to have demonstrated a technology to track such small squid, as this will extend the potential for understanding more of the life cycles and migrations of most commercial species. It is also interesting to extend laboratory-ield projections to smaller species. Loligo opalescens was the irst ever squid to swim in a swim-tunnel respirometer (O’Dor, 1982). Larger swim-tunnels have made it possible to directly measure the cost of transport for a range of larger species, and many of them have also been tracked in nature. Figure 3 illustrates that a fairly wide spectrum of commercial squid species undergo extensive migrations, travelling at optimal rates that are predicted from laboratory studies. This could be of great value for understanding the dynamics of squid life cycles, range expansions, and how they are likely to respond to climate change. Table 1. Summary of tracked squid Squid tag no. Mantle length (cm) Release (time, date) Sites (#) Time (d) Distance (km) 3636 12.0 16/09/05 22:45 2 4.86 2.66 S 3634 13.5 26/09/05 00:18 2 5.11 26.39 S 3639 13.0 26/09/05 01:00 1 44.85 17.08 S 3424 14.0 21/10/05 01:47 1 15.82 17.08 S 3693 16.5 23/10/05 22:15 1 3.84 17.08 S 3697 12.0 24/10/05 00:45 4 34.05 23.95 N, S 3691 14.0 26/10/05 23:00 1 4.00 10.83 N 3706 15.0 26/10/05 23:53 1 11.27 11.72 N 3696 14.0 27/10/05 00:28 3 9.84 30.19 S 3705 14.0 27/10/05 01:11 1 8.65 17.08 S 14/12/05 22:47 3 S 3698 13.0 4.94 32.89 Average 13.7 13.39 18.81 Median 14.0 8.65 17.08 Maximum 16.5 44.85 32.89 17 Heading The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Theoretical optimum jet speeds (m s-1) 0.9 y = 1.96x + 0.14 R2 = 0.97 0.8 0.7 Ommstrephid 0.6kg 0.6 Dosidicus 6 kg 0.5 0.4 0.3 Sepioid 0.6 kg Loliginid 0.04 kg Loliginid 0.6 kg 0.2 Nautilus 0.6 kg, no fins 0.1 0 0 0.05 0.1 0.15 0.2 0.25 0.3 0.35 Tracked speeds (m s-1) Figure 3. Theoretical optimum speeds that minimise the cost of transport for cephalopods using jets in tunnel respirometers, compared to actual tracked speeds in nature for species with similar anatomies. O’Dor (2002) found that speeds increased as in size decreased for a series of squid of 0.6 kg mass. Actual maximum tracked speeds are about half of theoretical speeds. The much smaller Loligo opalescens tracked here follow the same trend. Tracking speed is shown for much larger Dosidicus gigas (Gilly et al., 2006), but comparable tunnel respirometry results remain to be completed. The shelled cephalopod, Nautilus, which swims purely by jetting, shows better correspondence than the other cephalopods between theoretical and tracked speeds. Discussion At the tracked speeds, individual L. opalescens and D. gigas could undertake migrations on the order of 500 km and 2500 km, respectively, during the last three months of their lives, independent of currents. Taking advantage of currents, some squid have exhibited further increases to this range (O’Dor, 1992). Although we still understand little of how these two species use this mobility, we now have demonstrated the tools necessary to answer the questions. Clearly, these squid could make extensive migrations to ind areas of high production for feeding and return to natal spawning grounds. Alternatively, although individual life spans are short, the squid could spawn in new areas with appropriate conditions and expand the species range. This capacity to migrate, combined with rapid growth and high reproductive output, gives squid a formidable capacity to adapt to changing conditions, so we should not be surprised that they are increasing their biomass relative to longer lived vertebrates with less adaptable life styles. References Gilly W.F., U. Markaida, C.H. Baxter, B.A. Block, A. Boustany, L. Zeidberg, K. Reisenbichler, B. Robison, G. Bazzino and C. Salinas. 2006. Vertical and horizontal migrations by jumbo squid, Dosidicus gigas, revealed by electronic tagging. Marine Ecology Progress Series 324: 1-17. O’Dor R.K. 1982. The respiratory metabolism and swimming performance of the squid, Loligo opalescens. Canadian Journal of Fisheries and Aquatic Science 39: 580 587. O’Dor R.K. 1992. Big squid in big currents. South African Journal of Marine Science 12: 225-235. O’Dor R.K. 2002. Telemetered cephalopod energetics: swimming, soaring and blimping. Integrative and Comparative Biology 42: 1065-1070. Welch D.W., G.W. Boehlert and B.R. Ward. 2003. POST-the Paciic Ocean salmon tracking project. Oceanologica Acta 25: 243-253. Acknowledgements We gratefully acknowledge David Welch and the POST project for providing us with tags for the research and the following individuals who owned and/or operated the network of receivers on which the squid were detected: Fred Goetz, John Blaine, Scott Steltzner, Barry Berejikian, Skip Tezak, and Correigh Greene. This work is a contribution to the Census of Marine Life. 18 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Fin laps: key adaptation for habitat expansion in the squid, Dosidicus gigas? Ron O’Dor1, Julia Stewart2 and William Gilly2 1 Census of Marine Life Secretariat, Consortium for Oceanographic Research and Education, 1201 New York Ave., Washington, DC 20005, USA ([email protected]). 2 Hopkins Marine Station, Department of Biological Sciences, Stanford University, Paciic Grove, CA 93950, USA. Introduction The Humbolt squid, Dosidicus gigas, appears to have undergone a major range and biomass expansion in recent years. There has been much speculation about whether this has resulted from expansion of suitable habitats as a result of climate change or an increased competitive advantage as a result of decreasing predation or competition associated with declining stocks of large ishes. We suggest here that, regardless of the controlling mechanism(s), D. gigas must be remarkably eficient and adaptable in a wide variety of conditions to make range expansion possible, including the ability to utilise the hypoxic mesopelagic environment known as the oxygen minimum layer. Here we describe a previously unrecognised anatomical feature that may provide another mechanism allowing this squid to be a great generalist, rather than a specialist. Observations Cephalopods are fundamentally jet propelled, although jets are inherently ineficient because of low Froude eficiency (O’Dor, 1988, 2002). Although jetting achieves high accelerations in order to escape from predators and to attack prey, the modern shell-less coleoid cephalopods nearly all supplement their jets with ins of various sorts. These ins develop from three dimensional muscle cell complexes called muscular hydrostats (Kier et al., 1989), producing structures ranging from the fringing ins of neutrally buoyant cuttleish (Kier et al., 1989), to the large and powerful winglike ins used for soaring in currents by Loligo squid (O’Dor et al., 1994), to the much smaller ins of climb-and-glide swimming Illex (Hoar et al., 1994) - both denser than seawater and negatively buoyant. During recent tagging studies in the Sea of Cortez, Mexico, we noted that the ins of Dosidicus, otherwise similar in size and shape to those of Illex, have extremely thin and lexible hydrostat ‘laps’ on the head-ward edge of the in (Fig. 1), equal to about 10% of the in area. We Figure 1. A partially furled in lap on a living Dosidicus gigas of 710 mm mantle length. The watchband is 20 mm wide, for reference. 19 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA have since observed the in laps in action in a variety of existing images and video footage, but have not yet carried out any quantitative analysis. Detailed anatomical studies of the in-laps are currently underway, and Table 1 indicates that the in laps become fully developed only in relatively large specimens. Below about 25 mm mantle length (ML), there is a clear band at the anterior edge of the in that lacks chromatophores, and it does not obviously look like a lap. It is thinner than the rest of the in, but is not folded over when preserved in ethanol. In larger specimens above 50 mm ML, this region is folded over in ethanol preserved specimens and is obviously lap-like. The extreme anterior edge also seems to lack chromatophores in the larger specimens. Table 1. Anatomical measurements (mm) of in laps Dorsal ML (mm) Fin length Fin width Flap width <25.0 - - - 26.2 7.5 7.1 0.4 29.0 9.0 7.5 0.7 30.5 9.7 8.6 0.5 30.0 13.0 8.5 0.6 55.0 19.3 16.5 1.3 50.8 18.2 16.2 1.0 indistinct thin distinct 58.0 18.4 17.1 1.3 350.0 ? ? 8.0 710.0 318.0 209.0 15.0 Interpretation Like the laps and ailerons of airplanes, these squid in-laps can alter swimming performance in many ways: steering, braking, increasing lift, reducing drag, and other more complex effects derived from non-ixed-wing functions. When laps are folded completely, Dosidicus ins can function like Illex ins, minimising drag during long migrations and increasing eficiency by making long downward horizontal glides (O’Dor, 1988). Tunas, which are also negatively buoyant, use this same mechanism to increase migration eficiency. The most obvious use of laps on airplanes is during landing when increasing wing curvature increases lift at low speeds, also a key feature of gliders. Fin-laps would allow Dosidicus to soar in tidal currents around underwater structures like seamounts or canyon walls. These habitats appear to be favoured by this species, and the currents associated with such structures deliver potential prey. Loliginids typically soar with their heads facing into the current, allowing a head-irst interception of prey, although it is not uncommon to see squid in the same school facing in opposite directions. Dosidicus in-laps would seemingly work best for lift if the squid point in-irst into the current. Squid eyes provide a near-360° view, so in-irst orientation would not be a disadvantage for predation. If the laps are folded lat, they cause only a small fraction of the drag of large loliginid ins, so attacks may be faster allowing them to catch larger, faster prey. Illex have been observed to attack larger prey by over-taking them, using faster in-irst jetting, and then dropping back to make a head-irst attack (Foyle and O’Dor, 1988), so there are many possibilities. Video observations make it clear that the laps are also used like ailerons to increase manoeuvrability. It has also been suggested (Tierney Thys, pers. comm.) that the most critical use of the laps may be in escaping predators, not catching prey. Dosidicus have been ilmed lying in air ins irst (Cole and Gilbert, 1970), apparently being chased by predators beneath. Increased lift and control in air could be critical to predator avoidance, as in lyingishes. Maximum speed or acceleration in 20 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA cephalopods is always achieved by jetting ins-irst, and this would be the right orientation for lift. We have re-analysed Gilbert’s original footage, provided by the National Geographic Society, but unfortunately the resolution was inadequate to determine what the in-laps were doing. To the best of our knowledge in-laps have not been described for other squid, so it is important to look for them in other species. Examination of specimens of Sthenoteuthis oualaniensis in our possession reveals the same sort of in-lap structure. This species is most closely related to Dosidicus genetically (our unpublished analysis), but do other ommastrephid species also bear inlaps? Knowing that they exist, it is also important to look at what they are doing in a wide range of circumstances. Observations of Dosidicus in swim-tunnels are now underway, which should help understand some of the quantitative aspects of in-laps. But, footage of them in a variety of natural circumstances is essential to understanding how the laps are used behaviourally to aid one of the ocean’s major predators. References Cole K.S. and D.L. Gilbert. 1970. Jet propulsion of squid. Biological Bulletin 138: 245-246. Foyle T.P. and R.K. O’Dor. 1988. Predatory strategies of squid (Illex illecebrosus) attacking small and large ish. Marine Behaviour and Physiology 13: 155 168. Hoar J., E. Sim, D.M. Webber and R.K. O’Dor. 1994. The role of ins in the competition between squid and ish. p.27-43. In: J. Rayner, Q. Bone and L. Maddock (Eds.). Mechanics and physiology of animal swimming. Cambridge University Press, Cambridge, UK. Kier W.M., K.K. Smith and J.A. Miyan. 1989. Electromography of the in and musculature of the cuttleish Sepia oficinalis. Journal of Experimental Biology 143: 17-31. O’Dor R.K. 1988. The forces acting on swimming squid. Journal of Experimental Biology 137: 421 442. O’Dor R.K. 2002. Telemetered cephalopod energetics: swimming, soaring and blimping. Integrative and Comparative Biology 42: 1065-1070. O’Dor R.K., J.A. Hoar, D.M. Webber, F.G. Carey, S. Tanaka, H. Martins and F.M. Porteiro. 1994. Squid (Loligo forbesi) performance and metabolic rates in nature. Marine Freshwater Behaviour and Physiology 25: 163-177. Acknowledgements This work is a contribution to the Census of Marine Life. 21 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Epiplanktonic squid from the west coast of the Baja California Peninsula, Mexico Jasmín Granados-Amores1, Roxana De Silva-Dávila2 and Martín E. Hernández-Rivas Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Departamento de Plancton y Ecología Marina, Av. IPN, s/n. Apdo. Postal 592, CP 23000, La Paz, BCS, Mexico ([email protected]). 1 PIFI and CONACyT grant recipient, 2EDI and COFAA grant recipient 1 Cephalopods are the most frequently eaten food items of several top predators caught off Baja California and south to the Gulf of Tehuantepec, in the Gulf of California, and at the Revillagigedo Islands. The most important cephalopod taxa recordered in the stomach contents of sailish Istiophorus platypterus, hammerhead shark Sphyrna lewini, yellowin tuna Thunnus albacares, and dolphinish Coryphaena hippurus are: Dosidicus gigas, Abraliopsis afinis, Onychoteuthis banksi, Gonatus spp., Mastigoteuthis, Loligo opalescens, Thysanoteuthis rhombus, Ancistrocheirus lesueuri, Sthenoteuthis oualaniensis, and Argonauta spp. (Galván-Magaña, 1988). In spite of the importance of these mollusks in the trophic web, knowledge of the adult cephalopod communities in waters off Mexico is still incomplete. Identiication of squid early stages that live in the plankton is problematic. Through the identiication of the paralarvae, a better understanding of the reproductive biology of the adults and their life cycles is attainable. This will help to identify spawning areas and to estimate early growth rates of the target species. The objective of our study was to describe the distribution and abundance of the epipelagic squid collected along the west coast of the Baja California Peninsula, Mexico, during the winter and summer of 1998 and 1999, and to obtain some basic information on the community structure in relation to oceanographic processes. The biological material was collected during four oceanographic cruises made from Ensenada, BC to Punta Abreojos, BCS, Mexico, during the winter and summer of 1998 and 1999 by the “Investigaciones Mexicanas de la Corriente de California” (IMECOCAL) programme (Fig. 1). All paralarvae were sorted from the plankton samples collected with standard Bongo net tows (Smith and Richardson, 1979), and were identiied to the lowest possible taxonomic level, according to the criteria of Roper et al. (1984) and Sweeney et al. (1992). Abundance data were standardised based on Kramer et al. (1972). Taxa were grouped by biogeographic afinity of the adults (Roper et al., 1984). 32°N ENSENADA MEXICO GU 30°N LF PUNTA BANDA CA LI BAHIA VICAINO NI R FO Latitude OF 119 28°N A PUNTA EUGENIA PUNTA ABREOJOS 26°N GOLFO DE ULLOA 24°N 118°W 116°W 114°W Longitude Figure 1. Study area and grid sampling stations. 22 112°W The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Squid paralarvae were collected at 122 of the 268 IMECOCAL sampling stations. The specimens were grouped in 8 families, 12 genera, and 29 other taxa. Total squid paralarvae (PL) abundance in the four cruises was 917 PL/1000m3. Three families were the most important, accounting for 84% of the relative abundance of the paralarvae recorded during the four cruises. Paralarvae of the family Onychoteuthidae were the most important, representing 33% of the total abundance, followed by the Cranchiidae (28%), and the Gonatidae (23%). Important differences in PL abundance and number of taxa were found among the 1998 and 1999 cruises. Six more species of the family Ommastrephidae, were previously identiied from the 1998 cruises (Camarillo-Coop, 2006), resulting in a total of 35 epiplanktonic squid taxa in the study area. Durazo and Baumgartner (2002) mentioned that the signal of the El Niño event of 1998 reached its maximum expansion along the west coast of the Baja California Peninsula in July 1997, with unusually warm and salty water. The winter of 1998 was considered a transition period between El Niño and La Niña events. During October 1998 (summer), negative sea surface temperature anomalies established the presence of a La Niña event, which was recorded until August 1999 in our study area. During the winter of 1998, we recorded the paralarvae of temperate, cosmopolitan, and tropical taxa associated to the subarctic and transitional-subtropical water masses along the Baja Peninsula (Fig. 2). During summer 1998, the taxa of cosmopolitan and tropical afinities were less abundant, with taxa of tropical afinity distributed only in the southern, warmer region of our study area. The major presence of subarctic water in these months resulted in an increase of the temperate taxa. During the winter of 1999, we identiied 5 taxa, all of temperate afinity, while in summer 1999, at the end of the La Niña, temperate taxa were dominant but cosmopolitan taxa increased again. In the study area, the afinity of squid PL to water masses has been previously established. Paralarvae of Dosidicus gigas were the most abundant during the 1997-1998 IMECOCAL cruises, followed by those of S. oualaniensis, and the S-D group, which represents spawning events of the mentioned species. These species were associated with the transitional-subtropical water mass, while the temperate species Eucleoteuthis luminosa and Hyaloteuthis pelagica were associated with the subarctic water mass. The S-D group represented spawning events of the irst two species (Camarillo-Coop, 2006). Winter 1998 Cosmopolitan 47% Summer 1998 Tropical 20% Cosmopolitan 20% Temperate 33% Tropical 11% Temperate 69% Winter 1999 Summer 1999 Cosmopolitan 38% Temperate 100% Temperate 62% Figure 2. Relative abundance of squid paralarvae by adult afinity during the winter and summer of 1998 and 1999. 23 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Acknowledgements We would like to acknowledge the research projects from which the samples were taken: CONACyT No. G0041T and CGPI 2005-0673 and the Programa Institucional de Formación de Investigadores (PIFI) from the IPN, and the CONACyT for inancial support. We would also like to thank R. Young and E. Hochberg for their assistance on taxonomy. References Camarillo-Coop S. 2006. Variación espacio-temporal de paralarvas de calamares (Cephalopoda: Ommastrephidae) de importancia comercial en la costa occidental de la península de Baja California. Tesis de Maestría. CICIMAR-IPN. 92pp. Durazo R. and T. Baumgartner. 2002. Evolution of oceanographic conditions off Baja California: 19971999. Progress in Oceanography 54: 7-31. Galván-Magaña F. 1988. Composición y análisis de la dieta del atún aleta amarilla Thunnus albacares en el océano Pacíico Mexicano, durante el período 1984-1985. Tesis de Maestría. CICIMAR-IPN. 96pp. Roper C.F.E., M.J. Sweeney and C.E. Nauen. 1984. FAO Species Catalogue. Vol.3: Cephalopods of the world. FAO Fisheries Synopsis 125: 277pp. Smith P.E. and S.L. Richardson. 1979. Técnicas modelo para prospección de huevos y larvas de peces pelágicos. FAO Fisheries Technical Papers T175 175pp. Sweeney M.J, C.F. E. Roper, K.M. Mangold, M.R. Clarke and S.V. Boletzky. 1992. Larval and juvenile cephalopods: A manual for their identiication. Smithsonian Contributions to Zoology 153: 282pp. 24 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Post-spawning egg-care in the squid, Gonatus onyx: implications for diving mammals Brad A. Seibel Biological Sciences Center, University of Rhode Island, 100 Flagg Road, Kingston, RI 02881, USA ([email protected]). Gonatus is among the most abundant cephalopod genera in the upper layers of the subarctic Paciic and Atlantic Oceans, and falls prey to a variety of birds, ishes and mammals. The bottlenose whale, Hyperoodon ampullatus, for example, is known to feed primarily on Gonatus fabricii and efforts are underway to extend protection of the whale by including squid life history parameters among conservation priorities. However, the life history of gonatid squid is unresolved, in part because of the paucity of scientiic observations at the great depths where spawning is believed to occur. All known squid species die after spawning, leaving the eggs to develop on their own. Here we report direct observations of post-spawning parental egg-care (i.e. brooding) in the squid, Gonatus onyx (Fig. 1). G. onyx were observed between 1500 and 2600 metres depth holding an egg mass in their arms. They ventilated the egg mass and provided protection from predators via active locomotion. Upon extended pursuit they mechanically agitated the egg mass, triggering premature hatching. Figure 1. A female Gonatus onyx brooding an egg mass photographed at 1590 metres depth in Monterey Canyon, as observed by the ROV Tiburon, Monterey Bay Aquarium Research Institute. Gonatus onyx in the California Current, and G. fabricii in the North Atlantic, are both known to undertake an ontogenetic descent to great depths where spawning is believed to occur. Initially, researchers concluded that the eggs must be deposited on the sealoor and left to develop on their own. More recently, however, Seibel et al. (2000) suggested a pelagic egg-brooding behaviour for G. onyx based on indirect evidence, including two mature female squid captured in trawls with dissociated eggs at differing stages of development. Although limited evidence also suggests egg-brooding in other gonatid squid, the idea has remained controversial in the absence of direct observations because some aspects of gonatid life history appeared to run counter to the eggbrooding hypothesis. Most importantly, degeneration of the musculature that occurs at some point following sexual maturation was presumed to render the squid unit for active locomotion and egg protection. However, the present behavioural observations revealed substantial locomotory capacity which degenerates gradually over the entire duration of the egg development period. Temperature and egg size are the primary determinants of developmental rate in cephalopods. Published equations suggest that G. onyx eggs should develop within 3 to 4 months. However, this estimate depends on extrapolation outside the range of sizes and temperatures for which cephalopod development is known, and substantial deviations from predicted values have been documented. The abundance of juveniles of G. onyx in near-surface waters peaks seasonally from 25 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA April through July, suggesting the possibility of a yearly cycle with an egg-development period lasting as long as 6 to 9 months. This estimate is roughly consistent with the present egg collection dates and the relative developmental progress observed, however much more data is required to clearly demonstrate seasonality. Gonatid squid have large lipid stores in the digestive gland suficient to fuel metabolism for a long brooding period. The specimen with undeveloped eggs (437) had a irm digestive gland, while those with well-developed embryos appeared to be more laccid. However, two specimens captured within days of each other carried embryos at apparently different developmental stages, so development is apparently not well synchronised. Seasonality of spawning appears to be more synchronous in G. fabricii populations in the North Atlantic. Juvenile squid were triggered to hatch when pursued persistently by the submersible, presumably a last-resort “escape-hatch” that allows release of potentially viable offspring before they are consumed by a persistent predator. Such behaviour would not be beneicial unless the embryos were able to reach the abundant food supply near the surface, surviving to reproduce. Hatchlings from specimen number 239 survived for as long as 6 weeks in the laboratory without external food sources. These hatchlings appeared to have an extensive internal lipid store that diminished throughout development in the laboratory. These data argue that embryos could hatch at depth and survive to reach the surface, provided that swimming capacity had developed suficiently at the time of hatching. However, senescent gonatid squid have also been observed at the surface, including one unidentiied squid that was releasing hatchlings. The present observations clearly demonstrate active post-spawning egg care by G. onyx. Similar life-history strategies are suspected in other gonatids, as well as other families. Predator avoidance is accomplished by active in beats and jet propulsion via mantle contractions, which appear to decline in intensity as muscle degeneration progresses. Despite retaining some capacity for escape locomotion, the relatively immobile brooding squid at depth may be a major food supply for larger deep-sea predators, including some ishes. More importantly, beak analysis and fatty acid signatures indicate that gonatid squid are a dominant component in the diets of some whales and elephant seals. The upper depth limit of our observations is within the routine diving range of such predators. Thus, brooding squid may provide an easy target for “mesopelagic mammals” and a direct link between deep and shallow biomes. These indings are published (Seibel et al., 2000, 2005) and additional relevant literature is listed below. References Arkhipkin A.I. and H. Bjorke. 1999. Ontogenetic changes in morphometric and reproductive indices of the squid Gonatus fabricii (Oegopsida, Gonatidae) in the Norwegian Sea. Polar Biology 22: 347-365. Bjorke H., K. Hansen and R.C. Sundt. 1997. Egg masses of the squid Gonatus fabricii (Cephalopoda, Gonatidae) caught with pelagic trawl off Northern Norway. Sarsia 82: 149-152. Boletzky S.V. 1994. Embryonic development of cephalopods at low temperatures. Antarctic Science 6: 139-142. Drazen J.C. 2002. Energy budgets and feeding rates of Coryphaenoides acrolepis and C. armatus. Marine Biology 140: 677-686. Hochachka P.W. 1992. Metabolic biochemistry of a mesopelagic mammal. Experentia 48: 570-574. Hooker S.K., H. Whitehead and S. Gowans. 2002. Ecosystem consideration in conservation planning: energy demand of foraging bottlenose whales (Hyperoodon ampullatus) in a marine protected area. Biological Conservation 104: 51-48. Hunt J.C. and B.A. Seibel. 2000. Life history of Gonatus onyx (Cephalopoda): ontogenetic changes in habitat, behavior and physiology. Marine Biology 136: 543-552. 26 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Kristensen T.K. 1983. Gonatus fabricii. p.159-173. In: P.R. Boyle (Ed.). Cephalopod life cycles. Academic Press, London. Laptikhovsky V.V. 1991. A mathematical model to study the duration of embryogenesis for cephalopods. Biologicheskie Nauki 1: 37-48 [in Russian]. Le Boeuf B.J., D.E. Crocker, D.P. Costa, S.B. Blackwell, P.M. Webb and D.S. Houser. 2000. Foraging ecology of northern elephant seals. Ecological Monographs 70(3): 353-382. Nesis K.N. 1997. Gonatid squids in the subarctic north Paciic: ecology, biogeography, niche diversity and role in the ecosystem. Advances in Marine Biology 32: 242-325. Nesis K.N. 1999.The duration of egg incubation in high-latitude and deep-sea cephalopods. Russian Journal of Marine Biology 25: 499-506. Okutani T., T. Kubodera and K. Jefferts. 1988. Diversity, distribution and ecology of gonatid squids in the subarctic Paciic: a review. Bulletin of the Ocean Research Institute, University of Tokyo 26, 159-192. Okutani T., I. Nakamura and K. Seki. 1995. An unusual egg-brooding behavior of an oceanic squid in the Okhotsk Sea. Venus 54: 237-239. Seibel B.A., S.H.D. Haddock and B.H. Robison. 2005. Post-spawning egg-care by a squid. Nature 438: p.929. Seibel B.A., F.G. Hochberg and D.B. Carlini. 2000. Life history of Gonatus onyx (Cephalopoda: Teuthoidea): deep-sea spawning and post-spawning egg care. Marine Biology 137: 519-526. 27 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA CLIMATE IMPACTS How climate change may inluence loliginid squid populations Gretta T. Pecl1, George D. Jackson2 1 Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, Private Bag 49, Hobart 7001, Australia ([email protected]). 2 Institute of Antarctic and Southern Ocean Studies, University of Tasmania, Private Bag 77, Hobart 7001, Australia. By the end of the next century, global mean sea surface temperatures (SSTs) are expected to rise substantially (e.g. 1.4 to 5.8°C; Schneider, 2001). However, climate change may mean more than just temperature rises. Other predictions with potential impacts on squid populations include an increase in extreme events, with more intense El Niño events and more common El Niño like conditions (Easterling et al., 2000). Rises in atmospheric CO2 are also expected, which will cause an increase in surface ocean CO2 concentrations and result in an estimated drop in pH of about 0.4 units, which may inhibit oxygen uptake by squid (Seibel and Fabry, 2003). Abiotic changes in the world’s oceans will also result in concomitant changes in the biotic components. Global warming is expected to increase thermal stratiication of the upper ocean, thereby reducing the upwelling of nutrients and decreasing productivity (Seibel and Fabry, 2003). Indeed, the warming of some oceans has already been accompanied by a 70% decline in zooplankton abundance (Roemmich and McGowan, 1995). Loliginid squid populations inhabit nearshore waters and often reproduce in very shallow benthic habitats. Loliginid squid populations are, therefore, likely to be especially sensitive to global climate change and increases in seawater temperatures. Embryos and hatchlings As temperatures increase, development times of cephalopod eggs decrease (Boletzky, 1994), provided that temperatures do not fall outside thermal tolerance boundaries (Gowland et al., 2002). However, hatchlings emerge quicker under elevated temperatures and there is a negative relationship between incubation temperature and hatchling size (Vidal et al., 2002), so that under warmer temperatures loliginid hatchlings will emerge smaller. Within a single spawning season, Australian southern calamary (Sepioteuthis australis) hatchlings, which emerge at the start of the season (cooler), may be as large as 0.057g, whilst at the end of the spawning season (warmer), hatchlings may be as small as 0.023 g – only 40% of the size of the hatchlings at cooler temperatures (Pecl et al., 2004a). Warming oceans may, therefore, result in a downward shift in the size of squid hatchlings emerging from inshore spawning grounds, unless females compensate by producing larger and fewer eggs. Since growth in juvenile cephalopods is exponential, growth works like compound interest on an investment, and the starting size of the investment is crucial (Fig. 1). For example, a 0.023-g hatchling growing at 10% body weight per day would be 186 g after three months, whereas a 0.057 g hatchling growing at the same rate would be 462 g after the same time period. If elevated temperatures reduced hatchling size to say, 0.01 g, a hatchling of this size growing at 10% would only be 81 g after three months. Adult phase and reproduction Growth rates of squid are generally linked with temperature, with an increase in temperature leading to increased growth rate (Forsythe, 2004). However, as species approach their physiological maximum temperature, increasing temperatures may become metabolically costly. Also, some species that grow slower in warmer waters may be at their physiological limits with respect to temperature, resulting in reduced growth rates (e.g. Loliolus noctiluca; Jackson and Moltschaniwskyj, 2001). 28 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 30 0.02g 0.03g 0.04g 0.05g 0.06g 0.07g Weight (g) 25 20 15 10 5 0 5 15 25 35 45 55 65 75 85 95 Age (days) Figure 1. Hypothetical growth curves representing differential growth of Sepioteuthis australis that hatched at different sizes and grew exponentially at 6% per day for 100 d. With respect to potential changes in loliginid growth rates under a regime of elevated temperatures, several outcomes (not mutually exclusive) are possible. Firstly, if individuals are able to obtain suficient resources of both food and oxygen, see below, growth rates will increase (particularly for males) as will variance in growth rate because, although warmer years may give rise to faster growing squid, slow growers may still be present (Hatield, 2000; Pecl et al., 2004b). However, adult size may not necessarily increase as hatchling size, the starting point, will decrease. Under continued temperature elevation, there will likely come a point where growth rates start to decrease as metabolic costs continue to escalate, and growth potential is subsequently reduced. Secondly, as a function of increased growth rate, it is very likely that the average life-span of squid will decrease (e.g. L. noctiluca; Jackson and Moltschaniwskyj, 2001), and individuals will mature younger and at a smaller size (e.g. Sepioteuthis lessoniana; Jackson and Moltschaniwskyj, 2002). From ieldcollected data (Pecl, 2000; Jackson and Moltschaniwskyj, 2002), we know that individuals that grow through cool conditions will have larger gonads and greater reproductive output compared to their warm water counterparts that have shorter life spans and mature at a smaller size. Warm-water squid will have a greater relative gonad investment, with a higher percentage of their body weight as reproductive tissue. However, in absolute terms, their gonads will weigh less. Energetics Given the rapid digestion rates of squid, and a protein based metabolism that converts food into growth rather than storage, we can expect that, with increasing temperature, there will be a concomitant increase in feeding rates. The increased temperatures will also result in smaller hatchlings and a decrease in time that hatchlings can survive without food. Thus, hatchlings will need more food but will have less time for inding it before facing mortality. Furthermore, increased levels of CO2, resulting in decreased ocean pH, might impair O2 transport in squid. This could ultimately limit scope for activity in squid (Seibel and Fabry, 2003). Population considerations General predictions of the effect of global warming on marine populations include: extension of species geographic range boundaries towards the poles, extinction of local populations along range boundaries, and increasing invasion of weedy and/or highly mobile species, especially where local populations of other species are declining (Hughes, 2000). All these features are likely to be observed in squid populations, especially as squid have been referred to as ‘weeds of the sea’ (Jackson and O’Dor, 2001). Moreover, squid biomass may be affected by the carrying capacity of the changing ecosystem. If productivity decreases, however, the rate of cannibalism within squid populations may increase, which ultimately may reduce biomass if cannibalism levels are high. 29 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA In conclusion, the next 100 years will see over 100 generations of these highly responsive creatures, in comparison to a handful of generations of sharks, tunas, and other larger predators of our oceans. Squid, and cephalopods in general, have the intrinsic lexibility to adapt to climate change - their lifehistory and physiological traits enable them to be opportunists in variable environments (Rodhouse and Nigmatullin, 1996). Additionally, we will not have to wait decades to determine what these effects are. In species for which we have established good baseline data, changes will be immediately obvious, generation by generation, year by year. In contrast, for longer-lived predators it will take decades to establish cause and effect on their life-histories, populations and abundance. Whilst deinite answers to our questions about ocean-scale climate change and the potential impacts on inshore squid population dynamics or isheries biology are impossible, one thing is for certain, and that is, should the oceans warm, the pace of life for this high-speed group will increase even further. References Boletzky S. 1994. Embryonic development of cephalopods at low temperatures. Antarctic Science 6(2): 139-142. Easterling D.R., G.A. Meehal, C. Parmesan, S.A. Changnon, T.R. Karl and L.O. Mearns. 2000. Climate extremes: Observations, modeling, and impacts. Science 289: 2068-2074. Forsythe J.W. 2004. Accounting for the effect of temperature on squid growth in nature: From hypothesis to practice. Marine and Freshwater Research 55: 331-339. Gowland F.C., P. Boyle and L.R. Noble. 2002. Morphological variation provides a method of estimating thermal niche in hatchlings of the squid Loligo forbesi (Mollusca: Cephalopoda). Journal of Zoology 258: 505-513. Hatield E. 2000. Do some like it hot? Temperature as a possible determinant of variability in the growth of the Patagonian squid, Loligo gahi (Cephalopoda: Loliginidae). Fisheries Research 47: 27-40. Hughes L. 2000. Biological consequences of global warming: is the signal already apparent? Trends in Ecology and Evolution 15(2): 56-61. Jackson G.D. and N.A. Moltschaniwskyj. 2001. Temporal variation in growth rates and reproductive parameters in the small near-shore tropical squid Loliolus noctiluca; is cooler better? Marine Ecology Progress Series 218: 167-177. Jackson G.D. and N.A. Moltschaniwskyj. 2002. Spatial and temporal variation in growth rates and maturity in the Indo-Paciic squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae). Marine Biology 140: 747-754. Jackson G.D. and R.K. O’Dor. 2001. Time, space and the ecophysiology of squid growth, life in the fast lane. Vie et Milieu 51(4): 205-215. Pecl G.T. 2000. Comparative life history of tropical and temperate Sepioteuthis squids in Australian waters. PhD Thesis. James Cook University of North Queensland, Australia. Pecl G.T., M.A. Steer and K.E. Hodgson. 2004a. The role of hatchling size in generating the intrinsic size-at-age variability of cephalopods: extending the Forsythe Hypothesis. Marine and Freshwater Research 55: 387-394. Pecl G.T., N.A. Moltschaniwskyj, S. Tracey and A. Jordan. 2004b. Inter-annual plasticity of squid life-history and population structure: Ecological and management implications. Oecologia 139: 515-524. Rodhouse P.G. and C. Nigmatullin. 1996. Role as consumers. Philosophical Transactions of the Royal Society of London, Series B 351: 1003-1022. Roemmich D. and J.A. McGowan. 1995. Climatic warming and the decline of zooplankton in the California Current. Science 267: 1324-1326. Schneider S.H. 2001. What is ‘dangerous’ climate change? Nature 411: 17-19. Seibel B.A. and V.J. Fabry. 2003. Marine biotic response to elevated carbon dioxide. Advances in Applied Biodiversity Science 4: 59-67. Vidal E.A.G., F.P. DiMarco, J.H. Wormorth and P.G. Lee. 2002. Inluence of temperature and food availability on survival, growth and yolk utilization in hatchling squid. Bulletin of Marine Science 71(2): 915-931. 30 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Long-term changes in the stock abundance of neon lying squid, Ommastrephes bartramii, in relation to climate change, the squid ishery, and interspecies interactions in the north Paciic Taro Ichii1, Kedarnath Mahapatra2, Mitsuo Sakai1 and Denzo Inagake1 National Research Institute of Far Seas Fisheries, 2-12-4 Fukuura, Kanazawa-ward, Yokohama-City 236-8648, Japan ([email protected]). 2 Tokai University Frontier Ocean Research Center (T-FORCE), 3-20-1 Orido, Shimizu-ward, Shizuoka-city, Shizuoka 424-8610, Japan. 1 Introduction CPUE (No./ tan) The neon lying squid (Ommastrephes bartramii) is an oceanic squid that occurs worldwide in subtropical and temperate waters. In the North Paciic, this species plays an important role in the pelagic ecosystem and is an international ishery resource with high commercial value. We examined the interannual variation in the stock abundance of the autumn spawning cohort of this species, which was monitored initially by Hokkaido University (1979–1999) and recently by the National Research Institute of Far Seas Fisheries (2001-2006), using research driftnets (Yatsu et al., 2000; Ichii et al., 2006), to understand the effect of climate change, the effect of the large-scale squid driftnet ishery and the effect of interspeciic interactions on the squid stock. 5 4 Effects of climate change Neon flying squid During the period of 1999-2002, climate change, characterised by a northward displacement of the Aleutian Low and a northward shift of the transition zone chlorophyll front (TZCF), occurred (Bograd et al., 2004). This implies a reduced level of primary production in the subtropical frontal zone (STFZ), which corresponds to the spawning ground of the autumn cohort of neon flying squid (Ichii et al., 2004). Correspondingly, we found a lower stock level of the autumn cohort during this period (Fig. 1, period indicated by a pink bar). To understand how the lower stock level may be associated with the climate shift, we compared the extent of the productive autumn spawning ground during the productive STFZ regime (19781998) to that of the less productive STFZ regime (1999-2002). A temporal and spatial reduction in the extent of the productive spawning ground was observed during the latter regime. When the southern extent of the TZCF was weak (i.e. the TZCF was not observed south of 31°N) in winter, the stock level of the autumn cohort was very low. Thus, interannual variation in the position of the TZCF may have important implications for the stock level of the autumn cohort. 3 2 1 0 CPUE (No./ tan) 79 81 83 85 87 89 91 93 95 97 99 01 03 05 5 4 Pacific pomfret 3 2 1 0 CPUE (No./ tan) 79 81 83 85 87 89 91 93 95 97 99 01 03 05 0.5 0.4 Blue shark 0.3 0.2 0.1 0.0 79 81 83 85 87 89 91 93 95 97 99 01 03 05 Year Figure 1. Interannual variation in stocks of the autumn cohort of neon lying squid, large Paciic pomfret, and juvenile blue shark in the North Paciic based on research driftnet catch per unit effort (CPUE, number/tan). Data were obtained by Hokkaido University until 1999 and by the National Research Institute of Far Seas Fisheries from 2001 onward. 31 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Effects of the squid driftnet ishery The stock level of the autumn cohort was low during the period of the large-scale driftnet ishery (1980-1998; Fig.1, period indicated by a brown bar). We assessed whether the stock was adversely affected by this ishery (Ichii et al., 2006). The relative ishing mortality (F/FMSY) derived from the production model was 0.8-1.2, which was close to the appropriate (maximum sustainable yield, MSY) ishing level of 1.0, even during 1987-1990, when catches were large. The proportional escapement (number of squid alive at the end of the ishing season as a proportion of those that would have been alive had there been no ishing) was 18-64%, with an average of 42%, which was close to the management target of 40%, even during this period. Thus, the large-scale driftnet ishery is considered to have been sustainable. Effects of interspeciic interactions The squid driftnet ishery also reduced the stocks of Paciic pomfret (Brama japonica) and blue shark (Prionace glauca) because they were commonly caught in association with neon lying squid. We compared interannual variation in stocks of the autumn squid cohort, large Paciic pomfret, and juvenile blue shark based on the research driftnet data (Fig. 1). After the end of the ishery, the single-aged cohort of neon lying squid increased sharply. Regarding multi-aged species, blue shark stocks increased promptly, whereas Paciic pomfret stocks increased very slowly, even though the latter was more short-lived than the former. Considering that the autumn squid cohort and Paciic pomfret compete with each other ecologically, and they are both the predominant nekton species in the North Paciic ecosystem, it is possible that the autumn squid cohort occupied a trophic niche left unoccupied by the depletion of the Paciic pomfret stocks after the end of the ishery, and hence Paciic pomfret had dificulty reclaiming its former niche. Concluding remarks The autumn cohort of neon lying squid was found to respond quickly to environmental and ecosystem changes caused by climate changes and the large-scale ishery, and may have affected ecologically related species. References Bograd S.J., D.G. Foley, F.B. Schwing, C. Wilson, R.M. Laurs, J.J. Polovina, E.A. Howell and R.E. Brainard. 2004. On the seasonal and interannual migration of the transition zone chlorophyll front. Geophysical Research Letters 31(L17204): doi:10.1029/2004GL020637. Ichii T., K. Mahapatra, H. Okamura, D. Inagake and Y. Okada. 2004. Different body size between the autumn and the winter-spring cohorts of neon lying squid (Ommastrephes bartramii) related to the oceanographic regime in the North Paciic: a hypothesis. Fisheries Oceanography 13: 295-309. Ichii T., K. Mahapatra, H. Okamura and Y. Okada. 2006. Stock assessment of the autumn cohort of neon lying squid (Ommastrephes bartramii) in the North Paciic based on past large-scale high seas driftnet ishery data. Fisheries Research 78: 286-297. Yatsu A., T. Watanabe, J. Mori, K. Nagasawa, Y. Ishida, T. Meguro, Y. Kamei and Y Sakurai. 2000. Interannual variability in stock abundance of the neon lying squid, Ommastrephes bartramii, in the North Paciic Ocean during 1979-1998: impact of driftnet ishing and oceanographic conditions. Fisheries Oceanography 9(2): 163-170. 32 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA How climate change might impact squid populations and the ecosystems: A case study of the Japanese common squid, Todarodes paciicus Yasunori Sakurai Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido 041-8611, Japan ([email protected]). Annual catches of Japanese common squid, Todarodes paciicus, decreased during the cool regime period from the late-1970s to late-1980s, while Japanese sardine, Sardinopsis japonicus, increased exponentially. Squid catch has recently increased after the late-1980s warm regime period. These catch luctuations are similar with those of Jack mackerel, Trachurus japonicus, and the Japanese anchovy, Engraulis japonicus. After 1989, the feeding area of the winter spawning stock of squid expanded to the Oyashio region during summer-autumn. These squid feed on small ish and large zooplankton. It has also been suggested that they feed on juvenile walleye pollock, Theragra chalcogramma, on the Oyashio shelf region during autumn, and might strongly affect pollock recruitment. Todarodes paciicus produces gelatinous, nearly neutrally buoyant egg masses that contain many small eggs. These egg masses are thought to occur within or above the pycnocline at temperatures suitable for egg development. Recently, we estimated from laboratory studies that hatchlings (<1mm ML) will ascend to the surface at temperatures between 18-24°C, especially between 19.5-23°C. After hatching, the paralarvae presumably ascend from the mid layer near the pycnocline to the surface layer above the continental shelf and slope, and are transferred into convergent frontal zones. We used this new reproductive hypothesis to explain the last bi-decadal stock luctuation related to climatic regime shifts (Fig. 1). During the warm regime period after 1989, the inferred spawning areas of the winter spawning group have occurred along the continental edge off the Kyushu Island Offshore High survival of hatchlings: 19.5 - 23°C >18°C >25°C Swim to surface Spawning <24°C <18°C Hatch Egg mass Pycnocline <18°C Continental shelf and slope g nin re m tto Sit o nb fo be w pa s o Figure 1. New schematic view of reproductive processes of Japanese common squid, Todarodes paciicus (modiied from Sakurai et al., 2000). 33 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA and the Nansei Islands, and the inner low of the Kuroshio has transported the hatchlings in the surface layer northeastward along the continental edge from the spawning areas to the nursery areas. However, during the cool regime of the 1980s, when winter wind stress was stronger, air temperature at the sea surface was lower, and mixed layer depth at the spawning grounds was deeper than after 1989, the spawning areas were not connected along the continental edge. We conclude that short- and long-term change of the T. paciicus stock can be explained and predicted by physical parameters such as wind stress, air temperature, SST, and MLD during the spawning period based on this new reproductive hypothesis. Although we cannot forecast climate change, even in the next month or season, we can map the inferred spawning grounds using the SST areas between 18-24°C, especially between 19.5-23°C and within a speciic range of bottom topography (100-500 m depth). Based on this method, we can then monitor the trend of stock luctuation and structural change, such as a seasonal shift of the spawning period related to abrupt changes of the inferred spawning areas. As an example, we present how to monitor the recent seasonal changes of inferred spawning areas and predict the stock condition of the next year’s cohort. Furthermore, we try to predict whether the squid will be extinct or will occupy a marine ecosystem during the 21st century based on the Global Warning Scenario (IPCC, International Panel of Climate Change) using the Earth Simulation System (FRCGC, Frontier Research Center of Global Change, Japan). If we examine the monthly changes of squid distribution (temperature range of distribution: 12-23°C at 50 m depth) and inferred spawning areas in 2005, 2050, and 2099, the northern limit of the squid distribution shifts to the north by 1°/50 yr, and covers the water around Hokkaido Island by 2099. The inferred main spawning grounds also move from the southern Japan Sea and the East China Sea around Tsushima Strait to the East China Sea by 2099. The peak of inferred spawning period shifts from October-February in 2005 to November-March in 2050 and December-April in 2099. References Sakurai Y., H. Kiyofuji, S. Saitoh, T. Goto and Y. Hiyama. 2000. Changes in inferred spawning areas of Todarodes paciicus (Cephalopoda: Ommastrephidae) due to changing environmental conditions. ICES Journal of Marine Science 57: 24-30. 34 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Studies of the jumbo squid (Dosidicus gigas d´Orbigny, 1835) in Mexico: Fishery, ecology and climate C.A. Salinas-Zavala, S. Camarillo-Coop, A. Mejia-Rebollo, R. Rosas-Luis, J. Ramos-Castillejos, R. Ramírez-Rojo, D. Arizmendi, G. Bazzino, N. Dimaté-Velasquez and U. Markaida-Aburto CIBNOR Unidad Sonora, Centenario Norte 53, Col Prados del Centenario, CP 83260, Hermosillo, Sonora, Mexico. Introduction In 2006, the jumbo squid ishery was one of the ive principal isheries in Mexico. Based on 13 years of continuous oficial records, the jumbo squid is ished mostly inside the Gulf of California, while during ENSO events catches have been recorded off the western coast of the Baja California (BC) peninsula. The ishery By analysing the annual landings (Fig. 1), it is possible to reconstruct the history of the ishery. It began as a local artisanal ishery at the beginning of the 1970s. The “artisanal period” was characterised by four years of landings (2000 tonnes) by the artisanal leet, small boats with outboard motors that operated during the summer from ports in Santa Rosalía and Loreto, Baja California Sur (BCS). 40,000 20,000 El Niño 2003-04 La Niña 1999-2000 El Niño 1997-98 El Niño conditions 2005 High abundance period 60,000 Exploring west coast Artisanal period 80,000 Year 35 2007 2004 2001 1998 1995 1992 1989 1986 1983 1980 1977 1974 0 1971 Landings (t) 100,000 No fishing period Japanese exploring 140,000 120,000 La Niña 1988-89 After the federal government negotiated with Asian countries, large companies incorporated squid boats with the technology and capacity to process squid on board (Klett-Traulsen, 1981). This inlux of specialised boats began in February 1980 and culminated in November of the same year with landings of 22,464 t of jumbo squid. In 1981, the catches declined by one-half (11,000 t), and the ishery collapsed in 1982 (Klett-Traulsen, 1996). After seven years of no jumbo squid landings in Mexico, small catches were recorded in 1989 in the state of Sonora, coinciding with a La Niña event (Schwing et al., 2001). Starting in 1990 and lasting until 1993, the Gulf of California experienced a period of anomalous warm SSTs caused by El Niño conditions (US NOAA Climate Prediction Center website, http://www.cpc.noaa.gov/). During these years, the National Fishery Institute conducted exploratory ishing for jumbo squid, and found important quantities on the western coast of the BC peninsula, and 6,500 t were landed in the port of Ensenada BC. The following period in the ishery began in 1994 and has lasted 13 years. Korean companies began operating in the ports of Guaymas, Sonora; Santa Rosalía and Loreto, BCS; and La Reforma, Sinaloa. The Mexican government permitted the installation of foreign-owned processors, but limited catches by Mexicans, and authorised the operation of pangas and shrimp boats adapted for ishing jumbo squid. The landings reached an historical maximum of 117,351 t in 1997, followed closely in 2002. During the 13 years of this stage, the price paid to the ishermen on the beach Figure 1. Historical record of jumbo squid landings in Mexico. The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 4.00 Figure 2. Annual variations in the beach price of jumbo squid in Guaymas, Sonora, Mexico. Shrimp boat Small boat (pangas) 3.50 Average price (Mexican pesos) 3.00 2.50 2.00 1.50 1.00 0.50 0.00 1995 1996 1997 1998 1999 2000 2001 2002 2003 Year increased, then declined (Fig. 2), causing discontent and demotivation. Most of the Mexican squid production is exported as daruma to Korea and Japan, a small amount goes fresh-frozen to the United States, and a smaller amount is exported fresh-frozen to Spain. In the national market, jumbo squid is sold fresh-frozen, as frozen ins and tentacles, and recently as breaded and dried illets. The public consumption of jumbo squid in the northwest of Mexico increased by 36% from 2003 to May 2006. Ecology Given the socioeconomic importance of the jumbo squid ishery in Mexico, it is necessary to increase our knowledge of this species to improve its sustainable management. In 2003, the Jumbo Squid Team of CIBNOR began surveying the population off the west coast of the BC peninsula to describe its ecological role in the pelagic ecosystem inside and outside of the Gulf of California, to determine the diagnostic morphogenetic characteristics of the paralarvae, and to better understand the characteristics of its habitat in Mexican waters and the reason for its latitudinal expansion. One of the irst results of these investigations is a historical time series of the size composition of the landings (Fig. 3; Bazzino et al., submitted). Changes in the size structure of the population during 1995-1997 and 1998-1999 suggest that the occurrence of the 1997-1998 El Niño not only affected the abundance of jumbo squid inside the Gulf of California (Lluch-Cota et al., 1999), but also affected the population structure (Markaida, 2006). Our results indicate strong variability in the population structure inside the Gulf of California, based mainly on the size structure and length of irst maturity. Variability in jumbo squid abundance and population structure seems to be related to the occurrence and intensity of ENSO events. 80 70 100 FEMALES 2004 80 Individuals 60 ML (cm) 2003 50 40 60 40 30 20 20 0 10 1996 1997 1998 1999 2003 2004 J Year 80 M A M J J A Months S O N D Figure 4. Numbers of ommastrephid paralarvae (inset) caught off Santa Rosalía, BCS, Mexico by month during 2003 and 2004. MALES 70 60 ML (cm) F 50 40 30 20 10 1996 1997 1998 1999 Year 2003 2004 Figure 3. Average mantle length of jumbo squid landed in Santa Rosalía, BCS, Mexico. 36 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Station 1 2 3 4 5 6 7 32°N 30°N 4 Date Oct 04 Oct 04 Dec 04 Dec 04 Dec 04 Jun 05 Jun 05 n 9 6 13 2 3 1 2 Figure 5. Sites in Mexico where juvenile Dosidicus gigas were collected. ML average (cm) 7.95 8.58 2.67 1.83 1.81 4.71 2.05 5 28°N Latitude 3 26°N 2 1 7 24°N 6 22°N 118°W 116°W 114°W 112°W 110°W 108°W 106°W Longitude Presence of paralarvae and juveniles in the Gulf of California During 2003 and 2004, we made nocturnal surface hauls with a 60 cm diameter, 505 µm conical net, and collected Rhynchoteuthion paralarvae characteristic of the family Ommastrephidae (Fig. 4). This indicates presumably that Dosidicus gigas spawns in this area. In research cruises inside and outside the Gulf of California, juvenile squid between 1.81-8.58 cm mantle dorsal length (MDL) (Fig. 5) have been collected, which suggests a wide distribution of spawning and nursery grounds. These organisms were preserved in alcohol for future genetic analyses. Presence of paralarvae and adults off the west coast off Baja California 32°N 30°N 30°N 30°N 1 12 121 12 3 5 12 3 1 3 10 25 5 24°N 22°N 1 116°W 114°W 112°W Longitude 110°W 1 4 14 2 5 9 1 1 24°N 2 22°N 118°W 1 1 10 24°N 1 26°N ia 1 rn ifo al 5 fC 1 2 26°N Pacific Ocean fo ul 2 28°N G 1 ia 8 ia 4 12 8 Pacific Ocean rn ifo al 12 2 28°N fC rn ifo al 26°N fC 1 fo ul fo ul Pacific Ocean G 28°N Latitude 32°N Latitude 32°N G Latitude Since 2004, we participated in collecting jumbo squid off the west coast of the BC peninsula, and jumbo squid were caught at all stations during all cruises. In 2005, one side of the bongo net was preserved in ethanol for studies of the morphogenetic identiication of Rhynchoteuthion paralarvae (Fig 6). 22°N 118°W 116°W 114°W 112°W Longitude 110°W 118°W 116°W 114°W 112°W 110°W Longitude Figure 6. Stations off the west coast of Baja California where Rhynchoteuthion paralarvae were collected by the IMECOCAL programme. 37 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Sperm whales Marine mammals Pelagic sharks Large fish Medium fish Small fish Demersal fish Myctophid fish Jumbo squid Euphausiids Importance in the pelagic ecosystem of the Gulf of California Caddy and Rodhouse (1998) proposed that recent increases in cephalopod biomasses can be explained by the reduction of predators. In the Gulf of California, there is evidence that the biomass of jumbo squid has increased in the last decade; but the effect of this increase on other groups of organisms, or the effect of changes in abundance of other groups on the jumbo squid, has not been analysed. For this reason, it is necessary to understand the ecological role of the jumbo squid in the pelagic ecosystem. In this study, we found that the energy transfer in the pelagic ecosystem of the central Gulf of California is topdown, and that the jumbo squid is a key species that maintains the balance of the populations at lower trophic levels, while the jumbo squid population is regulated from above by top predators and the ishery (Fig. 7; Rosas-Luis, 2005). Red crabs Unidentified species Figure 7. Positive effects (black bars) and negative effects (grey bars) imposed by jumbo squid on various components of the pelagic ecosystem, according to an ECOPATH model. Age and growth We compared growth parameters of jumbo squid among two areas, the Gulf of California and the west coast of Baja California (Table 1). The growth curves of the females were signiicantly different among areas, and the rate of growth (K) differed by two orders of magnitude. Nevertheless, the asymptotic length (Y∞) differed of practically 2 cm. For the males, the growth curves were also statistically different, but the K’s were similar and the Y∞ were considerably different, with the Y∞ of the males from the Gulf of California being larger (Mejía-Rebollo, 2006). Table 1. Statistical comparison of growth parameters of jumbo squid sampled off the west coast (WC) of Baja California in 2004 and in the Gulf of California (GC) during 1995-1997 (Markaida, 2004), based on the integral logistic method. N=number of organisms, RSS=Residual Sum of Squares, MCR=Residual squares, *** = highly signiicant, P<0.001 Sex N Parameter RSS MCR Female WC 143 Y∞ = 877.5 K = 0.009536 To = 234.9 1255.39 8.9035 GC 247 Y∞ = 896.1 K = 0.01065 To = 235.0 489250 2005 Male WC 46 Y∞ = 792.1 K = 0.01065 To = 214.3 328.4971 7.465 GC 133 Y∞ = 842.1 K = 0.0116 To = 223.3 236077 1815 38 F (3,385) P 51.50 *** 12.24 *** The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Figure 8. Jumbo squid feeding on red crabs at the surface during the day time. Feeding Preliminary results of feeding studies of jumbo squid conducted during 2004-2005 off the west coast off Baja California are summarised in Table 2. The main components of the diet and their percent composition by weight are shown. During a research cruise on board the BIP XII-CIBNOR, jumbo squid were observed feeding on large numbers of red crabs (Pleuroncodes planipes) on the surface during the day (12:35 pm) at 23°26.84´N and 110°39.84´W (Fig. 8). Nine jumbo squid were collected; eight of them were females in maturity stages 3, 4 and 5 and one was a male in stage 5. The average MDL was 73.9 cm (♀) and 63.0 cm (♂). Table 2. Percent composition by weight of organisms in the diet of jumbo squid collected off the west coast off Baja California 2004 2005 Pleuroncodes planipes Prey 61.45 74.77 Vincingueria spp. 12.71 8.41 Myctophidae 2.78 2.04 Copepoda 10.25 Pteropoda 2.72 0.51 Pisces 0.90 3.56 Octopoda 0.11 0.59 Teuthoidea 2.91 1.78 Unidentiied organic material 1.63 2.21 Others 4.54 6.13 Climate: ENSO-jumbo squid relationships During 1998, the squid leet landed 7,466 t in San Carlos on the west coast of BC and 6,989 t in La Paz, BCS. This was due to the displacement of the jumbo squid outside the Gulf of California. In that year, the squid processors were located in Santa Rosalía, Mulegé, Loreto and Ciudad Constitution. Figure 9 shows that the landings in BCS were almost non-existent during this period, which followed a period with a negative Southern Oscillation Index during 1997-1999. In the winter of 2004-2005, this pattern occurred again, and part of the squid leet moved towards Magdalena Bay, BCS. Movements by the jumbo squid during anomalous climatic events, like ENSO, must be considered by the processors in order to optimise their industrialisation and processing. A longer historical time series of landings is required to understand the relationships between jumbo squid and large-scale events such as the Paciic Decadal Oscillation and climate change. 39 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Multivariate ENSO Index Multivariate ENSO Index 4 3 2 1 0 -1 -2 CPUE kg/boat 96 97 98 99 00 01 02 03 Santa Rosalía 4000 2000 0 96 97 98 99 00 01 02 03 CPUE kg/boat San Lucas 1000 750 500 250 0 96 97 98 99 00 01 02 03 CPUE kg/boat San Bruno 1000 750 500 250 0 96 97 98 99 00 01 02 03 CPUE kg/boat Mulegé 600 450 300 150 0 96 97 98 99 00 01 02 03 CPUE kg/boat Loreto 1500 1000 500 0 96 97 98 99 00 01 02 03 CPUE kg/boat La Paz 1500 1000 500 0 CPUE kg/boat 96 97 98 99 00 01 02 03 El Sargento 600 400 200 0 96 97 98 99 00 01 02 03 CPUE kg/boat La Rivera-Los Frailes 30 20 10 0 96 97 98 99 00 01 02 03 CPUE kg/boat Boca El Palmarito 30 20 10 0 96 97 98 99 00 01 02 03 CPUE kg/boat Bahía Magdalena 2000 1000 0 96 97 98 99 00 01 02 03 CPUE kg/boat La Bocana 6 4 2 0 96 97 98 99 00 01 02 03 CPUE t/boat Punta Eugenia 0.01 0.00 0.00 0.00 96 97 98 99 00 01 02 03 Year Figure 9. Relationship between the Southern Oscillation Index and jumbo squid landings during 1998 in Baja California Sur, Mexico. 40 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA References Bazzino G., C.A. Salinas-Zavala and U. Markaida. submitted. Population structure variability of jumbo squid (Dosidicus gigas) in Santa Rosalía, central Gulf of California. Ciencias Marinas. Klett-Traulsen A. 1981. Estado actual de la pesquería del calamar gigante en el estado de Baja California Sur. Depto. de Pesca (México). Serie Cientíica 21: 1-28. Klett-Traulsen A. 1996. Pesqueria de calamar gigante Dosidicus gigas. p.127-149. In: M. Casas-Valdez and G. Ponce-Diaz (Eds.). Estudio del potencial pesquero y acuícola de Baja California Sur. Vol. I. CIBNOR, La Paz, BCS, México. Lluch-Cota D., D. Lluch-Belda, S. Lluch-Cota, J. López-Martínez, M. Nevárez-Martínez, G. Ponce-Díaz, G. Salinas-Zavala, A. Vega-Velazquez, J.R. Lara-Lara, G. Hammann and J. Morales. 1999. Las pesquerías y El Niño. p.137-178. In: V.O. Magaña-Rueda (Ed.). Los impactos de El Niño en México. DGPC-SG-UNAM-IAI-SEP-CONACYT, México. Markaida U. 2006. Population structure and reproductive biology of jumbo squid Dosidicus gigas from the Gulf of California after the 1997-1998 El Niño event. Fisheries Research 79(1-2): 28-37. Mejía-Rebollo A. 2006. Edad y crecimiento de calamar gigante Dosidicus gigas d’Orbigny, 1835 en la costa occidental de la península de Baja California en el 2004. Tesis de Maestría en Ciencias, CIBNOR, La Paz BCS, Mexico. 110pp. Nevárez-Martínez M.O., G.I. Rivera-Parra, E. Moralez-Bojórquez, J. López-Martínez, D.B. Lluch-Belda, E. Miranda-Mier and C. Cervantes-Valle. 2002. The jumbo squid Dosidicus gigas ishery of the Gulf of California and its relation to environmental variability. In: S. Salinas, J.H. Urban and W.E. Arntz. (Eds.). Extended abstracts of the El Niño Symposium and Workshop. Investigaciones Marinas 30(1): 193-194. Rosas-Luis R. 2005. Importancia del calamar gigante Dosidicus gigas Orbigny, 1835, en la estructura tróica del ecosistema pelágico de la porción central del Golfo de California. Tesis Licenciatura, UABCS, Depto de Ciencias del Mar, La Paz BCS, México, 65pp. Schwing F.B., T. Murphree, L. de Witt and P.M. Green. 2002. The evolution of oceanic and atmospheric anomalies in the northeast Paciic during the El Niño events of 1995-2001. Progress in Oceanography 54: 459-491. 41 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA TROPHIC LINkS Contribution of cephalopod prey to large pelagic ish diet in the central north Atlantic Ocean John Logan1, Rebecca Toppin1, Sean Smith2, Julie Porter2 and Molly Lutcavage1 1 Large Pelagics Research Lab, University of New Hampshire, Durham, NH 03824, USA ([email protected]). 2 St. Andrews Biological Station, Canadian Department of Fisheries and Oceans, St Andrews, NB E5B2L9, Canada. Open ocean ecosystems in the north Atlantic host a broad range of teleost predators, but underlying food web linkages supporting these large pelagic species remain poorly understood. In the 1950s and 1960s, exploratory longline sampling cruises were conducted by the R/Vs Crawford and Delaware of the US Bureau of Commercial Fisheries to identify potential tuna ishing grounds (see Wilson, 1965; Wilson and Bartlett, 1967). Diet components of large pelagic ishes were obtained from these offshore regions (Matthews et al., 1977). In the 1980s, Russian scientists also studied the ecology of offshore squid (Zuev et al., 2002), but much of this work remains untranslated. Despite extensive longline isheries in the central Atlantic, there is a surprising lack of ecological information available for this region. To better understand the trophic ecology of large pelagic species, stomach samples were collected from ish captured during directed longline research cruises in the central north Atlantic in 2001 and 2002 (Lutcavage and Luckhurst, 2001). The cruises were conducted primarily to target and sample bluein tuna (Thunnus thynnus). Longline sets were made in offshore waters over a broad 85°W 80°W 75°W 70°W 65°W 60°W 55°W 50°W 45°W 40°W 35°W latitudinal range, extending from 43°N 54°W to 43°N 48°W (area 2) 50°N and 35°N 58°W to 37°N 52°W (area 1) from June to July 2001 and 45°N 23°N 71°W to 36°N 55°W (area 3) 40°N from May to June 2002 (Fig. 1). Additional sampling legs were 35°N conducted from June to October 2002 by the R/V Shoyo Maru (Satoh 30°N et al., 2004). A total of 83 stomachs were sampled in 2001 from Atlantic 25°N R/V Hamilton Banker swordish (Xiphias gladius) (n = 28), Eagle Eye II start points 20°N white marlin (Tetrapturus albidus; Eagle Eye II end points R/V Delaware 1977 n = 2), blue marlin (Makaira 15°N nigricans; n = 1), albacore tuna (Thunnus alalunga; n = 24), bigeye tuna (Thunnus obesus; n = 14) and yellowin tuna (Thunnus albacares; n = 14). A total of 107 stomachs 35°N were sampled in 2002 from Atlantic 40°N swordfish (n = 47), white marlin 30°N (n = 7), blue marlin (n = 2), longbill spearfish (Tetrapturus pfluegeri; n = 4), dolphinfish (Coryphaena 25°N hippurus; n = 11), albacore tuna 35°N (n = 12), bigeye tuna (n = 6) and 55°W 50°W 70°W 65°W 60°W yellowin tuna (n = 18). No bluein 55°W Figure 1. Longline set sampling locations for 2001 (areas 1 tuna were captured during either and 2) and 2002 (area 3). sampling year. 15 14 13 16 14 15 23 13 8 9 10 24 22 21 11 12 12 17 19 20 10 7 5 11 9 1 2 4 3 8 25 28 26 18 29 2 3 7 1 4 6 42 27 Mean percentage weight (MW%) Mean percentage weight (MW%) The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Cephalopoda Crustacea Teleosts Other 100% 80% 60% 40% 20% 0% 100% 80% 60% 40% Figure 2. Mean percent weight of stomach contents from large pelagic ishes sampled in 2001 in a) area 1 and b) area 2. 20% 0% Albacore Bigeye Swordfish Yellowfin Prey biomass of the large pelagic ishes sampled for 2001 and 2002 consisted mainly of cephalopods and teleost ishes (Figs. 2 and 3). The remaining stomach contents were composed mostly of crustacean prey, including decapod larvae and hyperiid amphipods, as well as trematode and nematode parasites. In 2001, cephalopods dominated the prey biomass for all species sampled in area 1, while teleost prey were more prevalent in area 2. In both areas, cephalopod prey consisted mainly of Ommastrephidae, with Gonatidae, Chiroteuthidae and Histioteuthidae also accounting for high proportions of cephalopod prey biomass in swordish sampled from area 2. Teleost prey were dominated by families Paralepididae in area 1 and Bramidae and Myctophidae in area 2. Other major teleost prey included Triglidae, Alepisauridae, Stromateidae, Scorpaenidae, Carangidae, Balistidae, and Monacanthidae. In 2002, the cephalopod prey of all species sampled consisted almost entirely of Ommastrephidae. Cephalopods were dominant prey items of albacore and bigeye tuna, longbill spearish, and Atlantic swordish. Teleost prey consisted mainly of Alepisauridae and Scombridae for the billishes, while tuna and dolphinish consumed mostly Molidae and Exocoetidae, with ish comprising the largest prey biomass for white marlin, blue marlin, dolphinish, and yellowin tuna. Along these broad ocean transects, the greatest overall prey biomass was comprised of Ommastrephidae, a widely distributed family of fast-swimming squid. Our stomach content results are similar to historical indings, demonstrating major contributions of Ommastrephidae to the diets of large pelagic ishes in the central north Atlantic (Matthews et al., 1977). Based on depth associations identiied by studies using pop-up satellite archival tags (PSAT), Atlantic tunas and billishes forage from the surface to at least 900 m, presumably in pursuit of cephalopod and teleost prey. Stomach samples from deeper-diving pelagic ishes, such as bigeye tuna and swordish, contained the greatest diversity and proportional biomass of cephalopods. More surface-dwelling Teleosts Crustacea Other 80% 60% 40% 20% Ye llo w fin lin W hi te df m ar is h h Sw or ph D ol ar pe ll s Lo ng bi in f fis is h lin ar m Bl ue ge Bi ba co re ye 0% Al Mean percentage weight (MW%) Cephalopoda 100% 43 Figure 3. Mean percent weight of stomach contents from large pelagic ishes sampled in area 3 in 2002. The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Nova Scotia Open Ocean Gulf of Mexico 0 -100 Depth (metres) -200 -300 -400 -500 -600 -700 Archived Depth Real Time Depth -800 15/10/05 04/11/05 24/11/05 14/12/05 03/0106 23/01/06 12/02/06 04/03/06 Figure 4. Depth distributions (m) of an Atlantic bluein tuna (Thunnus thynnus) released with a PSAT off Nova Scotia, Canada in 2005. pelagic ishes contained mostly Ommastrephidae. These preliminary stomach content analyses will be evaluated, along with stable isotope analyses of prey and predator tissues, in order to identify energy sources and trophic linkages in central north Atlantic food webs. Although no bluein tuna were sampled in the 2001-02 cruises, stomach content analyses conducted during the R/V Delaware cruises included mostly ommastrephid squid and teleosts of the families Bramidae and Balistidae (Matthews et al., 1977). A representative example of depth patterns of giant bluein tuna tracked with PSATs in the central north Atlantic (Fig. 4) shows repetitive deep descents that suggest extensive foraging, presumably on bathypelagic cephalopods and ishes (M. Lutcavage, unpubl. data). Given the prominence of cephalopods in large pelagic ish diets, more studies are needed to identify their trophic relationships and distributions in oceanic regions. Acknowledgements We thank the Central North Atlantic Steering Committee, crews of the F/V Hamilton Banker, Atlantic Optimist, and Eagle Eye II, Ben Galuardi, Larry Harris, Cheryl Harary, Piper Bartlett, Jillian Armstrong and 2001-02 cruise chief scientists Scott Heppell, Lisa Natansen, and Mike Musyl. Funding was provided by the US National Marine Fisheries Service and the Canadian Department of Fisheries and Oceans. References Lutcavage M. and B. Luckhurst. 2001. Consensus document: Workshop on the biology of bluein tunas in the mid-Atlantic, 5-7 May 2000, Hamilton, Bermuda. International Commission for the Conservation of Atlantic Tunas Collective Volume of Scientiic Papers 52: 803-808. Matthews F.D., D.M. Damkaer, L.W. Knapp and B.B. Collette. 1977. Food of western North Atlantic tunas (Thunnus) and lancetishes (Alepisaurus). US Department of Commerce NOAA Technical Report NMFS SSRF 706: 19pp. Wilson P. 1965. Cruise report, MV Delaware cruise 65-3, March 30 - April 23, 1965. Pelagic-Oceanic Explorations. May 20, 1965. USFWS Bureau of Commercial Fisheries. Wilson P.C. and M.R. Bartlett. 1967. Inventory of U.S. exploratory longline ishing effort and catch rates for tunas and swordish in the northwestern Atlantic 1957-1965. US Fish and Wildlife Service Special Science Report Fisheries 543: 1-52. Zuev G., C. Nigmatullin, M. Chesalin and K. Nesis. 2002. Main results of long-term worldwide studies on tropical nektonic oceanic squids genus Sthenoteuthis: An overview of the Soviet investigations. Bulletin of Marine Science 71: 1019-1060. 44 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Cephalopod prey of the apex predator guild in the epipelagic eastern Paciic Ocean Felipe Galván-Magaña1*, Robert J. Olson2 , Noemi Bocanegra-Castillo1 and Vanessa G. Alatorre-Ramirez1 Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Apartado Postal 592, La Paz, Baja California Sur, Mexico. 2 Inter-American Tropical Tuna Commission, 8604 La Jolla Shores Drive, La Jolla, California 92037-1508, USA. *COFAA-IPN fellowship 1 The stomach contents of apex predators provide valuable information about the biology of poorlyknown prey species. The distribution and abundance of pelagic cephalopods is not well known, considering the dificulty of catching them with traditional methods. Sharks, tunas, billishes, dolphins, and dolphinishes are known to be important predators of cephalopods in the eastern Paciic Ocean (Perrin et al., 1973; Galván-Magaña et al., 1985, 1989; Abitia-Cardenas et al., 1997, 1998, 1999, 2002; Aguilar-Palomino et al., 1998; Markaida and Sosa-Nishizaki, 1998; Galván-Magaña, 1999; Olson and Galván-Magaña, 2002; Rosas-Alayola et al., 2002). A dificulty in studying cephalopods in the stomach contents of large predators is due to muscle tissue being digested quickly. Often, only the cephalopod mandibles (beaks) are found in stomachs after all the mantle tissue has been digested. The predators sampled for stomach content analysis were caught by tuna purse-seine vessels ishing in the eastern Paciic Ocean (EPO) during two periods, 1992-1994 and 2003-2005 (Fig. 1). The study during 1992-1994 was sponsored by the US National Marine Fisheries Service, and was focused on investigating the relationship between yellowin tuna and dolphins in the EPO. The study during 2003-2005 was sponsored by the Pelagic Fisheries Research Program, University of Hawaii, and the goal was to better understand food web dynamics in the pelagic eastern, central, and western equatorial Paciic based on stable isotopes and diet composition. The cephalopods were identiied to the lowest taxon possible using morphological characteristics of the body and/or the mandibles. Whole cephalopods in an undigested state were identiied from information in Okutani (1980), Roper et al. (1984) and Fischer et al. (1995), and cephalopod mandibles were identiied based on Clarke (1962), Iverson and Pinkas (1971), Wolff (1982, 1984) and Clarke (1986). The cephalopod collections at the Santa Barbara Museum of Natural History and CICIMAR were used to validate the identiications. The frequency of occurrence and numbers of cephalopods found in the stomach contents were recorded by species. 160° 30° 150° 140° 130° 120° 110° 100° 90° 80° 1992-1994 2003-2005 30° 20° 20° 10° 10° 0° 0° 10° 10° 20° 160° 150° 140° 130° 120° 110° 100° 90° 80° Figure 1. Map of set locations where predators were caught and analysed for cephalopod predation in two time periods. 45 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Table 1. Predators caught in tuna purse seine sets in the eastern Paciic Ocean and sampled for stomach contents analysis during two sampling periods Predator Number of samples 1992-1994 2003-2005 Thunnus albacares Yellowin tuna 4831 937 Katsuwonus pelamis Skipjack tuna 1205 310 Thunnus obesus Bigeye tuna 80 82 Euthynnus lineatus Black skipjack 100 37 Auxis spp. Bullet tuna 55 20 Carcharhinus falciformis Silky shark 326 290 4 Carcharhinus longimanus Whitetip shark 30 Carcharhinus spp. Other carcharhinids 84 Sphyma spp. Hammerhead shark 48 4 Isurus oxyrinchus Mako shark 4 2 Prionace glauca Blue shark 2 Alopias spp. Thresher shark Nasolamia velox Whitenose shark Makaira indica Black marlin 25 Makaira mazara Blue marlin 15 Makaira spp. Marlins 18 Tetrapturus audax Striped marlin Istiophorus platypterus Sailish 12 3 2 14 8 1 49 1 Coryphaena spp. Mahi-mahi 545 295 Acanthocybium solandri Wahoo 235 417 Stenella attenuata Spotted dolphin 311 Stenella longirostris Spinner dolphin 209 Delphinus delphis Common dolphin Stenella coeruleoalba Striped dolphin 51 5 Total 8250 2417 A total of 10,667 stomach samples taken from a suite of predators during both sampling periods were analysed for this study (Table 1). Twenty-ive cephalopod genera or species were identiied, based mostly on the beaks. The octopods recorded were: Argonauta nouryi, Argonauta paciica, Argonauta cornutus, Argonauta spp., Japetella diaphana, Octopus rubescens, Tremoctopus violaceus, Alloposus mollis, Vitreledonella richardi, and Vampyroteuthis infernalis. The decapods were: Ancistrocheirus lessueuri, Octopoteuthis deletron, Thysanoteuthis rhombus, Dosidicus gigas, Sthenoteuthis oualaniensis, Onychoteuthis banksii, Pholidoteuthis boschmani, Abraliopsis falco, Abraliopsis afinis, Mastigoteuthis dentata, Mastigoteuthis spp., Loligo opalescens, Loliolopsis diomedeae, Liocranchia reinhardtii and unidentiied loliginids. We compared the cephalopods consumed by the predators grouped in taxonomic categories: sharks, tunas, billishes, dolphinishes, wahoo and dolphins. Our comparisons were based on the frequency of occurrence and number of prey consumed during each sampling period. Cephalopod remains were found in the stomach contents of the tunas, wahoo (Acanthocybium solandri) and rainbow runner (Elagatis bipinnulata) more frequently in the 2003-2005 period than in the 1992-1994 period, while sharks, billishes and dolphinishes consumed cephalopods more frequently in the earlier period than in the later period. The Humboldt squid (Dosidicus gigas), however, was consumed by the tunas, wahoo, rainbow runner, sharks, billishes and dolphinishes more frequently during the 1992-1994 period. D. gigas comprised the greatest proportion, by number, of the total cephalopod predation by the tunas and billishes in the 1992-1994 period, and by the dolphinishes, billishes, 46 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 2003-2005 1992-1994 100% 100% Number of organisms 60% 40% 20% Ancistrocheirus lesueuri Loliginidae Mastigoteuthis dentata Pholidoteuthis boschmai Onychoteuthis banksii Sthenoteuthis oualaniensis Dosidicus gigas Thysanoteuthis rhombus unid. Teuthoidea Japetella diaphana Argonauta spp. Argonauta cornutus Octopus rubescens 80% Number of organisms Mastigoteuthis spp. Abraliopsis falco Onychoteuthis banksii Sthenoteuthis oualaniensis Dosidicus gigas unid. Ommastrephidae Thysanoteuthis rhombus Octopoteuthis deletron unid.Teuthoidea Japetella diaphana Argonauta nouryi Argonauta spp. Octopus rubescens 80% 60% 40% 20% 0% 0% Sharks Tunas Billfishes Dolphins Sharks Tunas Dolphinfishes Wahoo and billfishes Figure 2. Taxonomic composition of the total cephalopod predation, in percent number of organisms, by several predator groups in the 1992-1994 and 2003-2005 studies. and wahoo in the 2003-2005 period (Fig. 2). The sharks ate greater proportions of Sthenoteuthis oualaniensis in the earlier period and Argonauta spp. in the later period. The dolphins ate more Abraliopsis falco than any other cephalopod taxon during 1992-1994 (Fig. 2). We also examined predation on epipelagic versus mesopelagic cephalopods by the various predator groups. Dosidicus gigas, S. oualaniensis, Onychoteuthis banksii and argonautids were the main epipelagic cephalopods and Japetella diaphana and Mastigoteuthis spp. were the main mesopelagic cephalopods consumed by the upper-trophic predators in the EPO. We will expand on this analysis in the near future, by examining the spatial and size-speciic characteristics of cephalopod predation. We consider that large predators are relatively unbiased samplers of the cephalopod fauna compared with nets used to sample nekton. Although cephalopod mandibles often accumulate in the stomach contents, the high frequency of occurrence and number of cephalopods consumed by large predators in the EPO indicate that pelagic squid and octopods are important components of the food web. Pelagic cephalopods are also important prey of birds and marine mammals, and in turn, are important predators of crustaceans and ishes at lower trophic levels (Markaida and Sosa-Nishizaki, 2003). The differences in cephalopod predation by the various predators suggest differences in foraging behaviour and habitat use. The vertical habitat of cephalopods has important implications on their rates of predation. Some cephalopods, such as Argonauta cornuta, A. noury, A. paciicus, Ancistrocheirus lesueuri, Loligo opalescens and Loliolopsis diomedeae occur close to the surface (0-125 m). Cephalopods are known to undertake vertical migrations at night (Clarke and Lu, 1975; Roper and Young, 1975) and this behaviour makes them vulnerable to epipelagic predators when they are closer to the surface. The species that vertically migrate from deep waters (1500 m) to the surface include D. gigas, S. oualaniensis, Pholidoteuthis boschmai, T. rhombus, O. banksii and Alloposis mollis. Other cephalopods vertically migrate from deep waters to mesopelagic waters (2000 - 200 m) and these include A. afinis, A. falco, Mastigoteuthis spp., V. infernalis, Japetella heathi, and V. richardi. Some predators (mainly sharks) are known to forage on cephalopods in deep waters. References Abitia-Cárdenas L.A., F. Galván-Magaña, F.J. Gutierrez-Sanchez, J. Rodriguez-Romero, B. AguilarPalomino and A. Moehl-Hitz. 1999. Diet of blue marlin Makaira mazara off the coast of Cabo San Lucas, Baja California Sur, Mexico. Fisheries Research 44(1): 95-100. Abitia-Cárdenas L.A., F. Galván-Magaña and A. Muhlia-Melo. 1998. Espectro tróico del marlin rayado Tetrapturus audax (Philippi, 1887), en el área de Cabo San Lucas, B.C.S., México. Revista de Biología Marina y Oceanografía 33(2): 277-290. Abitia-Cárdenas L.A., F. Galván-Magaña and J. Rodríguez-Romero. 1997. Food habits and energy values of prey of striped marlin, Tetrapturus audax, off the coast of Mexico. US National Marine Fisheries Service, Fishery Bulletin 95(2): 360-368. 47 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Abitia-Cárdenas L.A., A. Muhlia-Melo, V. Cruz-Escalona and F. Galván-Magaña. 2002. Trophic dynamics and seasonal energetics of striped marlin Tetrapturus audax in the southern Gulf of California, Mexico. Fisheries Research 57(3): 287-295. Aguilar-Palomino B., F. Galván-Magaña, L.A. Abitia-Cárdenas, A.F. Muhlia-Melo and J. RodriguezRomero. 1998. Aspectos alimentarios del dorado Coryphaena hippurus Linnaeus, 1758 en Cabo San Lucas, Baja California Sur, México. Ciencias Marinas 24(3): 253-265. Clarke M.R. 1962. The identiication of cephalopod “beaks” and the relationship between beak size and total body weight. Bulletin of the British Museum (Natural History) Zoology 8(10): 419-480. Clarke M.R. 1986. A handbook for the identiication of cephalopod beaks. Oxford University Press, Oxford. 273pp. Clarke M.R. and C.C. Lu. 1975. Vertical distribution of cephalopods at 18°N 25°W in the North Atlantic. Journal of the Marine Biological Association of the United Kingdom 59(2): 259-276. Fischer W., F. Krupp, W. Schneider, C. Sommer, K.E. Carpenter and V.H. Niem. 1995. Guía FAO para la identiicación de especies para los ines de la pesca. Pacíico centro-oriental. Volumen I. Plantas e invertebrados. FAO, Rome. 646pp. Galván-Magaña F. 1999. Relaciones tróicas ínterespecíicas de la comunidad de depredadores epipelágicos del Océano Paciico oriental. PhD thesis, Centro de Investigación Cientíica y de Educación Superior de Ensenada, Ensenada, Baja California, México. 212pp. Galván-Magaña F., H.J. Nienhuis and A.P. Klimley. 1989. Seasonal abundance and feeding habits of sharks of the lower Gulf of California, Mexico. California Fish and Game 75(2): 74-84. Galván-Magaña F., J. Rodriguez and H.J. Nienhuis. 1985. Cefalópodos, atün aleta amarilla y migración. CIBCASIO Transactions 10: 457-480. Iverson I.L.K. and L. Pinkas. 1971. A pictorial guide to beaks of certain eastern Paciic cephalopods. California Department of Fish and Game Fish Bulletin 152: 83-105. Markaida U. and O. Sosa-Nishizaki. 1998. Food and feeding habits of swordish, Xiphias gladius L., off western Baja California. p.245-259. In: I. Barrett, O. Sosa-Nishizaki and N. Bartoo (Eds.). Biology and isheries of swordish, Xiphias gladius. Papers from the International Symposium on Paciic swordish, Ensenada, Mexico, 11-14 December 1994. NOAA Technical Report NMFS 142. Markaida U. and O. Sosa-Nishizaki. 2003. Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. Journal of the Marine Biological Association of the United Kingdom 83(3): 507-522. Okutani T. 1980. Calamares de las aguas Mexicanas. Breve descripción de los calamares existentes en aguas Mexicanas. Departamento de Pesca, México, 64pp. Olson R.J. and F. Galván-Magaña. 2002. Food habits and consumption rates of common dolphinish (Coryphaena hippurus) in the eastern Paciic Ocean. US National Marine Fisheries Service, Fishery Bulletin 100(2): 279-298. Perrin W.F., R.R. Warner, C.H. Fiscus and D.B. Holts. 1973. Stomach contents of porpoise, Stenella spp., and yellowin tunas, Thunnus albacares, in mixed-species aggregations. US National Marine Fisheries Service, Fishery Bulletin 71(4): 1077-1092. Roper C.F.E., M.J. Sweeney and C.E. Nauen. 1984. FAO Species Catalogue. Vol.3: Cephalopods of the world. FAO Fisheries Synopsis 125: 277pp. Roper C.F.E. and R.E. Young. 1975. Vertical distribution of pelagic cephalopods. Smithsonian Contributions to Zoology 209: 1-51. Rosas-Alayola J., A. Hernández-Herrera, F. Galván-Magaña, A. Abitia-Cárdenas and A.F. Muhlia-Melo. 2002. Diet composition of sailish (Istiophorus platypterus) from the southern Gulf of California, Mexico. Fisheries Research 57(2): 185-195. Wolff C.A. 1982. A beak key for eight eastern tropical Paciic cephalopod species, with relationship between their beak dimensions and size. US National Marine Fisheries Service, Fishery Bulletin 80(2): 357-370. Wolff C.A. 1984. Identiication and estimation of size from the beaks of eighteen species of cephalopods from the Paciic Ocean. NOAA Technical Report NMFS 17: 50pp. 48 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA New information from predator diets on the importance of two Ommastrephidae: Sthenoteuthis oualaniensis in the Indian Ocean and Hyaloteuthis pelagica in the Atlantic Ocean Frédéric Ménard1, Michel Potier2, Evgeny Romanov1, Sébastien Jaquemet3, Richard Sabatié4 and Yves Cherel5 1 Institut de Recherche pour le Développement (IRD), Centre de Recherche Halieutique Méditerranéenne et Tropicale (CRH), BP 171, 34203 Sète Cedex, France ([email protected]). 2 Institut de Recherche pour le Développement (IRD), BP 172, 97492 Ste Clotilde Cedex, France. 3 Laboratoire ECOMAR, Université de la Réunion, BP 7151, 97715 St Denis Messag Cedex 09, France. 4 Laboratoire d’Ecologie Halieutique, Agrocampus-Rennes, 65 rue de Saint Brieuc, CS 84215, 35042 Rennes Cedex, France. 5 CEBC, UPR 1934 du Centre National de la Recherche Scientiique, BP 14, 79360 Villiers en Bois, France. Squid are widely distributed in the open ocean, where they constitute a key group in marine food webs (Rodhouse and White, 1995). They are among the most abundant in number and biomass of nektonic epipelagic organisms, and the large squid of the family Ommastrephidae (e.g. Dosidicus and Illex) support major isheries in both neritic and oceanic waters around the world (Rodhouse, 1997). This commercial importance has made the large ommastrephids the target of many scientiic investigations, and consequently their biology is reasonably well-known (Nigmatullin et al., 2001; Zuyev et al., 2002; Bower and Ichii, 2005; Markaida, 2006). However, the biology and ecological role of the unexploited squid species remain poorly known in many areas of the world ocean. Research cruises devoted to the study of squid are few, and in addition, cephalopods are dificult to collect by nets. Large pelagic ishes (e.g. tunas and tuna-like species), mammals and seabirds can be eficient biological samplers for collecting information on cephalopods, due to their opportunistic feeding behaviour (Cherel and Weimerskirch, 1999; Potier et al., 2007). In addition, cephalopod predators catch larger specimens and a greater diversity of species than sampling gear (Rodhouse, 1990; Cherel et al., 2004). In the stomach contents of large pelagic predators, cephalopod beaks, indigestible hard structures, accumulate over time. The beak morphology allows identiication to species level of most of the accumulated items found in predators’ stomachs (Clarke, 1986; Imber, 1992). Therefore, the description of dietary habits, which allows a better understanding of trophic interactions in the marine ecosystems, can also provide useful information on species composition, distribution, abundance and ecology of cephalopods occurring within the predators’ foraging range. In this note, we illustrate the usefulness of cephalopod predators for describing the importance of Sthenoteuthis oualaniensis (Ommastrephidae) in the pelagic food webs of the western Indian Ocean, and of Hyaloteuthis pelagica (Ommastrephidae) in the Atlantic Ocean. In the Indian Ocean, the biomass of the purpleback squid S. oualaniensis has been estimated to be approximately 2 millions tonnes (Zuyev et al., 1985). In the northern part of the Arabian Sea, its density could reach up to 4-8 tonnes km-2 (Gutsal, 1989), although the population structure of S. oualaniensis is poorly known. Nesis (1993) described three different forms, which differ by anatomy, geographic distribution and period of spawning: (1) the giant form is found exclusively in the Red and Arabian Seas; (2) the dwarf form, with no photophores, inhabits the equatorial waters of the Indian Ocean, and spends most of its life in the upper mixed layers; (3) the third form, characterised by photophores on the mantle, is the most common, and has a wider geographic repartition with a much deeper vertical distribution than the dwarf form. In the equatorial waters surrounding the Seychelle Islands, S. oualaniensis constituted a dominant or a signiicant prey in the diet of swordish and subsurface tunas (yellowin and bigeye) caught 49 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA by a longliner (Potier et al., 2007). S. oualaniensis accounted for 19.1% and 15.9% of the whole reconstituted weight, and contributed 13.3% and 9.0% by number in the diet of yellowin tuna and swordish, respectively (Potier et al., 2007). In Russian studies that have been carried out in the same area, S. oualaniensis represented 26.7% and 15.1% of the total index of relative importance (IRI) in the diet of subsurface yellowin and bigeye tunas (no published data). However, stomach content analyses of tunas caught by surface purse-seine isheries in the same area have shown that S. oualaniensis did not contribute signiicantly to the diets: it represented only 3.2% and 0.1% by number in the diet of yellowin and bigeye tunas (Potier et al., 2004). Such tunas caught by purse seiners occur generally in dense schools at the surface and several studies have shown that these tunas seek out and feed on large concentrations of monospeciic prey (Bard et al., 2002; Ménard and Marchal, 2003; Potier et al., 2004). Once a concentration is detected, feeding involves successive capture of individuals of the same species. Therefore, in the equatorial waters surrounding the Seychelles, we hypothesize that the purpleback squid does not occur in concentrations that are sought out by surface predators during the daylight hours. However, purpleback squid can also undertake diel migration in order to avoid predators chasing at the surface during daytime. The size distribution of the beaks of the purpleback squid found in the stomachs of yellowin tuna and swordish are clearly different (Fig. 1): swordish catch larger specimens than yellowin tuna. Swordish are known to undertake large vertical migrations, enabling them to prey actively at greater depths than yellowin tuna. Therefore, it can be assumed that S. oualaniensis adults, which are fed on by swordish, have a greater vertical range than the juveniles, which are fed on by yellowin tuna. On the other hand, it is possible that the two predators could feed on two forms of S. oualaniensis, each having different size and bathymetric distributions (Nesis, 1993). Russian studies have shown that the importance of the purpleback squid in the diet of large ish predators decreases in the tropical waters around Mauritius (6.2% of the IRI for subsurface yellowin tuna; unpublished data). Furthermore, preliminary studies conducted in the Mozambique Channel have shown that another ommastrephid (Ommastrephes bartrami) has replaced S. oualaniensis in the diet of swordish. However, S. oualaniensis plays a major role in the diet of tropical seabirds breeding on islands in the Mozambique Channel. This prey species contributed 19% by number in the diet of great frigatebirds (Weimerskirch et al., 2004) and 15.4% by reconstituted weight in the diet of the red-tailed tropicbird Phaeton rubricauda (Le Corre et al., 2003). In the diet of the sooty tern Sterna fuscata, S. oualaniensis occurred in 53% of the stomachs sampled on Europa and Glorieuses Islands and was ranked irst by the IRI. On Juan de Nova Island, S. oualaniensis occurred in 33% of the stomachs and ranked third by the IRI (Jaquemet et al., in prep). Figure 1 displays the size distribution of the beaks found in the stomachs of sooty terns. Sooty terns catch the smallest specimens of S. oualaniensis (with mean sizes signiicantly different for the three predators). We suspect that the three forms of S. oualaniensis that were described by Nesis (1993) are found in the Mozambique Channel.. 25 yellowfin 20 swordfish Percentage sooty tern 15 10 5 0 0.4 1.2 2 2.8 3.6 4.4 5.2 6 6.8 LRL (mm) 50 7.6 8.4 9.2 Figure 1. Frequency distribution of lower rostral lengths (LRL) (mm) of the beaks of Sthenoteuthis oualaniensis eaten by yellowfin tuna, sooty tern and swordish in the western Indian Ocean. The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA In a recent study, Cherel et al. (2007) described the importance of the glassy lying squid Hyaloteuthis pelagica, Bosc, 1802 in the diets of large pelagic ishes sampled in the central tropical Atlantic Ocean. H. pelagica is the smallest ommastrephid, reaching a maximum mantle length of only 90 mm (Nesis, 1987). H. pelagica was by far the most important cephalopod prey of the community of large predatory ishes sampled during research cruises in autumn 2000. H. pelagica was a major prey of white marlin (Tetrapturus albidus) and a common food item of albacore (Thunnus alalunga), longbill spearish (T. pluegeri) and sailish (Istiophorus albicans). All ishes fed upon the same size range of H. pelagica, including both juvenile and adult squid, but overall the ishes preyed on squid of different mean sizes: white marlin and longbill spearish fed more on adult squid than did albacore and sailish. The ommastrephid Sthenoteuthis pteropus, usually abundant in the tropical Atlantic Ocean, was surprisingly absent in ish diets in the study of Cherel et al. (2007). The authors hypothesize that S. pteropus was not an important and available nektonic prey organism at the time of sampling. These two examples emphasise the usefulness of marine predators to gain valuable information on the biology and the distribution of their prey. In addition, our studies show that cephalopods constitute a link in the transfer of energy from lower trophic levels (most likely mesozooplankton) to higher trophic levels (including tunas, billishes and swordish). References Bard F-X, B. Kouamé and A. Hervé. 2002. Schools of large yellowin (Thunnus albacares) concentrated by foraging on a monospeciic layer of Cubiceps pauciradiatus, observed in the eastern tropical Atlantic. ICCAT Collective Volume of Scientiic Papers 54: 33-41. Bower J.R. and T. Ichii. 2005. The red lying squid (Ommastrephes bartramii): a review of recent research and the ishery in Japan. Fisheries Research 76: 39-55. Cherel Y., G. Duhamel and N. Gasco. 2004. Cephalopod fauna of subantarctic islands: new information from predators. Marine Ecology Progress Series 266: 143-156. Cherel Y. and H. Weimerskirch. 1999. Spawning cycle of onychoteuthid squids in the southern Indian Ocean: new information from seabird predators. Marine Ecology Progress Series 188: 93-104. Cherel Y., R. Sabatié, M. Potier, F. Marsac and F. Ménard. 2007. New information from ish diets on the importance of glassy lying squid (Hyaloteuthis pelagica) (Teuthoidea: Ommastrephidae) in the epipelagic cephalopod community of the tropical Atlantic Ocean. US National Marine Fisheries Service, Fishery Bulletin 105: 147-152. Clarke M.R. 1986. A handbook for the identiication of cephalopod beaks. Clarendon Press, Oxford, 273pp. Gutsal D.K. 1989. Nektonic oceanic oualaniensis squid of the Arabian Sea and promises of its commercial use. Hydronaut Base, Sevastopol, 23pp. [in Russian]. Imber M.J. 1992. Cephalopods eaten by wandering albatrosses (Diomedea exulans L.) breeding at six circumpolar localities. Journal of the Royal Society of New Zealand 22: 243-263. Jaquemet S., J. Kojadinovic, M. Le Corre, M. Potier, Y. Cherel, P. Bustamante and P. Richard. in prep. Diet and ecological niche of the sooty tern Sterna fuscata in the Mozambique Channel. Le Corre M., Y. Cherel, F. Lagarde, H. Lormée and P. Jouventin. 2003. Seasonal and inter-annual variation in the feeding ecology of a tropical oceanic seabird, the red-tailed tropicbird Phaeton rubricauda. Marine Ecology Progress Series 255: 289-301. Markaida U. 2006. Food and feeding of jumbo squid Dosidicus gigas in the Gulf of California and adjacent waters after the 1997–98 El Niño event. Fisheries Research 79: 16-27. Ménard F. and E. Marchal. 2003. Foraging behaviour of tunas feeding on small schooling Vinciguerria nimbaria in the surface layer of the equatorial Atlantic Ocean. Aquatic Living Resources 16: 231238. 51 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Nesis K.N. 1987. Cephalopods of the world. Squids, cuttleishes, octopuses, and allies. TFH Publishers, Neptune City, NJ, 351pp. Nesis K.N. 1993. Population structure of oceanic ommastrephids, with particular reference to Sthenoteuthis oualaniensis: A review. Recent Advances in Fish Biology 375-383. Nigmatullin C.M., K.N. Nesis and A.I. Arkhipkin. 2001. A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda:Ommastrephidae). Fisheries Research 54: 9-19. Potier M., F. Marsac, Y. Cherel, V. Lucas, R. Sabatié, O. Maury and F. Ménard. 2007. Forage fauna in the diet of three large pelagic ishes (lancetish, swordish and yellowin tuna) in the western equatorial Indian Ocean. Fisheries Research 83: 60-72. Potier M., F. Marsac, V. Lucas, R. Sabatié, J.P. Hallier and F. Ménard. 2004. Feeding partitioning among tuna taken in surface and mid-water layers: the case of yellowin (Thunnus albacares) and bigeye (T. obesus) in the western tropical Indian Ocean. Western Indian Ocean Journal of Marine Science 3: 51-62. Rodhouse P.G. 1990. Cephalopod fauna of the Scotia Sea at South Georgia: potential for commercial exploitation and possible consequences. p.289-298. In: K.R. Kerry and G. Hempel (Eds.). Antarctic ecosystems. Ecological change and conservation. Springer Verlag, Berlin. Rodhouse P.G. 1997. Large and meso-scale distribution of the ommastrephid squid Martialia hyadesi in the Southern Ocean: a synthesis of information relevant to ishery forecasting and management. Korean Journal of Polar Research 8: 145-154. Rodhouse P.G. and M.G. White. 1995. Cephalopods occupy the ecological niche of epipelagic ish in the Antarctic Polar Frontal Zone. Biological Bulletin 189: 77-80. Weimerskirch H., M. Le Corre, S. Jaquemet, M. Potier and F. Marsac. 2004. Foraging strategy of a top predator in tropical waters: great frigatebirds in the Mozambique Channel. Marine Ecology Progress Series 275: 297-308. Zuyev G., Ch.M. Nigmatullin, M. Chesalin and K. Nesis. 2002. Main results of long-term worldwide studies on tropical nektonic oceanic squid genus Sthenoteuthis: an overview of the Soviet investigations. Bulletin of Marine Science 71: 1019-1060. Zuyev G.V., Ch.M. Nigmatullin and V.N. Nicholsky. 1985. Nektonic oceanic squids (genus Sthenoteuthis). Agropromizdat, Moscow. 224pp. [in Russian] 52 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Trophic ecology of jumbo squid Dosidicus gigas in the Gulf of California and adjacent waters Unai Markaida1, Rigo Rosas2, Cesar Salinas2 and William Gilly3 1 Departamento de Aprovechamiento y Manejo de Recursos Acuáticos, El Colegio de la Frontera Sur, Calle 10 No. 264, Col. Centro, CP 24000 Campeche, Mexico ([email protected]). 2 Centro de Investigaciones Biológicas del Noroeste, S.C., Mar Bermejo No. 195, Col. Playa Palo de Santa Rita, Apdo. Postal 128, La Paz, BCS 23090, Mexico. 3 Hopkins Marine Station, Department of Biological Sciences, Stanford University, Paciic Grove,CA 93950, USA. Jumbo squid Dosidicus gigas currently leads world cephalopod catches and is perhaps the most abundant middle-sized predator in the eastern Paciic Ocean. Since 1995, we have analysed the stomach contents of 1,259 jumbo squid from the Gulf of California and adjacent waters in order to discern its trophic role and feeding habits. Hard remains (ish otoliths, squid beaks) were mainly used to identify the prey. Prey %N, %FO and %W were used to quantify the diet. The Guaymas Basin, in the Gulf of California, may be considered the primary habitat for this squid, where they are abundant all year round, supporting >95% of the catches. Large jumbo squid in the basin feed on mesopelagic micronekton, mainly the nyctoepipelagic myctophid Benthosema panamense, and to lesser degree on another lanternish, Triphoturus mexicanus, micronektonic squid A C Guaymas Basin 45-78 cm ML 1995-97 24-42 cm ML 1999 Offshore, Western Baja 2004-2005 20-87 cm ML Benthosema Pterygionteuthis Clio Pleuroncodes Pleuroncodes Carmen & Farallón Basins, 1999 20-40 cm ML B D Topolobampo Loreto Clio Western Baja - Off Magdalena Bay 2000, offshore 24-27 cm ML 2005, inshore 67-79 cm ML Euphausiacea Vinciguerria Merluccius Triphoturus Prionatus Synodus Figure 1. Trophic relations of jumbo squid from the Guaymas Basin in the Gulf of California for A) two different maturing sizes, B) southern basins of Carmen and Farallon, C) squid from western Baja California peninsula in offshore waters and D) off Magdalena Bay in offshore and inshore waters. 53 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA and crustaceans (Markaida and Sosa-Nishizaki, 2003). This pattern was also observed during postEl Niño conditions, when medium-sized squid were found in the Gulf (Markaida, 2006; Fig. 1a). In southern basins of the Gulf, other mesopelagic ishes such as T. mexicanus and Vinciguerria lucetia dominate the diet instead of Benthosema (Fig. 1b). Thus, Dosidicus depends on a little known but important food chain based on annual prey, whose productivity is far larger than their standing stock. Squid diel vertical migrations revealed by our research (Gilly et al., 2006) are consistent with the feeding on this micronektonic assemblage, which is associated with deep scattering and oxygen minimum layers. Research on these prey and their habitat is critical to properly understand large luctuations in squid abundance and changes in their population structure. Off western Baja California, the jumbo squid diet is largely dominated by the pelagic red crab Pleuroncodes planipes. This galatheid is the main grazer and an important prey for most pelagic predators in the area. Thus, Pleuroncodes shortens the pelagic food chain by one step, contributing to a more eficient energy transference (Kashkina and Kashkin, 1994). Secondary prey off western Baja include a much larger diversity of micronektonic myctophids than inside the Gulf, where there is a less-developed oxygen minimum layer (Fig. 1c). Dosidicus caught in inshore waters of western Baja, although still dependant on Pleuroncodes, also feed on neritic ishes, including lizardish and hake (Fig. 1d). This is important to note in the view of recent expansions of the range of this abundant squid. Jumbo squid invasions on the continental shelf may impact on other food chains and on valuable commercial ishes. However, it is unlikely that this kind of prey, whose annual production is smaller than their standing stock, may support large squid abundances for long periods of time. References Gilly W.F., U. Markaida, C.H. Baxter, B.A. Block, A. Boustany, L. Zeidberg, K. Reisenbichler, B. Robison, G. Bazzino and C. Salinas. 2006. Vertical and horizontal migrations by the jumbo squid Dosidicus gigas revealed by electronic tagging. Marine Ecology Progress Series 324: 1-17. Kashkina A.A. and N.I. Kashkin. 1994. Mexican red crab Pleuroncodes planipes Stimpson 1860 (Galatheidae) as an intermediate trophic link in the upwelling ecosystem along the shores of Baja California. Oceanology 33: 502-509. Markaida U. 2006. Food and feeding of jumbo squid Dosidicus gigas in the Gulf of California and adjacent waters after the 1997-98 El Niño event. Fisheries Research 79(1-2): 16-27. Markaida U. and O. Sosa-Nishizaki. 2003. Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. Journal of the Marine Biological Association of the United Kingdom 83(3): 507-522. 54 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA The jumbo squid, Dosidicus gigas, a new groundish predator in the California Current? John C. Field and Kenneth A. Baltz Fisheries Ecology Division, Southwest Fisheries Science Center, National Oceanic and Atmospheric Administration, Santa Cruz, CA 95060, USA ([email protected]). The jumbo squid (Dosidicus gigas) is an important component of subtropical food webs, as both a major predator of forage ishes and an important prey item for tunas, billishes and marine mammals. While the usual range of jumbo squid extends through the coastal and pelagic waters of the eastern tropical Paciic Ocean, and north into the Gulf of California, they have been sporadic visitors in the waters off California over the last century. They were particularly abundant off of central California for several years during the mid 1930s, when they were described as a nuisance to both commercial and recreational ishermen (Croker, 1937). Beginning in the late 1990s, and especially from 20042006, jumbo squid were observed in substantial numbers off California and as far north as Alaska. Signiicant occurrences of these squid have appeared in research surveys along the west coast of the US, in commercial ishing operations, and in the stomachs of California sea lions from the southern California bight. California Commercial Passenger Fishing Vessels have begun targeting these squid for recreational customers since the late 1990s, with particularly high landings off central California during the winter months (January through March) in 2005 and 2006. Animals collected from California waters seem to show growth patterns comparable to animals off of Baja California, with smaller animals in May and June, progressively larger animals during the summer and early autumn, and the largest animals during the winter months. 5.0 bottom trawl crab pot 4.5 salmon fishery hake trawl shrimp trawl sperm whales line, pot coastal sharks toothed whales pinnipeds large flatfish dogfish albacore lingcod sablefish seabirds jumbo squid salmon 4.0 baleen whales skates thornyheads mackerel Trophic level shelf rockfish Pacific hake 3.5 slope rockfish small flatfish 3.0 forage fish benthic fish crustaceans dover sardine jellyfish epibenthic euphausiids 2.0 mesopelagics carnivorous zooplankton pandalid shrimp 2.5 cephalopods infauna copepods microzooplankton amphipods 1.5 1.0 benthic detritus pelagic detritus phytoplankton Figure 1. Food web model of the California Current, with a focus on jumbo squid and their known or suspected predators,including isheries, (in black) and prey items identiied in this study (grey). The estimated trophic level is along the y axis, the height of the boxes is scaled to the log of the standing biomass, and the width of the bars represents biomass lux of prey to predators. 55 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA To evaluate their potential impacts on the food web, particularly on commercially important groundish, we opportunistically collected over 400 stomach samples between 2005 and 2006 at various sites along the California coastline. Stomachs were initially frozen or stored in ethanol, and when processed, contents were weighed and identiied to the lowest taxonomic level possible. As with most cephalopod food-habit studies, prey identiications were made from otoliths, beaks, scales, bones and other hard parts, based on both published guides and reference collections. Additionally, standard lengths (for ishes) and mantle lengths (for cephalopods) were reconstructed based on published and itted regressions against otolith lengths and rostrum lengths, where possible. Estimates of prey weight were then reconstructed from weight-length relationships for those items that were identiiable to species level. Results conirm that Dosidicus are indeed capable of predation on adult groundish, as well as being signiicant predators on a wide range of forage species, as the ten most frequently encountered species or taxonomic groups (in descending order of importance) were Paciic hake (Merluccius productus), northern lampish (Stenobrachius leucopsarus), northern anchovy (Stenobrachius leucopsarus), other jumbo squid, Paciic sardine (Sardinops sagax), blue lanternish (Tarletonbeania crenularis), shortbelly rockish (Sebastes jordani), unidentiied rockish (Sebastes spp.), Euphausiidae, and California headlightish (Diaphus theta). When the average weight of prey items was taken into account, the importance of groundish as prey items increased relative to that of mesopelagic ishes. Approximately 40 additional species or taxonomic groups were also observed. We also used the resulting food habits information in an altered version of an existing ecosystem model of the Northern California Current (Field et al., 2006), to include jumbo squid solely for the purpose of graphically representing their relative trophic role in the California Current food web. Production and consumption rates were taken from Olson and Watters (2003), which in turn were based on Ehrhardt (1991). Together with the food habits data, the model indicates that Dosidicus are signiicant higher-trophic-level predators in the California Current ecosystem, with much of their diet comprised of commercially important groundish and coastal pelagic species (Fig. 1). By contrast, they tend to be prey for many commercially important species in semi-tropical and tropical waters of the Paciic (Olson and Watters, 2003). This is consistent with the widely held notion that jumbo squid are opportunistic predators, capable of feeding on a wide range of prey items throughout the eastern Paciic Ocean. Although the impact on the ecosystem is hard to infer, given the lack of abundance data, the potential impact could be substantial, particularly due to the mismatch of tropical versus temperate life histories. References Croker R.S. 1937. Further notes on the jumbo squid, Dosidicus gigas. California Fish and Game 23: 246-247. Ehrhardt N.M. 1991. Potential impact of a seasonal migratory jumbo squid (Dosidicus gigas) stock on a Gulf of California sardine (Sardinops sagax caerulea) population. Bulletin of Marine Science 49: 325-332. Field J.C., R.C. Francis and K. Aydin. 2006. Top-down modeling and bottom-up dynamics: linking a isheries-based ecosystem model with climate hypotheses in the Northern California Current. Progress in Oceanography 68: 238-270. Olson R.J. and G.M. Watters. 2003. A model of the pelagic ecosystem in the eastern tropical Paciic Ocean. Inter-American Tropical Tuna Commission Bulletin 22: 135-218. 56 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Artisanal catches of jumbo squid, Dosidicus gigas, off Coquimbo, Chile and their relation to environmental variables Enzo Acuña1, Luis Cid2, Juan Carlos Villarroel1 and Manuel Andrade1 1 Area de Pesquerías - Departamento de Biología Marina, Universidad Católica del Norte, Casilla 117, Coquimbo, Chile ([email protected]). 2 Departamento de Estadística, Universidad de Concepción, Concepción, Chile. Introduction The jumbo squid, Dosidicus gigas, is an important cephalopod in the eastern Paciic Ocean. According to Rocha and Vega (2003), D. gigas had been ished sporadically by small-scale and industrial ishing leets in Chile since 1957. Schmiede and Acuña (1992) recorded a large increase in catches in 1992, and suggested that D. gigas could be an interesting potential new resource for the artisinal leet in the zone of Coquimbo. Fernández and Vásquez (1995) analysed the 1991-1994 ishing period, and characterised it as an ephemeral mainly industrial ishery, based primarily on the fact that more than 80% of the landings in 1994 were from factory vessels. The characteristics of the current ishery for D. gigas, during its latest appearance in the zone of Coquimbo, are drastically different from the previous period. Acuña et al. (submitted) analysed the evolution of this ishery from 2001 to 2005, and described the leet, catches, effort, CPUE and some biological parameters during that period. This paper describes some biological parameters of D. gigas and the latest development of the artisanal ishery in the area of Coquimbo during late 2005 and 2006, as well as relationships between the catches and some environmental variables during 2001-2006. Methods The study area was the zone of Coquimbo, between latitudes 29°12’S and 31°00’S. Data on jumbo squid catches were obtained from the oficial ishery statistics of the Chilean National Fisheries Service (SERNAPESCA) and from records of the artisanal ishermen. Data on mantle length (ML, 1 cm precision), weight (1 kg precision) and sex were recorded during 2006. The relative abundance was analysed using the catch per unit of effort (CPUE), with effort deined as a ishing trip with catch, following Leos (1998). To determine if there were causal relationships between the CPUE and environmental factors, the methodology of Pierce and Haugh (1977) was followed, and corrected by the method of Box et al. (1994). 8000 Landings (tonnes) 7000 6000 5000 4000 3000 2000 1000 0 J F MAM J J A S ON D J F MAM J J A S ON D J F MAM J J A S ON D J F MAM J J A S ON D J F MAM J J A S ON D J F MAM J J A S ON D 2001 2002 2003 2004 2005 2006 Year-month Figure 1. Catches/landings of D. gigas in the zone of Coquimbo, 2001-2006, by month and year. 57 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 8000 Landings (tonnes) 7000 6000 5000 4000 3000 2000 1000 0 J F M A M J J A S O N D Month 2001 2002 2003 2004 2005 2006 2003-2006 mean Figure 2. Monthly catches/landings of D. gigas in the zone of Coquimbo during the 2001-2006 period. Results 1) Catches/landings. The jumbo squid catches/landings in the IVth Region increased during the study period, with the greatest catches/landings during 2005 (Fig. 1). These catches/landings were taken mainly during the irst semester, with a maximum in August, decreasing in September and October, and recovering in November (Fig. 2). This decrease seems to be due to the squid migrating offshore for reproduction, at least out of the range of the boats. This feature is more apparent during the 2003-2006 period, when a processing plant was fully operative. During 2006, the catches decreased relative to the previous year, although they were signiicantly greater than those of 2001 to 2003 (Fig. 2). Of the D. gigas catches in the IVth Region during 2001 to 2006, 99.7% were taken by artisanal boats for which D. gigas was the target species, and 98.6% were taken in the zone of Coquimbo. The boats were from the ports of Coquimbo, Guayacán, Guanaqueros and Tongoy. 2) CPUE. The monthly CPUE time series showed an increasing tendency during the study period to a maximum in May-July 2006 (Fig. 3). The CPUE values typically declined toward the end of each year, suggesting a drastic decrease in availability, especially during 2004 and 2005 (Fig. 3). CPUE (ton/number of trips) 3.5 3.0 All Guayacán 2.5 2.0 1.5 1.0 0.5 0.0 J F MA M J J A S ON D J F MA M J J A S ON D J F MA M J J A S ON D J F MA M J J A S ON D J F MA M J J 2002 2003 2004 2005 2006 Figure 3. Monthly time series of catch per unit of effort (CPUE) for the port of Guayacán and for all ports, 2001-2006. 58 Frequency (%) 90 80 70 60 50 40 30 20 10 0 Frequency (%) 90 80 70 60 50 40 30 20 10 0 Frequency (%) 90 80 70 60 50 40 30 20 10 0 Frequency (%) 90 80 70 60 50 40 30 20 10 0 Frequency (%) 90 80 70 60 50 40 30 20 10 0 Frequency (%) 90 80 70 60 50 40 30 20 10 0 Frequency (%) The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 90 80 70 60 50 40 30 20 10 0 10 Frequency (%) Frequency (%) 70 80 90 20 90 80 70 60 50 40 30 20 10 0 30 40 50 60 70 80 90 20 40 50 60 70 80 90 90 80 70 60 50 40 30 20 10 0 20 30 40 50 60 70 80 90 90 80 70 60 50 40 30 20 10 0 20 30 40 50 60 70 80 90 90 80 70 60 50 40 30 20 10 0 20 30 40 50 60 70 80 90 90 80 70 60 50 40 30 20 10 0 20 30 40 50 60 70 80 90 90 80 70 60 50 40 30 20 10 0 August Males n=53 10 20 30 40 50 60 70 80 90 90 80 70 60 50 40 30 20 10 0 10 20 30 40 50 60 70 80 90 90 80 70 60 50 40 30 20 10 0 October Males n=22 10 20 30 40 50 60 70 80 90 90 80 70 60 50 40 30 20 10 0 November Males n=26 10 20 30 40 50 60 70 80 90 100 100 20 30 40 50 60 70 80 90 100 20 30 40 50 60 70 80 90 100 20 30 40 50 60 70 80 90 100 20 30 40 50 60 70 80 90 100 20 30 40 50 60 70 80 90 100 20 30 40 50 60 70 80 90 100 20 30 40 50 60 70 80 90 100 September Females n=40 20 30 40 50 60 70 80 90 100 30 40 50 60 70 80 90 100 40 50 60 70 80 90 100 October Females n=48 10 100 90 August Females n=88 10 100 80 4) Relationship with environmental variables. The apparent relationship between jumbo squid catches and different environmental variables, especially related to El Niño - La Niña, was explored. Two environmental time series were considered as input variables, the sea-surface temperature of the Niño1+2 area (N1+2) and the Southern Oscillation Index (SOI; NOAA, Climate Prediction Center), for the period February 2001 to November 2006. An autoregressive-moving average (ARMA) (1, 2, 4; 1) was itted to the SOI series, and an ARMA (2; 2) to the N1+2 series. The seasonal/annual component was removed from all series, and a linear trend was removed from the catch/ landing series prior to the itting process. The results of the analysis for the SOI indicated a signiicant cross-correlation at 6 months lag, (P = 0.033) (Fig. 5). For the N1+2 input variable, a signiicant cross-correlation at 5 months lag (P = 0.037) was found (Fig. 6). Discussion 10 100 September Males n=14 70 3) Biological aspects. Length-frequency distributions (mantle length, ML) for jumbo squid collected during 2006 showed a size range from 40 to 102 cm, with modes between 63-67 cm in males and 68-72 cm in females (Fig. 4). July Females n=9 10 100 60 June Females n=52 10 100 50 May Females n=87 10 100 40 April Females n=172 10 100 30 March Females n=23 10 100 20 February Females n=101 10 100 90 80 70 60 50 40 30 20 10 0 30 January Females n=56 10 100 July Males n=2 10 Frequency (%) 60 June Males n=23 10 Frequency (%) 50 May Males n=35 10 90 80 70 60 50 40 30 20 10 0 40 April Males n=47 10 90 80 70 60 50 40 30 20 10 0 30 March Males n=7 10 90 80 70 60 50 40 30 20 10 0 20 February Males n=39 10 90 80 70 60 50 40 30 20 10 0 90 80 70 60 50 40 30 20 10 0 January Males n=25 20 November Females n=65 10 20 30 Figure 4. Mantle length percent-frequency distributions in male and female jumbo squid collected during 2006. 59 The fishery for jumbo squid in the zone of Coquimbo during 2001-2006 was primarily an artisanal ishery, in contrast to the 1991-1994 period when an industrial leet was responsible for most of the landings (Fernández and Vásquez, 1995). Taipe et al. (2001) indicated that jumbo squid are most abundant in the oceanic area off Perú (over 20 nm) in the autumn, winter and spring, and disperses out during the summer. This pattern was also very clear in the catch and CPUE time series in the squid ishery off Coquimbo, although the decrease is found in the spring during October. This decrease in availability during the spring in the coastal zone is probably due mainly to the fact that the small artisanal boats can not follow the squid as they migrate offshore (outside 12 nm from the coast). This offshore migration seems to be related to the reproductive cycle of D. gigas in the area of Coquimbo, because large specimens can be caught again one month later (November) within 12 nm of the coast. 0.35 0.4 0.25 0.3 0.15 cross correlation cross correlation The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 0.05 -0.05 -0.15 -0.25 0.2 0.1 0.0 -0.1 -0.2 -0.3 -0.35 -0.4 1 2 3 4 5 6 7 8 9 10 11 12 13 1 lag (months) 2 3 4 5 6 7 8 9 10 11 12 13 lag (months) Figure 5. Cross-correlation function for the SOI input variable and D. gigas catches. The red dashed lines indicate the two standard deviation signiicance limits. Figure 6. Cross-correlation function for the N1+2 input variable and D. gigas catches. The red dashed lines indicate the two standard deviation signiicance limits. The mean catch rate of the artisanal leet off Coquimbo is 3.5 t per trip (up to 7 t per trip), which is higher than those reported by Bojórquez et al. (2001) for the Mexican artisanal leet in the Gulf of California, Mexico, during 1995-1998. On the other hand, Taipe et al. (2001) reported mean catch rates of an industrial leet between 0.7 and 23.8 t per trip off Peru during the 1991-1999 period. The female jumbo squid captured and measured during the 2006 season off Coquimbo were larger than the males, which coincides for specimens captured as bycatch in identiication hauls during acoustic surveys of common hake Merluccius gayi in July-September 2002 (Lillo et al., 2003) and during July-August 2004 (Lillo et al., 2005). According to Nigmatulin et al. (2001) and Arguelles et al. (2001), the specimens captured in our coasts during the study period should be considered mainly part of the “large” jumbo squid group (> 520 mm ML). The length frequency distribution of specimens captured in Mexico, described by Markaida and Nishizaki (2001, 2003) and Markaida et al. (2004), during 1995-1997 period, were signiicantly smaller than the specimens recorded in this study, and in both cases the females were larger than the males. Although the values obtained in the analysis using two environmental time series do not indicate strong evidence of a lagged dependency between the processes, one can conclude the existance of causality, which needs to be studied further. Of interest could be to explore longer time series and to correct for the ishing effort associated with the landings. Acknowledgements This research was partly inanced by Fondo de Investigación Pesquera FIP Project Nº 2005-38. References Acuña E., J.C. Villarroel and M. Andrade. submitted. The jumbo squid (Dosidicus gigas) artisanal ishery in the zone of Coquimbo, Chile, 2001-2005. Fisheries Research. Arguelles J., P.G. Rodhouse, P. Villegas and G. Castillo. 2001. Age growth and population structure of the jumbo lying squid Dosidicus gigas in Peruvian waters. Fisheries Research 54: 51-61. Bojórquez M.E., M.A.C. Mata, M.O.N. Martínez and A.H. Herrera. 2001. Review of stock assessment and ishery biology of Dosidicus gigas in the Gulf of California, Mexico. Fisheries Research 54: 53-94. Box G.E.P., G.M. Jenkins and G.C. Reinsel. 1994. Time Series Analysis. Forecasting and Control. 3rd. Edition. Prentice Hall. Fernández F. and J.A. Vásquez. 1995. La jibia gigante Dosidicus gigas (Orbigny, 1835) en Chile: Análisis de una pesquería efímera. Estudios Oceanologicos 14: 17-21. Leos R.R. 1998. The biological characteristics of the Monterey bay squid and the effect of a two-dayper-week ishing closure. CalCOFI Report 39: 204-211. 60 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Lillo S., J. Olivares, M. Braun, E. Díaz, S. Núñez, A. Saavedra, J. Saavedra and R. Tascheri. 2005. Evaluación hidroacústica de merluza común, año 2004. Informes Técnicos FIP. FIP/IT Nº 2004-09, 395pp. Lillo S., M. Rojas, R. Tascheri, V. Ojeda, J. Olivares, F. Balbontín, R. Bravo, S. Núñez, M. Braun, J. Ortiz, P. Torres, F. Véjar, L. Cubillos and A. Saavedra. 2003. Evaluación hidroacústica de merluza común, año 2002. Informes Técnicos FIP. FIP/IT Nº 2002-03, 379pp. Markaida U., C. Quiñones-Velázquez and O. Sosa-Nishizaki. 2004. Age, growth and maturation of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. Fisheries Research 66: 31-47. Markaida U. and O. Sosa-Nishizaki. 2001. Reproductive biology of jumbo squid Dosidicus gigas in the Gulf of California, 1995-1997. Fisheries Research 54(1): 63-82. Markaida U. and O. Sosa-Nishizaki. 2003. Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. Journal of the Marine Biological Association of the United Kingdom 83(03): 507-522 . Nigmatullin Ch.M., K.N. Nesis and A.I. Arkhipkin. 2001. A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae). Fisheries Research 54: 9-19. Pierce D.A. and L. Haugh. 1977. Causality in temporal systems: characterizations and a survey. Journal of Econometrics 5: 265-293. Rocha F. and M.A. Vega. 2003. Overview of cephalopod isheries in Chilean waters. Fisheries Research 60: 151-159. Schmiede P. and E. Acuña. 1992. Regreso de las jibias (Dosidicus gigas) a Coquimbo. Cartas al Editor. Revista Chilena de Historia Natural 65: 389-390. Taipe A., C. Yamashiro, L. Mariategui, P. Rojas and C. Roque. 2001. Distribution and concentrations of jumbo lying squid (Dosidicus gigas) off the Peruvian coast between 1991 and 1999. Fisheries Research 54: 21-23. 61 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Use of stable isotopes to examine foraging ecology of jumbo squid (Dosidicus gigas) R. Iliana Ruiz-Cooley1 and Unai Markaida2 1 Department of Biology, MSC 3AF, New Mexico State University, P.O. Box 3002, Las Cruces, NM 88003-8001, USA ([email protected]). 2 Departamento de Aprovechamiento y Manejo de Recursos Acuáticos, El Colegio de la Frontera Sur, Calle 10 No. 264, Col. Centro, CP 24000 Campeche, Mexico. Cephalopods are a main prey of many marine predators (including endangered species), and are also voracious predators (Clarke 1983, 1996). Understanding their ecological importance in marine ecosystems has mainly been addressed through the analysis of stomach contents. While such analyses can be quite informative, they have limitations. In this study, we combined stomach content analysis with stable isotope analysis of carbon and nitrogen to investigate the trophic ecology of mesopelagic cephalopods, such as the jumbo squid, Dosidicus gigas. We sampled buccal masses and stomach contents of large and medium-sized jumbo squid from three locations in the Gulf of California over three years (see Ruiz-Cooley et al., 2006). Muscle samples from their main prey were also collected. (a) The relationship between mantle length (ML) and both ∂13C and ∂15N values of both muscle and beaks of the jumbo squid were analysed. The results revealed significant differences and high correlations between ∂13C and ∂15N from muscle and beak samples. An ontogenetic effect in trophic position was observed, which was consistent with results from stomach content analysis. The scaling relationships between the isotopic signatures and squid size were as follows (r2 = 0.73 – 0.9; P<0.001): For carbon: ∂13C (muscle) = -17.01 + 0.035 * Mantle length ∂ C (beak) = -17.95 + 0.035 * Mantle length ∂15N (muscle) = 13.59 + 0.054 * Mantle length ∂ N (beak) = 9.039 + 0.068 * Mantle length 13 For nitrogen: 15 There was an allometric relationship (slope signiicantly different from 1.0) between N-isotopic values and squid size, but only a marginally signiicant relationship (P = 0.06) between C-isotopic values and squid size (Fig. 1). (b) A comparison of squid tissues revealed that muscle isotopic values were higher than those of beaks by approximately 1‰ for ∂13C and 3.5- 4.0‰ for ∂15N. This C and N-isotopic difference was consistent among all D. gigas collected in different years and locations. Therefore, we derived the following equations to estimate C and N isotopic values of muscle using the isotopic signature of beaks: ∂13C (muscle) = - 2.30 + 0.81 ∂13C (beak) ∂15N (muscle) = 7.76 + 0.68 ∂15N (beak) An open question is whether squid beaks collected from the digestive tracks of their predators can be used to evaluate trophic relationships. We tested this proposition by measuring the C and Nisotopic values of jumbo squid beaks collected from a stomach of a stranded sperm whale, and then comparing these values to the isotopic signatures of D. gigas muscle and sperm whale skin (data from Ruiz-Cooley et al., 2004). We conirmed viability of this method, at least for jumbo squid in the Gulf of California. More research is needed to investigate the fractionation among squid beak and muscle in other areas. 62 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA -13.5 19 -14.0 R2=0.82 18 R2=0.83 ∂13C in muscle ∂15N in muscle -14.5 17 16 15 -15.0 -15.5 -16.0 -16.5 14 -17.0 13 -17.5 9 10 11 12 13 14 15 -18 ∂15N in beak -17 -16 -15 -14 ∂13C in beak Figure 1. Allometric relationships between stable isotope signatures of beak and muscle tissues of Dosidicus gigas. (a) The ∂15N values exhibited signiicant allometry (p = 0.002), while (b) the ∂13C values were marginally signiicant (p = 0.06). Finally, we compared stomach content analysis versus stable isotope analysis in evaluating squid trophic relationships. Both methods indicated that larger-sized maturing squid showed a higher trophic position than did medium-sized individuals. However, some discrepancies between stomach contents analysis and stable isotope analysis were found. The discrepancies were likely the result of differences between analyses in their respective time frames: stomach content analysis gives an instantaneous estimate of diet, while stable isotope analysis gives an estimate integrated over several weeks. We recommend that tissue samples of prey and predators be collected at the same time and area for a more precise isotopic analysis. References Clarke M.R. 1983. Cephalopod biomass-estimation from predation. p.221-237. In: P.R. Boyle (Ed.). Cephalopod life cycles. Vol. 2. Comparative reviews. Academic Press, London. Clarke, M.R. 1996. Cephalopods as prey. III. Cetaceans. Philosophical Transactions of the Royal Society of London, Series B 351(1343): 1053-1065. Ruiz-Cooley R.I., D. Gendron, S. Aguiñiga, S. Mesnick and J.D. Carriquiry. 2004. Trophic relationships between sperm whales and jumbo squid using stable isotope of C and N. Marine Ecology Progress Series 277: 275-283. Ruiz-Cooley R.I., U. Markaida, D. Gendron and S. Aguiñiga. 2006. Stable isotopes in jumbo squid (Dosidicus gigas) beaks to estimate its trophic position: comparison between stomach content and stable isotopes. Journal of the Marine Biological Association of the United Kingdom 86: 437-445. 63 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Signature fatty acids: a robust method for evaluating trophic relationships in open ocean ecosystems Charles F. Phleger1,3, Jock W. Young2, Michaela Guest4, Matt Lansdell2 and Peter D. Nichols2,3 San Diego State University, 5500 Campanile Drive, San Diego, CA 92128 USA ([email protected]). 2 CSIRO, Division of Marine and Atmospheric Research, GPO Box 1538, Hobart, TAS 7001, Australia. 3 Antarctic and Climate Ecosystems Cooperative Research Centre, University of Tasmania, GPO Box 252-80, Hobart, TAS 7001, Australia. 4 Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, Marine Research Laboratories, Nubeena Crescent, Taroona, TAS 7053, Australia. 1 Introduction One of the main objectives of CLIOTOP Working Group 3 (Trophic pathways in open ocean ecosystems) is to gather suficient information on trophic relations of ocean top predators to enable comparisons of the trophic links in the three major oceans. Stomach-content analysis is a traditional means by which trophic relationships may be examined. This approach is limited however, by the absence and/or rapid digestion of food items in the consumers’ stomach, particularly for purseseine caught predators, and provides only a snapshot of daily feeding. Furthermore, the scarcity of studies in the main tropical and temperate oceans (e.g. Indian Ocean) has restricted comparisons between open ocean systems. Therefore, techniques that can provide detailed prey information from the tissues of the predator would greatly contribute to our understanding of trophic connections within and between oceans. Signature fatty acids are showing promise in this area, as once the lipid proiles of a particular prey group are identiied they can be used to help elucidate the feeding history of the predator, allowing broad comparisons from relatively few data (Bradshaw et al., 2003; Lea et al., 2002; Phillips et al., 2001; Phleger et al., 2005). Here we report on a pilot study, using signature fatty acids, that examines the contribution of oceanic cephalopods to the diet of broadbill swordish (Xiphias gladius) captured off eastern Australia between July 2004 and August 2006. Methods The diet of wild-caught swordish from eastern Australia was examined through signature fatty acid analysis of swordish and a range of key prey species, with an emphasis on squid and myctophid ishes. Muscle tissue was collected from swordish (size range 89-203 cm orbit to fork length) from waters off eastern Australia (Young et al., 2006). Samples were extracted and the fatty acids were prepared and analysed by gas chromatography (GC) and GC-mass spectrometry using methods described in Phillips et al. (2001) and Phleger et al. (2005). The fatty acid compositions (%) comprising 61 fatty acids detected in all species were compared using non-metric multidimensional scaling (MDS) with a Bray-Curtis similarity coeficient (Clark and Gorley, 2006). Results Lipid content was moderate in most squid prey (4-10% of dry weight), fish prey (7-9%) and myctophids (6-10%). In contrast, swordish muscle contained high levels of lipid, 24-42% of dry weight. Levels of DHA (docosahexaenoic acid, 22:6 n-3), a highly reactive PUFA (polyunsaturated fatty acid), when compared in squid from swordish stomachs, fresh frozen samples, and specimens left at 20°C for 24 hours, were unaffected (Fig. 1). This comparison conirmed the robustness of the signature fatty acid approach, and indicated that stomach-content samples and material not frozen 64 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Squid preservation trial: DHA / 16:0 1.8 Fresh, frozen samples & 24 hours at 20°C Stomach samples Fresh & frozen samples 1.6 Ratio DHA / 16:0 1.4 1.2 1.0 0.8 0.6 Figure 1. Comparison of the ratio of DHA/16:0 for squid (Sthenoteuthis oualaniensis) samples collected and preserved using different procedures. 0.4 0.2 0.0 1 3 78 79 80 81 82 83 84 85 86 87 Sample immediately can still be used when fresh-frozen samples are not available. DHA levels from muscle and skeletal samples dissected from different locations in a whole swordish also did not show major differences (unpublished data). Whilst sampling from a standardised location along the ish would be the preferred option, where logistic constraints exist and prevent such an approach, these indings also demonstrate that samples from different lesh locations are generally comparable. Principal fatty acids differed substantially among 24 squid (for example, 34.8% DHA, 10.7% EPA [eicosapentaenoic acid, 20:5 n-3]; Fig. 2) and 20 swordish (9.7% DHA and 2.0% EPA). Myctophids (40 ish) contained on average 20% DHA and 4.9% EPA, similar to ive other ish prey species with 17% DHA and 4.6% EPA. Ordination using multi-dimensional scaling (MDS) indicated that swordish were trophically more closely related to myctophid ishes (ive species) and other ish prey (Cubiceps baxteri, C. pauciradiatus and Sudis atrox) than to seven squid prey species (Fig. 3). Myctophids, particularly Diaphus termophilus and Ceratoscopelus warmingii, were also separated by MDS indicating different diets among these prey species. Squid prey species, such as Sthenoteuthis oualaniensis, Ommastrephes bartramii, Eucleoteuthis luminosa and others displayed close trophic afinity, whereas Argonauta nodosa and Todaropsis eblanae were separated by MDS. Stress: 0.09 s sp . m tra r ba sa do no a os in e na la eb us ph re t as m hi ut ite ch m a ut na go Ar O Ar m lu . sp i is ns ie an al ou s i th is is s i ps u te eo h ut te th eu ro da To cl Eu ro hi C ot en St 65 Figure 2. Scatter plot of multidimensional scaling (MDS) for fatty acid data (expressed as percent of total fatty acids) of squid. Axis scales are arbitrary in non-metric MDS and are therefore omitted. The data are not transformed or standardised and a Bray Curtis similarity matrix is used. The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Stress: 0.06 Swordfish trophic relationships Squid Other fish Myctophids Swordfish Figure 3. Scatter plot of multidimensional scaling (MDS) for fatty acid data (expressed as percent of total fatty acids) of swordfish and potential prey items. Axis scales are arbitrary in non-metric MDS and are therefore omitted. The data are not transformed or standardised and a Bray Curtis similarity matrix is used. Discussion Signature fatty acid proiles of a range of myctophid and other ishes grouped these species together. Cephalopod species were clearly distinguishable from all ishes and from the muscle samples of their swordish predators. The proximity of the myctophid and other ish signatures to the swordish suggests that ishes were more important as prey than cephalopods, for the swordish examined. However, the swordish we examined were nearly all small ish, and we know from recent stomach analyses that small swordish prey mainly on small ish including myctophids (Young et al., 2006). Further sampling of larger swordish, and from different regions, would help resolve ontogenetic, spatial and temporal variations in their trophic ecology. Some oegospsid squid species contain oil rich digestive glands (DG), and the FA proiles of the squid DG were similar to myctophid prey (Phillips et al., 2001, 2002). As the squid DG lipid is therefore of dietary origin, and the oil content of the DG greatly exceeds that in the mantle, the overall lipid signature of an oegopsid may more closely resemble its prey species than does the lipid in the squid mantle. In this study, the collection and sampling methods used provided squid samples which generally contained only low oil content. Whether or not the squid examined in our study contained lipid-rich DG remains to be investigated. In summary, signature lipid proiles can be used to complement traditional stomach contents analyses and other biochemical methods, such as stable isotope analysis. Signature lipids have a high potential to increase our understanding of marine predator-prey interactions, particularly for the mid-trophic levels, including cephalopods. Acknowledgements The research was supported by an Ernst Frohlich Fellowship to Professor C.F. Phleger, CSIRO Marine and Atmospheric Research, and a grant from the Fisheries Research and Development Council, Australia. References Bradshaw C., M.A. Hindell, N.J. Best, K.L. Phillips, G. Wilson and P.D. Nichols. 2003. You are what you eat: estimating diet structure of southern elephant seals (Mirounga leonine) using blubber fatty acids. Proceedings of the Royal Society of London, Series B 270: 1283-1292. Clark K.R. and R.N. Gorley. 2006. Primer v6: User Manual/Tutorial. Primer-E: Plymouth. Lea M.-A., P.D. Nichols and G. Wilson. 2002. Fatty acid composition of lipid-rich myctophids and mackerel iceish – Southern Ocean food-web implications. Polar Biology 25: 843-854. 66 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Phillips K.L., G.D. Jackson and P.D. Nichols. 2001. Predation on myctophids by the squid Moroteuthis ingens around Macquarie and Heard islands: stomach content and fatty acid analyses. Marine Ecology Progress Series 215: 179-189. Phillips K.L., P.D. Nichols and G.D. Jackson. 2002. Lipid and fatty acid composition of four Southern Ocean squid species: implications for food-web studies. Antarctic Science 14: 212-200. Phleger C.F., M.N. Nelson, A.K. Groce, C.S. Cary, K.J. Coyne and P.D. Nichols. 2005. Lipid composition of deep-sea hydrothermal vent tubeworm Riftia pachyptila, crabs Munidopsis subsquamosa and Bythograea thermydron, mussels Bathymodiolus sp. and limpets Lepetodrilus spp. Comparative Biochemistry and Physiology B 141: 196-210. Young J.W., M. Lansdell, S. Riddoch and A. Revill. 2006. Feeding ecology of broadbill swordish, Xiphias gladius (Linnaeus, 1758), off eastern Australia in relation to physical and environmental variables. Bulletin of Marine Science 79: 793-811. 67 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA MODELLING Assessing the potential role of predation by jumbo squid (Dosidicus gigas) and ishing on small pelagics (common sardine Strangomera bentincki and anchovy Engraulis ringens) and common hake (Merluccius gayi) in central Chile, 33-39°S Hugo Arancibia1 and Sergio Neira2 1 Departamento de Oceanografía, Universidad de Concepción, Chile ([email protected]). 2 Zoology Department, University of Cape Town, South Africa. Since the early 2000s, jumbo squid (Dosidicus gigas) have been unusually abundant off central Chile (33°S-39°S). Although many hypotheses have been proposed for the increase in abundance, there is little agreement on why the increase is occurring. Periodic outbreaks of this species are frequent in central Chile, suggesting some underlying and recurrent cause. Due to the unpredictable nature of these events, there is no ishery for jumbo squid off central Chile, although jumbo squid are occasionally caught by trawlers and purse-seiners that target demersal ishes and small pelagics. Consequently, the biology and trophic ecology of jumbo squid is poorly known in the region. The jumbo squid is a voracious predator, and this characteristic has been used by Chilean stake holders (from public institutions, leet owners organisations, workers organisations and some researchers from public and private institutes) to explain the decline in hake (Merluccius gayi) (Subsecretaría de Pesca, 2004), and, to a lesser degree, of small pelagic ishes such as the common sardine (Strangomera bentincki) and anchovy (Engraulis ringens). Here we present results of the trophic impact of jumbo squid on pelagic and demersal ish stocks, particularly the common sardine, anchovy and hake, in waters off central Chile (Fig. 1, Table 1). Jumbo squid Anchovy (a) Anchovy (j) Common sardine (a) Common sardine (j) Hake (a) Hake (j) Sea lion We assumed an ecologically sound biomass for this species based on predators and ishery requirements represented in a 31-group Ecopath model of the central Chile marine ecosystem in the year 2000, following Neira et al. (2004). With this model, we calculated the biomass of the main prey removed by jumbo squid per year. In addition, using Ecopath with Ecosim (EwE, version 5.1; Christensen and Pauly, 1992; Walters et al., 1997), we simulated a one order-of-magnitude increase in the biomass of jumbo squid from year 2000 to 2005. Then, we analysed the effects of this change on the biomass of hake, common sardine and anchovy considering mixed (vulnerability, v=2) and top-down (v=5) trophic controls. Sea lion Hake (a) Hake (j) Common sardine (j) Common sardine (a) Figure 1. Mixed trophic impacts in the central Chile marine ecosystem, year 2000. Y-axes: impacting groups; X-axes: impacted groups. Anchovy (j) Anchovy (a) Jumbo squid 68 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Table 1. Inputs and outputs from the Ecopath model representing the central Chile marine ecosystem in the year 2000 Group name Trophic level Biomass (t/km²) P/B (/year) Q/B (/year) EE P/Q Cetaceans 4.42 0.007 0.600 10.000 0.167 0.060 Sea lion 3.93 0.072 0.250 20.000 0.381 0.013 Marine birds 3.59 0.065 0.500 20.000 0.000 0.025 Hake (juveniles) 3.35 7.793 2.500 8.323 0.977 0.300 Hake (adults) 3.92 12.189 0.456 5.159 0.660 0.088 Common sardine (j) 2.03 41.355 1.453 14.530 0.309 0.100 Common sardine (a) 2.03 14.600 1.875 18.750 0.276 0.100 Anchovy (j) 2.03 23.971 0.703 7.030 0.613 0.100 Anchovy (a) 2.03 14.631 2.120 21.200 0.241 0.100 Squid 3.73 3.337 3.500 10.606 0.999 0.330 Jumbo squid 4.54 6.351 1.750 5.303 0.500 0.330 Mesopelagic ish 3.40 48.985 1.200 12.000 0.999 0.100 Red squat lobster (j) 2.00 0.227 5.900 18.000 0.999 0.328 Red squat lobster (a) 2.00 0.541 3.569 12.500 0.999 0.286 Yellow squat lobster 2.00 0.077 3.569 11.600 0.782 0.308 Shrimp 2.00 0.400 2.500 12.000 0.467 0.208 Horse mackerel 3.52 23.980 0.564 14.200 0.359 0.040 Hoki 3.78 21.900 0.528 5.280 0.992 0.100 Swordish 4.66 0.640 0.500 5.000 0.750 0.100 Kingklip 3.53 0.300 0.700 3.500 0.351 0.200 Rattail ish 3.00 2.117 0.700 3.500 0.999 0.200 Big-eyed lounder 3.00 0.200 0.700 3.500 0.014 0.200 Cardinal ish 3.50 6.661 0.700 3.500 0.999 0.200 Paciic sand perch 3.57 0.045 0.700 3.500 0.095 0.200 Skates 3.00 0.253 0.362 2.413 0.131 0.150 Polychaetes 2.00 1.886 2.410 15.900 0.000 0.152 Jellyish 2.63 7.774 0.584 1.420 0.150 0.411 Copepods 2.25 79.257 45.000 154.519 0.999 0.291 Euphausiids 2.50 65.418 13.000 31.707 0.999 0.410 Phytoplankton 1.00 343.713 120.000 - 0.300 - Detritus 1.00 1000.000 - - 0.001 - Additionally, we ran a second simulation analysis using results of an Ecopath model representing the central Chile marine ecosystem in year 1970, that had been calibrated using time series from 1970-2004. Using EwE (Christensen and Pauly, 1992; Walters et al., 1997), we simulated the biomass of hake (2005 to 2010), under the following scenarios: a) ishing mortality constant (F=F2005); b) F=0 (2007 to 2010). Each ishing scenario was evaluated considering recruitment and predation mortality (constant, 1 variable). The EwE model estimated a biomass of around 300 thousand tonnes for jumbo squid in central Chile in 2000. Our results showed that jumbo squid had a high trophic level (TL>4), and they could have removed signiicant levels of biomass of hake, anchovy, common sardine and other prey from the system. However, the analysis did not take into account the varied diet of the jumbo squid. 69 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Speciically, the diet proportions of hake, common sardine and anchovy used in the model were unlikely to relect the opportunistic predator behaviour of this species. For example, the proportion of hake in its diet was higher than expected from the abundance of hake in the environment. In contrast, small pelagic ishes were relatively under-represented in the diet compared with their abundance in the region. Simulations with EwE indicated that an increased abundance of jumbo squid from 2000 to 2005 could have had a moderate-to-strong impact on hake biomass, depending on the kind of trophic control simulated (mixed vs. top-down). However, no noticeable impacts were observed for the common sardine and anchovy, regardless of the kind of trophic control simulated. The dynamics of the hake stock simulated using EwE indicated that the recovery of the stock in the medium- to long-term could be possible only under a F=0 scenario. The effect of predation by jumbo squid on the dynamics of hake was not signiicant from 2005 onwards. References Christensen V. and D. Pauly. 1992. ECOPATH II. A software for balancing steady state ecosystem models and calculating network characteristics. Ecological Modelling 61: 169-185. Neira S., H. Arancibia and L. Cubillos. 2004. Comparative analysis of trophic structure of commercial ishery species off Central Chile 1992 and 1998. Ecological Modelling 172: 233-248. Subsecretaría de Pesca, Chile. 2004. Cuota global anual de captura de merluza común año 2004. Informe Técnico (Res. Pesqueras) 80: 31pp. Walters C., V. Christensen and D. Pauly. 1997. Structuring dynamic models of exploited ecosystems from trophic mass-balance assessments. Reviews in Fish Biology and Fisheries 7: 139-172. 70 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA The direct and indirect contributions of cephalopods to global marine isheries Mary E. Hunsicker1, Timothy E. Essington1, Reg Watson2 and Rashid Sumaila2 1 2 School of Aquatic and Fishery Sciences, University of Washington, Seattle WA USA ([email protected]). Fisheries Centre, University of British Columbia, Vancouver BC, Canada. Cephalopods are a key component of marine food webs, providing sustenance for ishes, seabirds, and marine mammals worldwide. Cephalopods are also of increasing economic importance, evidenced by the rapid rise in their global landings over the past thirty years. Due to their ecological interactions, increased removal of cephalopods from marine ecosystems may have an unintended negative impact on the productivity of their predators, including commercially valuable ish stocks and charismatic megafauna. Thus, increased harvesting could be disadvantageous from both economic and conservation viewpoints. For example, the direct contribution of cephalopods to ishery landings could be less valuable than their indirect contribution through the ecological enhancement of ish production and production of species of non-consumptive value. We estimated the direct and indirect contribution of cephalopods to marine isheries in 17 large marine ecosystems (LMEs) using published diet data and species-speciic landing and market values (Sea Around Us Project). We also estimated the contribution of cephalopods to two pelagic marine ecosystems, the central north Paciic and eastern tropical Paciic, using previously published data (Ito and Machado, 2000; Cox et al., 2002; Olson and Watters, 2003; WPRMC, 2005; FFA, 2006). Our results indicate that, among many of the sampled ecosystems, approximately 10% to 30% of the ishery landings and market values may pass through the cephalopod biomass pool (Figs. 1 and 2). In the Patagonian shelf region, this value may be as high as 50%-55%. As expected, the total contribution (direct + indirect) of cephalopods to isheries landings is highest in ecosystems in which isheries are targeting species at the trophic level of cephalopods or higher, i.e. the Patagonian shelf, the eastern tropical Paciic, and the central north Paciic. A similar trend was found for the total contribution of cephalopods to isheries market values (Fig. 2). This analysis has identiied potential trade-offs among cephalopod and inish isheries that should be further evaluated prior to increased expansion of cephalopod isheries. Additionally, future work should incorporate the conservation value of cephalopods as they are a valuable prey item to species of non-consumptive value and conservation concern. Total contribution to landings (%) 60 50 Indirect Direct 40 30 20 10 0 f f f f elf ent el ea el elf ea ific ico ent el el elf nia ea ka ea ent ific Sh urr il Sh g S d Sh l Sh n S Pac ex urr r Shn Sh Sh lifor g S las h S urr Pac n M o C a C n z n a i a n a in A rt C l nia ia ra eri la nt ab l N of as ad ali tia C er of o la ica go forn th B B Zea tine Ar ntra ulf ulh abr ustr Sco lf of E B ulf N gue rop a W i G t l u G Ag f/L A n T w on Gu Ce Pa Ca So w E Be E Ne S C Ne S U Large Marine Ecosystem NE 71 Figure 1. The total contribution (%) of cephalopods to fisheries landings in 19 marine ecosystems. Estimates are based on previously published diet and landings data (LME landings data averaged over years 1990-2001). The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Total contribution to market value (%) 60 Indirect Direct 50 40 30 20 10 0 f f f t t f elf en el ea el elf ea ific ico ent el el elf nia ea ka ea en ific Sh urr il Sh g S d Sh l Sh n S Pac ex urr r Shn Sh Sh lifor g S las h S urr Pac n A t n M C C n o a C z n l r a a i n a i a ni ia ra eri la nt ab l N of as ad ali tia C er of o la ica go rn B B ea ne r ra lf lh br tr co of B lf N gue rop ta alifo uth W w Z onti A ent Gu gu f/La Aus S ulf E Gu n T a A w E G C P C So Be E Ne S C Ne S U NE Large Marine Ecosystem Figure 2. The total contribution (%) of cephalopods to isheries market values in 19 marine ecosystems. Estimates are based on previously published diet data and market values. Acknowledgements This work was supported by a NSF Biological Oceanography Program grant awarded to J.F. Kitchell and T.E. Essington and by the School of Aquatic and Fishery Sciences at the University of Washington. References Cox S.P, T.E. Essington, J.F. Kitchell, S.D. Martell, C.J. Walters, C. Boggs and I. Kaplan. 2002. Reconstructing ecosystem dynamics in the central Paciic Ocean, 1952–1998. II. A preliminary assessment of the trophic impacts of ishing and effects on tuna dynamics. Canadian Journal of Fisheries and Aquatic Sciences 59: 1736-1747. FFA (Paciic Islands Forum Fisheries Agency). 2006. Tuna market news. Paciic Islands Forum Fisheries Agency, Honiara, Solomon Islands. Ito I.Y. and W.A. Machado. 2000. Annual report of the Hawaii-based longline ishery for 2000. Technical Report, NMFS Honolulu. Olson R.J. and G.M. Watters. 2003. A model of the pelagic ecosystem in the eastern tropical Paciic Ocean. Bulletin of the Inter-American Tropical Tuna Commission 22(3): 220pp. WPRMC (Western Paciic Regional Management Council). 2005. Pelagic Fisheries of the Western Paciic Region Annual Report 2004. Western Paciic Regional Management Council, Honolulu, Hawaii. 72 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Modelling environmental inluences on squid life history, distribution, and abundance Graham J. Pierce1, M. Begoña Santos2, Colin D. MacLeod1, Jianjun Wang1, Vasilis Valavanis3 and Alain F. Zuur4 1 School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK ([email protected]). 2 Instituto Español de Oceanografía, Centro Costero de Vigo, Cabo Estay, Canido, 36200 Vigo, Spain. 3 Marine Geographic Information Systems, Hellenic Center for Marine Research, P.O. Box 2214, 71003 Iraklion, Crete, Greece. 4 Highland Statistics Ltd, 6 Laverock Road, Newburgh, Aberdeenshire AB41 6FN, UK. Following Caddy and Gulland’s (1983) classiication, squid populations can be described as displaying irregular or spasmodic abundance luctuations, as opposed to steady or cyclical patterns. Squid are short-lived, fast growing marine animals, thought to be especially sensitive to environmental inluences (Coelho, 1985). Because generations are essentially non-overlapping, modelling of population dynamics reduces to predicting recruitment success (Caddy, 1983; Pierce and Guerra, 1994). Environmental signals are expected to have a strong effect on spawning and hatching success and on growth and survival of early life stages. Since squid are increasingly important ishery resources in many parts of the world, much recent research has focused on understanding their distribution and abundance, to provide the basis for eficient and sustainable utilisation of these resources. The recent high abundance of jumbo squid Dosidicus gigas in the eastern Paciic Ocean raises questions as to why abundance and range have increased, the ecological consequences and whether or for how long its current status will persist. The aim of this brief review is to synthesise approaches to modelling the spatiotemporal patterns in squid life history, distribution, abundance and isheries, and to identify relevant research questions in relation to D. gigas. In principle, models of spatio-temporal variation can be itted to data on ishery catches and squid distribution, abundance and life history parameters. Critical stages of the life cycle include spawning, hatching, early growth, recruitment to the ishery and movements to the spawning grounds. In many squid, the paralarval (post-hatching) period tends to be the least well known. Because there is no buffering effect of older age classes, environmental effects on the extant generation are a particularly important feature of population dynamics, which has led to a focus on empirical rather than mechanistic models of abundance. In particular, we need to understand the relationship between spawning stock size and subsequent recruitment and pre-spawning mortality of recruits. Data on squid may arise from isheries, surveys, predators, tagging or direct observation: all have associated limitations and biases. Relevant considerations include availability, coverage, resolution (in time and space), accuracy and precision. Relevant environmental factors include large scale phenomena such as the El Niño-Southern Oscillation (ENSO) and North Atlantic Oscillation (NAO), current systems, ixed physical phenomena such as seabed depth and substrate, oceanographic parameters such as sea surface temperature (SST) and salinity (SSS), meso-scale ocean surface (and sub-surface) features and daily, lunar and seasonal cycles. The selection of relevant variables is normally a compromise between biological relevance and data availability. The most readily available oceanographic data tend to be related to surface characteristics measured by satellitebased instruments, but it is also important to consider the vertical dimension. Developments in remote sensing, geographic information systems (GIS) and statistical modelling have all facilitated current modelling applications. Empirical modelling is not without its critics: by focusing on the data rather than the underlying mechanisms it encourages data-driven rather than hypothesis-driven research. However, these are also advantages: hypotheses can be generated about the mechanisms and functional forms of relationships. As with all models, adequate testing of predictions is needed to eliminate spurious 73 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA (coincidental) relationships: as noted by Solow (2002), time-series correlations often disappear once longer series become available, and similar caveats apply to spatial models. Several generic issues apply to time-series and spatial modelling: these include model selection, model itting, testing predictions, decisions about scale, incorporating environmental effects that are displaced in space and/or time (time-lags and teleconnections), autocorrelation, seasonal patterns and unexplained trends, interactions between variables, identiication of data distributions, variance structure and linearity of relationships. Time series can be modelled using regression, generalised linear or additive models (GLM or GAM), but such models may be invalidated by temporal auto-correlation, i.e. non-independence of adjacent values of the response variable, which can inlate apparent statistical signiicance by up to 400% (Zuur et al., 2007). In short-lived species, the link between abundance or life history parameter values in successive generations (years) may be weak or non-existent. In the former case, inserting a term for the previous year’s value as an extra explanatory variable into the model may adequately account for autocorrelation. Whether this is an issue can be conirmed by testing the model residuals for temporal autocorrelation. Otherwise, solutions include Generalised Additive Mixed Modelling (GAMM), Seasonal and Trend decomposition using Loess (STL), Autoregressive Integrated Moving Average Models (ARIMA) or Dynamic Factor Analysis (DFA, a multivariate extension of STL). On a cautionary note here, the autocorrelation, moving average, seasonal and trend terms in such models capture variation without explaining it. Environmental parameters may however, be included. Time-lagged relationships with environmental variables can also be detected using cross-correlation analysis; some authors recommend so-called “pre-whitening” (de-trending) of series prior to analysis. However, common trends thus removed may indicate a genuine causal link. Links between Illex argentinus abundance and ENSO events, with a 5-year time-lag were detected by Waluda et al. (1999). ARIMA and DFA models of temporal trends in Loligo forbesi abundance have been published, and demonstrate effects of SST and the NAO index on abundance (Pierce and Boyle, 2003; Zuur and Pierce, 2004). However, these models tend to have low predictive power and, given the weak temporal structure of the squid time-series, approaches using regression, GAMs or regression trees, may be equally useful (e.g. Bellido et al., 2001; Waluda et al., 2001). Sims et al. (2001) used polynomial regression to demonstrate a link between timing of migration and the NAO index in L. forbesi. Pierce et al. (2005) used GAMs to extract interannual variation in size at maturity in L. forbesi, and then used correlation analysis to demonstrate that this residual variation could be related to the NAO index. Spatial modelling has been greatly facilitated by GIS (Pierce et al., 2002). Routines have been developed to identify meso-scale ocean surface features from variability or discontinuities in temperature (Valavanis et al., 2005; Wang et al., 2007, see Figure 1), as well as from variability in temperature and chlorophyll anomalies (Valavanis et al., 2004a). It is also possible to incorporate temporal variation into such models, although to date, there has been little work modelling distribution in the vertical dimension. Data from tagging have allowed description of squid movements underwater, in relation to oceanographic data, and such data would be amenable to itting models. Essential habitat and migration corridor models may be constructed using an entirely GIS-based process, incorporating ishery and environmental data constrained by life history data on species’ “preferred” living environmental conditions (Valavanis et al., 2002; Valavanis et al., 2004b). GAMs have been used to describe distribution patterns in both L. forbesi and I. argentnus, while regression trees have also been applied to data on L. forbesi, revealing relationships with temperature, salinity and depth (Pierce et al., 1998; Bellido et al., 2001; Sacau et al., 2005). Moreno et al. (in press) used GAMs to separate seasonal, annual and temperature effects on growth rates in L. vulgaris. The latter effects represent spatial variation in growth rates. Where presence records are available (e.g. from predator samples or tags) but there are no absence records, presence only modelling techniques such as ENFA (Hirzel et al., 2000) may be applied. There are no current applications to data on squid. 74 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 2 2 2 2 i 2 2 2 Null 1.1 1.1 2 1.3 i 1.4 1.5 2 1.6 1.7 1.8 a) Local SST relative variability RVi = 1/9 = 0.111 Profile view of a sink b) Local SST relative variability RVi = 7/8 = 0.875 1.750 21.630 21.630 21.630 21.630 21.630 21.630 21.630 21.630 21.630 21.630 21.500 21.500 21.630 1.750 21.630 21.750 21.630 21.630 21.630 21.630 21.500 21.630 21.630 21.630 21.630 21.630 21.630 1.750 21.630 21.750 21.630 21.630 21.630 21.500 21.500 21.500 21.500 21.500 21.500 21.630 21.630 1.750 21.750 21.750 21.630 21.630 21.630 21.500 21.500 21.630 21.630 21.630 21.630 21.630 21.630 1.630 21.500 21.500 21.500 21.500 21.500 21.500 21.500 21.630 21.630 21.630 21.500 21.630 21.630 1.630 21.630 21.630 21.500 21.500 21.500 21.500 21.630 21.630 21.630 21.500 21.500 21.630 21.630 1.500 21.630 21.500 21.500 21.500 21.630 21.630 21.630 21.630 21.630 21.630 21.630 21.630 21.750 1.500 21.630 21.630 21.630 21.630 21.630 21.500 21.500 21.630 21.630 21.630 21.630 21.630 21.630 Figure 1. Use of AVHRR SST data to identify meso-scale ocean surface features. Right: calculating relative variability in SST (Wang et al., 2007). Below: identifying SST (and Chla) “sinks” (Valavanis et al., 2005). As with time-series models, autocorrelation in spatial data is an important issue. Model residuals can be checked for spatial autocorrelation, and if none exists, spatial autocorrelation may be ignored. However, ideally, spatial autocorrelation should be included in the model (Pinheiro and Bates, 2000; Wood, 2004; Zuur et al., 2007) and this is possible using the software package R, among others. Latitude and/or longitude may be included in models as explanatory variables, although if these effects interact, results will be dificult to interpret. In any case, spatial trends revealed in this way are essentially unexplained trends. Many of the published models of environmental variation in squid relate to demersal species, in which temperature, salinity and large-scale phenomena (e.g. NAO) have been shown to inluence distribution, abundance and life history parameters. While the role of mesoscale ocean surface features was not analysed in these studies, generally because the relevant data were not available, recent analysis has shown that local variability in SST (presumed to be related to fronts) affects hake distribution in the south west Atlantic (Wang et al., 2007). Pelagic squid such as D. gigas tend to occur more remotely from land and are less well known than demersal squid. Less dependent on the substrate, they produce many more eggs, with the eggs being pelagic rather than attached to the seabed, hence strongly dependent on currents for dispersal. They tend to be highly migratory and might be expected to show stronger associations with meso-scale ocean surface features and have more variable abundance patterns. Useful goals for environmental modelling in D. gigas would include improved understanding of egg and paralarval distribution, recruitment success and limits to distribution. Tagging data should facilitate 4-dimensional (in space and time) modelling of individual movement patterns. Useful parallels could be drawn from comparative studies on European ommastrephid species such as Todarodes sagittatus. 75 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Acknowledgements GJP thanks the Workshop organisers for the invitation to attend the workshop and for inancial support and the workshop participants for useful discussions on the topic of analysing environmental relationships. Much of the work described in this paper was funded by the European Commission under various collaborative research projects, most recently CEPHSTOCK (Q5CA-2002-00962). References Bellido J.M., G.J. Pierce and J. Wang. 2001. Modelling intra-annual variation in abundance of squid Loligo forbesi in Scottish waters using generalised additive models. Fisheries Research 52: 23-39. Caddy J.F. 1983. The cephalopods: factors relevant to their population dynamics and to the assessment and management of stocks. In: J.F. Caddy (Ed.). Advances in assessment of world cephalopod resources. FAO Fisheries Technical Paper 231: 416-449. Caddy J.F. and J.A. Gulland. 1983. Historical patterns of ish stocks. Marine Policy 7: 267-278. Coelho M. 1985. Review of the inluence of oceanographic factors on cephalopod distribution and life cycles. NAFO Scientiic Council Studies 9: 47-57. Hirzel A.H., V. Helfer and F. Metral. 2001. Assessing habitat-suitability models with a virtual species. Ecological Modelling 145: 111-121. Moreno A., M. Azevedo, J. Pereira and G.J. Pierce. 2007. Growth strategies in the squid Loligo vulgaris from Portuguese waters. Marine Biology Research 3(1): 49-59. Pierce G.J., N. Bailey, Y. Stratoudakis and A. Newton. 1998. Distribution and abundance of the ished population of Loligo forbesi in Scottish waters: analysis of research cruise data. ICES Journal of Marine Science 55: 14-33. Pierce G.J. and P.R. Boyle. 2003. Empirical modelling of interannual trends in abundance of squid (Loligo forbesi) in Scottish waters. Fisheries Research 59: 305-326. Pierce G.J. and A. Guerra. 1994. Stock assessment methods used for cephalopod isheries. Fisheries Research 21: 255-285. Pierce G.J., J. Wang and V.D. Valavanis. 2002. Application of GIS to cephalopod isheries: workshop report. Bulletin of Marine Science 71: 35-46. Pierce G.J., A.F. Zuur, J.M. Smith, M.B. Santos, N. Bailey, C.-S. Chen and P.R. Boyle. 2005. Interannual variation in life-cycle characteristics of the veined squid (Loligo forbesi) in Scottish (UK) waters. Aquatic Living Resources 18: 327-340. Pinheiro J. and D.M. Bates. 2000. Mixed Effects Models in S and S-PLUS. Statistics and Computing, Springer-Verlag, New York. Sacau M., G.J. Pierce, J. Wang, A.I. Arkhipkin, J. Portela, P. Brickle, M.B. Santos and X. Cardoso. 2005. The spatio-temporal pattern of Argentine shortin squid Illex argentinus abundance in the southwest Atlantic. Aquatic Living Resources 18: 361-372. Sims D.W., M.J. Genner, A.J. Southward and S.J. Hawkins. 2001. Timing of squid migration relects North Atlantic climate variability. Proceedings of the Royal Society of London, Series B 268: 2607-2611. Solow A.R. 2002. Fisheries recruitment and the North Atlantic Oscillation. Fisheries Research 54: 295-297. Valavanis V.D., S. Georgakarakos, A. Kapantagakis, A. Palialexis and I. Katara. 2004b. A GIS environmental modelling approach to essential ish habitat designation. Ecological Modelling 178: 417-427. Valavanis V.D., S. Georgakarakos, D. Koutsoubas, C. Arvanitidis and J. Haralabous. 2002. Development of a marine information system for cephalopod isheries in the Greek seas (eastern Mediterranean). Bulletin of Marine Science 71: 867-882. 76 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Valavanis V.D., A. Kapantagakis, I. Katara and A. Palialexis. 2004a. Critical regions: A GIS-based model of marine productivity hotspots. Aquatic Science 66: 139-148. Valavanis V.D., I. Katara and A. Palialexis. 2005. Marine GIS: Identiication of mesoscale oceanic thermal fronts. International Journal of Geographical Information Systems 19: 1131-1147. Waluda C.M., P.G. Rodhouse, G.P. Podestá, P.N. Trathan and G.J. Pierce. 2001. Surface oceanography of the inferred hatching grounds of Illex argentinus (Cephalopoda: Ommastrephidae) and inluences on recruitment variability. Marine Biology 139: 671-679. Waluda C.M., P.N. Trathan and P.G. Rodhouse. 1999. Inluence of oceanographic variability on recruitment in the Illex argentinus (Cephalopoda: Ommastrephidae) ishery in the South Atlantic. Marine Ecology Progress Series 183: 159-167 Wang J., G.J. Pierce, M. Sacau, J. Portela, M.B. Santos, X. Cardoso and J.M. Bellido. 2007. Remotely sensed local oceanic thermal features and their inluence on the distribution of hake (Merluccius hubbsi) at the Patagonian Shelf edge in the SW Atlantic. Fisheries Research 83(2-3): 133-144. Wood S.N. 2004. Stable and eficient multiple smoothing parameter estimation for generalized additive models. Journal of the American Statistical Association 99: 637-686. Zuur A.F., E.N. Ieno and G.M. Smith. 2007. Analysing ecological data. Springer-Verlag. Zuur A.F. and G.J. Pierce. 2004. Common trends in Northeast Atlantic squid time series. Netherlands Journal of Sea Research 52: 57-72. 77 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA PERSPECTIvES AND DISCUSSIONS Squid – the new ecosystem indicators George D. Jackson1 and Ron K. O’Dor2 1 Institute of Antarctic and Southern Ocean Studies, University of Tasmania, Private Bag 77, Hobart, Australia 7001 ([email protected]). 2 Census of Marine Life Secretariat, Consortium for Oceanographic Research and Education, Suite 420, 1201 New York Ave. NW, Washington, DC 20036, USA. Squid occupy most oceanic regions, from the shallow tropical seas to the deep ocean. They play important roles as both predators and prey in these habitats. In many ways, they are ecological equivalents to teleost ishes and compete successfully with them in the various oceanic ecosystems. There is a diversity of body forms in both near-shore and oceanic squid, and their success in the ocean is related to their ability to ill a variety of niches. The large muscular ommastrephid squid (e.g. Dosidicus, Ommastrephes, Sthenoteuthis) play an important role in many ocean current systems, and are formidable predators. These active squid that inhabit the epipelagic realms and function as ecological equivalents to the large piscivorous teleosts, such as the tunas and billishes. In the near-shore environment, the loliginid squid have life cycles generally associated with shallow water environments and lay their eggs on the bottom and feed on near-shore prey. Loliginids (e.g. Lolilgo, Sepioteuthis) function much as near-shore inishes and play an important role in that environment. In the deep ocean, there are large-bodied squid that are ammoniacal, slower moving and probably tend to stalk their prey (e.g. Mastigoteuthis, Moroteuthis, Architeuthis, Mesonychoteuthis). These large deepwater squid are functioning as important deep sea predators in much the same way as large sixgill or sleeper sharks do. In fact, squid and other cephalopods may ind a refuge in the very deep ocean, where they function as top predators due to the lack of sharks and other elasmobranchs in abyssal waters (Priede et al., 2005). Interestingly, while we think of squid as fast moving and generally muscular, there are a number of mesopelagic species that have body cavities full of ammonia and sit within the open ocean like balloons waiting passively to snag prey with their arms and tentacles. There are a variety of cranchiid squid that incorporate this lifestyle (e.g. Cranchia, Liocranchia, Teuthwenia), and they do not swim very much. Such species actually have a life style more in tune with jellyish than teleosts. Whatever the strategy adopted, squid are successful components in these diverse environments, although they have a life style that is energetically more costly (jet pressure compared to teleost undulatory swimming, O’Dor and Webber, 1986). In polar waters, ommastrephid squid appear to actually replace large predatory ishes by illing a niche normally occupied by teleosts (Rodhouse and White, 1994). A rapid life style is one feature that stands out for all squid species, as opposed to the majority of larger teleost ishes. Most squid have life spans of less than a year, with few species living beyond a year (Jackson, 1994; Jackson and O’Dor, 2001). Many inshore loliginid species have life spans considerably less than a year, and tropical squid generally have life spans no greater than 200 days (Jackson, 2004). This work has been greatly facilitated by the use of daily statolith growth increments to age squid. This brief lifespan contrasts with that of the majority of large-bodied predatory teleosts that have perennial life cycles, and some deepwater teleosts that can live for over a century. Squid have thus been referred to as being ‘weeds of the sea’, and living ‘life in the fast lane’. There are a number of features that enable this fast life style: (1) rapid, eficient digestion and a proteinbased metabolism that converts food into growth rather than storage, (2) continual recruitment of new muscle (hyperplasia) ibres throughout growth, (3) eficient utilisation of oxygen and (4) low levels of antioxidative defense (Jackson and O’Dor, 2001). These features enable the rapid growth and short life spans of squid. They also drive the continual non-asymptotic growth that is a common feature of squid, and very different to the asymptotic growth of teleost ishes. The continued recruitment of new muscle ibres throughout the life cycle is thought to be one of the physical mechanisms that 78 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Fish Squid Hypertrophy and hyperplasia Size Size Hypertrophy Hyperplasia Hyperplasia Age Age Figure 1. Diagrammatic representation of asymptotic growth of ishes, in which hyperplasia ceases and growth only occurs by hypertrophy, compared with non-asymptotic continual growth in squid, which show both hypertrophy and hyperplasia in adults. The circles on the graph represent the relative sizes of muscle ibres. enable the rapid continual growth of squid (Moltschaniwskyj, 1994). In contrast, while teleost ish have hyperplasia when young, this eventually ceases later during ontogeny, and ish are dependent on enlargement of existing muscle ibres to drive growth (Fig. 1). Fast growth rates and short life spans in squid result in a rapid turnover of populations. This makes managing squid isheries challenging and predicting potential recruitment almost impossible. Squid populations appear to be more inluenced by oceanographic conditions rather than by ishing pressure, and stock luctuations appear to be closely tied with environmental conditions (Waluda et al., 2004). Squid also have huge biomass. It has been estimated that a single predator, the sperm whale consumes annually 100 million tonnes of squid per year. This value is similar to all world isheries catches combined and equates to about the half the biomass of humanity (Clarke, 1980). Although the biomass is high, given the rapid life spans of squid, there is a rapid turnover in biomass over time. During times of food shortages, squid readily turn to cannibalism, which can also act to limit biomass. The fast life style of squid means that they have extremely plastic growth, depending on existing environmental conditions. Growth rates and body size can change rapidly if thermal or biological conditions markedly change over short time periods. This was relected in the population of Loligo opalescens off the California coast (Jackson and Domeier, 2003). Individuals of L. opalescens that lived through the 1997 El Niño had substantially smaller body sizes and slower growth rates compared to individuals that grew through the subsequent La Niña period, which was cooler but dramatically more productive, with increased upwelling and zooplankton. Thus, the population parameters of squid will quickly respond to the conditions that they experience, providing a means to monitor changes within the marine ecosystem. Due to the fast life styles of squid, they can act as real time ecosystem indicators and productivity integrators. Longer-lived organisms cannot monitor the environment in this way, as longer life spans and slower growth rates mean that environmental changes are integrated over much longer time periods. Although we now have relatively synoptic data on ocean climate itself, we still do not know how to translate this into edible biomass. Collecting long-term time series of squid age and growth in relation to oceanographic data can thus serve as a means to monitor how key elements in the marine community respond to ongoing changing environmental conditions. As the marine environment faces global warming and increasing sea temperatures, it is likely that nearshore and shallow water squid populations will be one of the irst organisms to relect changes in a new warmer marine environment. Because squid play important roles in a variety of marine ecosystems, and because they are commercially important, changes in squid populations will probably lead to a variety of profound effects. 79 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA References Clarke M.R. 1983. Cephalopod biomass – estimation from predation. Memoirs of the National Museum Victoria 44, 95-107. Jackson G.D. 1994. Application and future potential of statolith increment analysis in squids and sepioids. Canadian Journal of Fisheries and Aquatic Sciences 51: 2612-2625. Jackson G.D. 2004. Advances in deining the life histories of myopsid squid. Marine and Freshwater Research 55: 357-365. Jackson G.D. and M. Domeier. 2003: The effects of an extraordinary El Niño/La Niña event on the size and growth of the squid Loligo opalescens off Southern California. Marine Biology 142: 925-935. Jackson G.D. and R.K. O’Dor. 2001. Time, space and the ecophysiology of squid growth, life in the fast lane. Vie Milieu 51(4): 205-215. Moltschaniwskyj N.A. 1994. Muscle tissue growth and muscle ibre dynamics in the tropical loliginid squid Photololigo sp. (Cephalopoda, Loliginidae). Canadian Journal of Fisheries and Aquatic Sciences 51: 830-835. O’Dor R.K. and D.M. Webber. 1986. The constraints on cephalopods: why squid aren’t ish. Canadian Journal of Zoology 64: 1591-1605. Rodhouse P.G. and M.G. White. 1995. Cephalopods occupy the ecological niche of epipelagic ish in the Antarctic Polar Frontal Zone. Biological Bulletin 189: 77-80. Priede I.G., R. Froese, D.M. Basiley, A. Bergstada, M.A. Collins, J.E. Dyb, C. Henriques, E.G. Jones and N. King. 2006. The absences of sharks from abyssal regions of the world’s oceans. Proceedings of the Royal Society, Series B 1592: 1435-1441. Waluda C.M., P.N. Trathan and P.G. Rodhouse. 2004. Synchronicity in southern hemisphere squid stocks and the inluence of the Southern Oscillation and Trans Polar Index. Fisheries Oceanography 13: 255-266. 80 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Perspectives on Dosidicus gigas in a changing world William F. Gilly1 and Unai Markaida2 1 Hopkins Marine Station, Department of Biological Sciences, Stanford University, Paciic Grove,CA 93950, USA ([email protected]). 1 Departamento de Aprovechamiento y Manejo de Recursos Acuáticos, El Colegio de la Frontera Sur, Calle 10 No. 264, Col. Centro, CP 24000 Campeche, Mexico. Overview A large portion of “The Role of Squid in Open Ocean Ecosystems” workshop was focused on one species of oceanic squid – Dosidicus gigas (Humboldt or jumbo squid), the largest member of the family Ommastrephidae. Furthering our understanding of this species and its interactions with the ecosystems in the eastern Paciic Ocean was deemed to be of critical importance for reasons discussed below. Many of the features of D. gigas biology are likely to be relevant to other ommastrephids in the eastern Paciic, particularly Sthenoteuthis oualaniensis and Ommastrephes bartramii, which have overlapping ranges, are genetically close and probably show similar behaviours (Nakamura, 1993; Nesis, 1993; Yokawa, 1994). Because of its extremely fast growth, highly migratory nature and profound adaptability, D. gigas (and probably other ommastrephid species) are likely to provide a rapid indicator of environmental changes on a spatial scale ranging from local to whole ocean basins. The invasion of D. gigas into new areas is undoubtedly related, in speciic ways, to oceanographic changes that alter productivity, e.g. temperature, upwelling, oxygen levels, etc. As discussed below, many mesopelagic organisms on which D. gigas feed are short-lived species that can also respond quickly to environmental perturbations and productivity events. Unfortunately, our knowledge of the dynamics of responsiveness of either squid predators or their prey to environmental luctuations is presently limited, and improving this situation should be given high priority in directing research efforts. If D. gigas reacts rapidly to take advantage of perturbations, its appearance provides a positive indication of climate change. Sometimes such indications can be extremely dramatic, such as mass strandings of large squid visible to even the most casual observer. In general, appearance is a much less ambiguous and more easily monitored signal than the disappearance or inhibition of a ‘standard’ indicator species. Additional research that is aimed at providing a deeper understanding of migrations by D. gigas would provide the basis for interpreting the relationships of movements to particular oceanographic or food web variables. The tight coupling between D. gigas and its prey, and the adaptability of both groups, lies at the heart of what we need to know, and we will have to learn more about both to elucidate any overall principles. It is already becoming apparent that D. gigas may be exerting a strong top-down predatory inluence on the pelagic ecosystems that it invades, and this restructuring may act to amplify and modify impacts of climate change on many prey species in complex ways that would not be predicted from direct effects of climate change alone. This article is not intended to be a comprehensive review of the biology of D. gigas. Instead, we focus on aspects that we feel are most relevant to climate change. We also propose an outline for a research programme that would greatly expand our view. A large part of this research could be immediately carried out with established methods – what is needed is a systematic, largescale study in both northern and southern hemispheres. In addition, some newer methodologies should be adapted for use with D. gigas and other ommastrephid squid. Development of these techniques must be encouraged, and they would provide a strong complementary set of tools to methods already established. It seems clear that studies today about pelagic food webs that are expanding and thriving in response to climate change will provide insight into what the oceans will look like in the future. We do not know the distance to the future, but it is likely we are already well on the way. 81 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Why is Dosidicus gigas ecologically and economically important on a global scale? A number of factors come together and reveal the importance of D. gigas, 1) large geographic range, 2) enormous biomass and extremely high reproductive output, 3) lexible feeding strategies, 4) tolerance of environmental extremes, and 5) great ishery potential. These factors are discussed individually below. 1) Expanding range. D. gigas is a highly migratory oceanic squid that also inhabits continental shelf environments. It differs in this latter regard from S. oualaniensis and O. bartramii, both of which are more truly oceanic. D. gigas has an enormous historical range in the eastern Paciic, stretching from central California to northern Chile (Roper et al., 1984; Nigmatullin et al., 2001). During the last few years this range has expanded to Alaska (Cosgrove, 2005; Wing, 2005) and southern Chile (Chong et al., 2005). Although the western boundary for the species is thought to be about 140°W at the equator (Wormuth, 1998), this longitude is rather vague. It is not known whether westward expansion is also occurring. Such range expansions can be long-lasting or transient, but our understanding of the reasons for such expansions, including underlying oceanographic perturbations, is very incomplete. Satellite tagging studies in the Gulf of California have revealed that individual jumbo squid undertake daily horizontal movements of tens of km, even at times when no mass directed-migrations are known to be occurring (Gilly et al., 2006b and unpublished data). This short-term migratory behaviour is probably associated with searching for food and is likely to be intimately related to the nature of D. gigas as a species to undertake periodic excursions (Gilly, 2005). 2) Biomass and reproductive output. Presently, there is no good estimate of the biomass of D. gigas, but analysis of stomach contents of sperm whales in Peru before the curtailment of commercial whaling indicated that sperm whales alone consumed about 10 million tonnes of D. gigas each year off Chile and Peru (Clarke et al., 1988). Clearly the biomass is extremely large, and may be increasing along with geographical range. Dosidicus gigas is the most fecund of all cephalopods, producing up to 30 million eggs per female (Nigmatullin et al., 1999). Growth is extraordinarily rapid, with a tiny planktonic hatchling of ~0.01 g (unpublished data; Yatsu et al., 1999) reaching an adult size of 40 kg or more in a life-span of only 1-2 years (Arkhipkin and Murzov, 1986; Masuda et al., 1998; Markaida et al., 2004). D. gigas also shows a complex population structure, with a high degree of variability in the size reached by an individual animal at the time of sexual maturity (Nigmatullin et al., 2001). This plasticity appears to be related to environmental factors, including temperature and food supply (Nesis, 1983; Markaida et al., 2004; Bazzino et al., 2007). Altered size-structure of D. gigas populations by climate change would be expected to lead to a complex suite of ecological impacts. Juvenile jumbo squid serve as prey for many species of pelagic ishes, including tunas, billishes and seabirds throughout the squid’s range (Perrin et al., 1973; Pinkas et al., 1971; Abitia-Cardenas et al., 1999; Olson and Galván-Magaña, 2002). Large adults serve as prey for the largest ishes, such as swordish (de Sylva, 1962; Ibáñez et al., 2004; Markaida and Sosa-Nishizaki, 1998; Markaida and Hochberg, 2005), and marine mammals, including sperm whales both off Peru (Clarke et al., 1976, 1988; Fiscus et al., 1989) and in the Gulf of California (Jaquet and Gendron, 2002, 2003; Ruiz-Cooley et al., 2004, 2006). Thus, different predators will be selectively impacted, either positively or negatively, by environmentally inluenced changes in the body size of jumbo squid available to them in a given area. 3) Feeding strategies. Dosidicus gigas is a voracious, opportunistic predator that consumes vast quantities of mesopelagic myctophid ishes, crustaceans and other cephalopods, including its own kind (Markaida, 2006; Markaida and Sosa-Nishizaki, 2003; Shchetinnikov, 1986, 1989), thereby directly competing with pelagic vertebrates that also forage on these organisms. But these feeding habits also mean that D. gigas provides an important and direct link between small mesopelagic organisms and apex vertebrate predators. The relationship of D. gigas to vertebrate predators is thus, an extremely complex and multidimensional one. 82 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Most of our knowledge concerning the diet of D. gigas comes from work in the Gulf of California. Recent stomach-content analyses from the Paciic Ocean, both off Magdalena Bay (Baja California Sur, Mexico) and off central California were presented at the meeting by Unai Markaida and Ken Baltz, respectively. Both studies revealed substantial differences from the diets described in the Gulf, particularly in greater numbers and variety of larger, neritic ishes. This inding was especially dramatic in the California case, in which D. gigas was found to be preying on commercially valuable ishes, including hake and rockishes (Field et al., in press). D. gigas has also been implicated with reductions of hake populations in Chile (Ibáñez and Cubillos, in press; Arancibia and Neira, p.68 this volume) and with predation on yellowin tuna during commercial ishing operations (Olson et al., 2006). Although little is known about predatory behaviour directed against such larger ish species, adult jumbo squid are clearly physically capable of preying on large ishes. Feeding habits of D. gigas are thus extremely diverse. Perhaps most importantly, lexibility in foraging strategies allows jumbo squid to take maximum advantage of whatever prey resources they encounter in the course of their migrations. 4) Environmental tolerance. Archival electronic tagging of D. gigas in the Gulf of California has revealed that the squid can move frequently over the course of a day between near-surface waters, which are well oxygenated (cool in winter, hot in summer), and cold, deep waters of 300 m or more, which can be seriously hypoxic (Gilly et al., 2006b). Remarkably, the squid appears to be highly active in both environments and may forage continuously. Tolerance of such environmental extremes, coupled with a lexible diet, would clearly be advantageous to D. gigas when it ranges into a new and unfamiliar area, as in the case of its recent northward range expansions Unpublished tagging results also suggest that D. gigas varies its behavioural patterns, presumably relecting foraging strategies, seasonally in the Gulf of California. In this region, sea-surface temperature, prevailing winds and currents, productivity events (upwelling), as well as the oxygen proile of the water column all show dramatic seasonal changes. Thus, D. gigas is well adapted to major environmental changes on a regional scale. How this adaptability extrapolates to other areas in its broad range is unknown, but it is again likely to be a major factor in periodic excursions and longer-lasting range expansions. 5) Fishery. Dosidicus gigas presently supports the world’s largest cephalopod ishery – 800,000 tonnes in 2004 (FAO statistics), primarily from Chile, Peru and Mexico. It constitutes the third most valuable ishery in Mexico, with typical landings of 100,000 tonnes made almost entirely in a small near-shore portion of the Guaymas Basin in the Gulf of California. Recently, landings have expanded elsewhere in Mexico, particularly off Magdalena Bay on the Paciic coast of Baja California, where a ishery has developed in the springtime. Perhaps an equally important factor concerning isheries relates to potentially negative impacts of D. gigas invasions on established commercial and recreational isheries. As discussed above, such impacts are probably occurring at the present time in the California Current system (Field et al., in press; Zeidberg and Robison, 2007) and elsewhere. At the present time, recreational isheries in southern California are being heavily impacted by D. gigas (Thomas, 2007; Sarabia, 2007). Taken together, these characteristics indicate that D. gigas is ecologically important as both predator and prey over much of the eastern Paciic. Moreover, they strongly suggest that D. gigas plays a major role in structuring the pelagic and mesopelagic ecosystems in this large region, particularly in areas that it invades. D. gigas can cope with large variations in temperature, dissolved oxygen levels, and prey type. It is highly migratory and can react rapidly to environmental changes on a variety of temporal and spatial scales. Changing climate conditions, due to both natural and anthropogenic factors, will undoubtedly lead to future alterations of the range of D. gigas and its relationships to food webs that connect ishes, seabirds, marine mammals and humans. 83 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA What more do we need to learn and where do we look? All of the aspects reviewed above led to an informal consensus at this workshop that an international research effort was immediately needed to advance our knowledge of D. gigas and its impacts on the highly productive ecosystems in its range, including the California and Peru Currents and the Costa Rica Dome. Because of the present range expansion, it was deemed that such research should be carried out as rapidly as possible because of the window of opportunity. In many cases, necessary research methods are already in use and have demonstrated feasibility. These efforts should commence immediately. In other cases, adaptation of newer methods will be necessary, and rapid developments in this area should be encouraged. Because of the large geographic range of D. gigas and the substantial regional ecological differences, it would seem necessary to approach the problem by dividing the species range into bio-geographical regions, each with a coordinating investigator and speciic participants. These should include: 1) Paciic Northwest (Alaska, British Columbia, Washington, Oregon), 2) California, 3) Mexico (Gulf of California and Paciic Ocean), 4) Costa Rica Dome and Ecuador, 5) Peru, and 6) Chile. A variety of proven methods should be used to address the questions outlined below, with a consistent programme applied across the 6 regions. It seems likely that we will be able to elucidate general truths only by systematically comparing results from the same approaches in different regions. New methods must be developed and added to the programme as their feasibility is demonstrated. Such a programme must be comprehensive to succeed. Variability and lexibility are key features of D. gigas that make it successful, and this must be kept in mind when designing a coordinated research effort that must search for common threads in data from different regions collected by different investigators. Identiication of speciic model-systems that support quasi-stable populations of D. gigas on a yearround basis should be particularly encouraged, because intense, focused study in such areas is tractable and likely to reveal important links between environmental signals and squid movements that are applicable on much larger geographic scales. In the Guaymas Basin of the Gulf of California, a fairly well-deined seasonal movement of D. gigas occurs between summer ishing grounds on the Baja coast and winter grounds off the mainland coast in Sonora (Markaida et al., 2005). In the Monterey canyon system off central California, D. gigas appears to be present year-round but is more abundant in the winter (Zeidberg and Robison, 2007). A large scale migration pattern centred on the Costa Rica Dome has been proposed for South American waters (Nesis, 1983), but no direct demonstration has been made. In no case, do we yet understand the relationship between environmental or oceanographic events and squid movements, and a close examination of these data sets needs to be undertaken. Identiication of other geographically restricted areas with well-deined annual movements of squid would be valuable. Such areas, particularly in the southern hemisphere, might be identiiable simply from local commercial landings data. Focused study of these sites should be encouraged. What general questions can be studied with existing methodology? 1) Where are the squid at any given time? This includes analysis of horizontal migrations and their progress over both short- and long-term time scales. These movements should be viewed in association with seasonality and oceanographic conditions, especially productivity, temperature, and dissolved oxygen. Methods available include jigging surveys, conventional tag-and-recapture studies, acoustic tracking using the POST array in the Paciic Northwest, and pop-up satellite-tag methods. All of these approaches should be complemented by an analysis of the available satellite data and with conventional oceanographic proiles collected in the ield. In particular, oxygen-depth proiles should be sampled more often and at more selected locations in some coherent manner. Available data should be compiled and changes over time examined – for example in relation to the appearance of D. gigas in the Gulf of California (pre 1970?), Monterey Bay (post 1997/98 ENSO) or Alaska (2004). The nearshore hypoxia anomaly off Oregon (Grantham et al., 2004) during the recent spread of D. gigas through the Paciic Northwest is a good example of such a candidate event. 84 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Development of new methods, such as analysis of statolith microchemistry to determine geographical migrations, should be encouraged. Examining how the population dynamics of D. gigas varies across the range of its habitat, using statolith ageing and possibly gladius (pen) increment analysis, would shed light on population turnover rates, and this information is necessary for developing ecosystem models relevant to the different climatic zones where D. gigas is found. Sampling D. gigas and other ommastrephid squid using research driftnets from the coast to offshore, similar to the manner in which Ichii et al. (p.31 this volume) studied Todarodes paciicus, would shed much light on changes in geographical range of a given species. For example, what is the western boundary of D. gigas? What is the habitat separation/overlap between D. gigas and other ommastrephid species in the Paciic? 2) Where and when does breeding occur? The Costa Rica Dome area was thought to be the major spawning ground (Vecchione, 1999), but recent work in the Guaymas Basin suggests that spawning takes place there as well (Gilly et al., 2006a). It seems likely that other (perhaps many other) spawning areas exist (Nesis, 1983; Nigmatullin et al., 2001). Conventional plankton tows for D. gigas paralarvae or dip-netting small juveniles at the surface at night are good indicators of recent spawning in a general area. In many areas of the eastern Paciic, standard genetic analysis of ommastrephid paralarvae will be necessary to unambiguously identify the species collected (Gilly et al., 2006a) because of overlap with other ommastrephid squid, particularly Sthenoteuthis oualaniensis and poor morphological differentiation to species level despite previous efforts working with paralarvae (Camarillo-Coop et al., p.7 this volume; Granados-Amores et al., p.22 this volume; Yatsu et al., 1998). An historical examination of this question might also be possible by identiication of D. gigas paralarvae and juveniles in available zooplankton samples from previous studies, such as the CalCOFI sampling of the California Current system (Okutani and McGowan, 1969). Other sampling programmes in Mexico and the southern hemisphere may also have yielded useful collections, and these need to be systematically examined. 3) Do genetically identiiable populations exist? Recent genetics work, using a RAPD approach (Sandoval-Castellanos et al., 2007) as well as analysis of mitochondrial gene sequences (our work, in preparation) has revealed little spatial structure for D. gigas populations over a broad geographical scale. Future work directed at this important question should include development of additional genetic markers, including microsatellites. 4) What are the squid eating as adults and juveniles? What vertebrate species are eating them at different stages? How variable are these links and how rapidly do they change? Traditional gut-content analysis of adult and juvenile squid, as well as vertebrate predators, would go a long way to answering these questions. Application of newer methods, as discussed below, would also be extremely helpful. 5) What are the characteristics of short-term vertical migrations, i.e., how are squid utilising the water column? This question is intimately linked to diet, because D. gigas undoubtedly employs vertical (as well as horizontal) migrations to search for optimal foraging areas. We have been observing much individuality in both dynamics of vertical migrations and diet in the Gulf of California, and it will be important to sample enough individuals to obtain a general picture at any one place and time. Archival electronic tags can be used in areas with high levels of commercial ishing, and ishery-independent pop-up satellite-tag methods can be employed anywhere (Gilly et al., 2006b). At present there is no commercially available tag that is capable of measuring dissolved oxygen at the depths inhabited by D. gigas. Development of such a tag would provide a powerful new tool, because of the strong link between this squid and hypoxic midwater environments. 6) How many squid are being caught commercially – where and when? Historical and contemporary commercial landings data provide a good indicator of the presence of squid and a detector of range expansions. Analysis of such data in conjunction with satellite and oceanographic data bases might provide valuable insights into reasons underlying long-term range expansions (Waluda et al., 2004; Waluda and Rodhouse, 2006). 85 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 7) What are the local social and economic effects of the squid ishery? Although D. gigas is presently the target of the world’s largest cephalopod ishery, much of the ishing (in both the northern and southern hemispheres) is artisanal in nature and carried out in small vessels. In some cases, such as Santa Rosalia in the Gulf of California, a large part of the local economy depends on the squid ishery, either directly or indirectly. Impacts of this ishery on such local communities are important to document, because they are part of the relevant ecosystems, and must ultimately be considered in any management plans for marine resources. Development of the D. gigas ishery has historically depended on demand from Asian markets. This makes for volatile local squid prices and a risky ishery. 8) What kind of models can be developed for fast-growing, short-lived squid and their reactions to environmental perturbations and climate change? This issue is discussed by Graham Pierce (p.73 this volume). Although we are still lacking much of the biological data to guide modelling, application of established isheries models, based on long-lived species like ishes, are unlikely to accurately account for or predict variations in squid abundance or distribution. This will be a challenging and ultimately rewarding area for research. Newer methodologies A number of relatively recently developed techniques have been applied to other squid species, and need to be adapted or validated for use with D. gigas and other ommastrephid squid. Numbering of this section corresponds to that above. 1a) Analysis of migrations through statolith microchemistry. Seasonal collection of samples of D. gigas paralarvae should be made wherever they are available (especially in the Gulf of California and Costa Rica Dome), and the extracted statoliths should be used for microchemical analysis to obtain an elemental ingerprint of home regions using ICPMS. Analysis of statoliths from adults collected along expansion fronts, or elsewhere, could then determine the ingerprint of the centralmost (oldest) region to detect the natal hatching region. This technique has been successfully used for deining hatch regions for a reef squid, Sepioteuthis australis, in Tasmania by Gretta Pecl, University of Tasmania, but early work on an ommastrephid, Ommastrephes bartramii, proved not to be so successful (Yatsu et al., 1998). Recent progress in this ield is encouraging, and application to oceanic squid clearly needs exploration. 1b) Dynamics of movements of individual squid using acoustic tags. Acoustic tagging technology should be applied in conjunction with the extended acoustic array being developed by POST and OTN in the northern hemisphere. Important predators, such as sperm whales in the Gulf of California, should also be tagged in order to track their movements. Strategic VR3 acoustic receivers can be placed at the entrance and within the Gulf of California to expand the geographical extent of the existing POST array. The existing POST array would be able to track the movement of D. gigas as individuals move between California and Alaska. 1c) Use of acoustic (sonar) technology to monitor squid movements and estimate biomass. Although squid generally are thought to be problematic targets for acoustic surveys, the large size of D. gigas and relatively simple structure of the midwater community in certain areas where it is abundant, e.g. Gulf of California (relatively simple) vs. California Current system (much more complex), makes application of these methods promising. Recent preliminary ield trials in the Gulf of California were extremely encouraging (Benoit-Bird et al., submitted). Development of acoustic methods for biomass estimation should be a high priority research goal, because such data are necessary for both a deeper understanding of the ecology of the species and for any management measures. Because acoustic methods can be applied over a relatively large area in a small amount of time, they would be excellent in limited regions where D. gigas is abundant, for example the Guaymas Basin. Real-time acoustic monitoring of squid in the water column would also provide an independent means of studying how D. gigas utilises the water column in relation to acoustic scattering layers and other oceanographic features. 86 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA 2) Utilisation of existing samples to map presence of paralarvae. Documenting the historical presence of D. gigas in the California Current should be feasible through identiication of paralarvae in zooplankton collections made by previous CalCOFI expeditions or by similar programmes in Mexico (IMECOCAL) and in South America. 3) Fatty acid and stable isotope analysis of trophic linkages. Application of these techniques should be encouraged to better understand the prey of D. gigas using signature fatty acid analysis and stable isotope analysis (Ruiz-Cooley et al., 2006). Sampling needs to be carried out on thoughtful spatial and temporal scales. Sperm whale blubber biopsies can be collected for comparing the fatty acid and stable isotope signatures between these important predators and prey. In the Gulf of California, consumption of D. gigas by sperm whales is probably on the order of that landed commercially – about 100,000 tonnes per year. Again, this factor is relevant to both basic ecology of the species and in management efforts, and any management plan must account for potential impacts of the squid ishery on marine mammal populations (Clarke et al., 1993). 4a) Development of an oxygen-sensing archival tag. Because of the strong link between D. gigas movements and the midwater hypoxic environment presented by the oxygen-minimum layer (OML), efforts to commercially develop an archival tag that also samples oxygen to depths of 1,000 metres should be encouraged. Such tags would also be extremely valuable for studying other species of ommastrephid squid and pelagic predatory ishes, especially tunas, in the eastern Paciic. These ishes must be limited in their ability to forage in the OML, and D. gigas is likely to be the top predator in this vast midwater environment (excluding marine mammals). Utilisation of the OML may be one of the most important biological features of D. gigas, but the present inability to directly relate archival data of vertical and horizontal movements to oxygen levels measured simultaneously is a major limitation. 4b) Understanding the mesopelagic community through new technologies. In order to truly understand how D. gigas utilises the water column, we will have to learn much more about the other organisms that it interacts with at various depths and times. Clearly, D. gigas depends heavily on the mesopelagic micronektonic community on which it feeds. Even though much of the productivity in the eastern Paciic is channelled through this community, dynamics of the energy transfer through this system remain poorly understood. This community is characterised by short-lived (often annual) organisms whose productivity is larger than their standing stock. Such organisms tend to respond quickly to environmental variations, and these responses are likely to be intimately related to historical variations in D. gigas abundance and distribution. Large historical variations are characteristic of scale deposition by myctophids in the deep-basin sediments in the Gulf of California (Holmgren-Urba and Baumgartner, 1993), but this feature has not been well exploited as a tool in studies of midwater ecology. Understanding the community of micronektonic ishes, squid and crustaceans has proven dificult, largely due to major challenges involved in systematic and large-scale sampling efforts, but also due to small-scale problems inherent with net sampling, particularly net avoidance by reactive organisms. Perfection of newer techniques, including acoustic surveys and low-light cameras, promises to greatly aid future research (Benoit-Bird and Au, 2006). Studying dynamics of mesopelagic planktonic communities will be challenging and expensive, but failure to advance in this area will almost certainly preclude achieving a deep understanding of environmental changes and how they are impacting top pelagic predators. The relevant organisms, like myctophids, may be dificult to study and not particularly charismatic, but they really matter. We are reminded of a dictum made by Steinbeck and Ricketts in Sea of Cortez (1941) - “None of it is important or all of it is.” Acknowledgements We acknowledge the support of GLOBEC/CLIOTOP in making it possible to attend the the Role of Squid in Open Ocean Ecosystems workshop. Preparation of this report and the results of our research disussed here were supported by Census of Marine Life through the Tagging of Paciic Pelagics program, National Geographic Society, US National Science Foundation (OCE 0526640) and the David and Lucille Packard Foundation. 87 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA References Abitia-Cárdenas L.A., F. Galván-Magaña, F.J. Gutierrez-Sanchez, J. Rodriguez-Romero, B. AguilarPalomino and A. Moehl-Hitz. 1999. 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Proceedings of the National Academy of Sciences 104(31):12948-12950. 90 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA WORkSHOP PARTICIPANTS Acuña, Enzo Universidad Catolica del Norte Casilla 117 Coquimbo Chile E-mail: [email protected] De Forrest, Lisa Department of Oceanography University of Hawaii 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] Allain, Valérie Oceanic Fisheries Programme Secretariat of the Paciic Community Nouméa New Caledonia E-mail: [email protected] Dewar, Heidi NOAA Fisheries Southwest Fisheries Science Center 8604 La Jolla Shores Drive La Jolla, CA 92037 USA E-mail: [email protected] Arancibia, Hugo Universidad de Concepción Department of Oceanography PO Box 160-C Concepción Chile E-mail: [email protected] Domokos, Reka NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Arkhipkin, Alexander Fisheries Department PO Box 598 Stanley FIQQ 1ZZ Falkland Islands E-mail: [email protected] Drazen, Jeff Department of Oceanography University of Hawaii 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] Baltz, Kenneth NOAA Fisheries Southwest Fisheries Science Center 110 Shaffer Road Santa Cruz, CA 95060 USA E-mail: [email protected] Ferriss, Bridget University of Washington School of Aquatic & Fishery Sciences Box 355020 Seattle, WA 98195 USA E-mail: [email protected] Boecklen, William New Mexico State University Laboratory of Ecological Chemistry Department of Biology MSC 3AF Las Cruces, NM 88003 USA E-mail: [email protected] Galván-Magaña, Felipe Centro Interdisciplinario de Ciencias Marinas Avenida IPN s/n Apdo. Postal 592 La Paz, Baja California Sur México E-mail: [email protected] Camarillo-Coop, Susana Centro de Investigaciones Biológicas del Noroeste, S.C. (CIBNOR) Centenario Norte 53 Col Prados del Centenario CP 83260, Hermosillo, Sonora México E-mail: [email protected] Gilly, William Hopkins Marine Station Stanford University 120 Oceanview Blvd. Paciic Grove, CA 93950 USA E-mail: [email protected] Choy, Anela Department of Oceanography University of Hawaii 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] 91 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Ichii, Taro Oceanic Squid Section National Research Institute of Far Seas Fisheries 2-12-4 Fukuura, Kanazawa-ward Yokohama-City, 236-8648 Japan E-mail: [email protected] Gilman, Eric Blue Ocean Institute Muttontown Park and Preserve 34 Muttontown Lane P.O. Box 250 East Norwich, NY 11732 USA E-mail: [email protected] Glazier, Edward Impact Assessment, Inc. Paciic Islands Ofice 2950-C Paciic Heights Road Honolulu, HI 96813 USA E-mail: [email protected] Itano, David Pelagic Fisheries Research Program Joint Institute for Marine and Atmospheric Research University of Hawaii at Manoa 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] Graham, Brittany Department of Oceanography University of Hawaii 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] Jackson, George University of Tasmania IASOS Private Bag 77 Hobart, Tasmania, 7001 Australia E-mail: [email protected] Hamm, David NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Juanes, Frances University of Massachusetts Amhurst Department of Natural Resources Conservation Amherst, MA 01003 USA E-mail: [email protected] Hochberg, Eric Santa Barbara Museum of Natural History 2559 Puesta del Sol Road Santa Barbara, CA 93105 USA E-mail: [email protected] Kirby, David Oceanic Fisheries Programme Secretariat of the Paciic Community Noumea New Caledonia E-mail: [email protected] Hospital, Justin NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Kiyofuji, Hidetada NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Howell, Evan NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Klieber, Pierre NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Hunsicker, Mary School of Aquatic and Fishery Sciences University of Washington Box 355020 Seattle, WA 98195 USA E-mail: [email protected] Laurs, Michael RML Fishery Oceanographer Consultant 555 Grove Street Jacksonville, OR 97530 USA E-mail: [email protected] 92 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Lehodey, Patrick Marine Ecosystems Modeling and Monitoring by Satellites (MEMMS) CLS 8-10 rue Hermes 31520 Ramonville France E-mail: [email protected] Nielsen, Anders Pelagic Fisheries Research Program Joint Institute for Marine and Atmospheric Research University of Hawaii at Manoa 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] Lutcavage, Molly University of New Hampshire Large Pelagics Research Center G54 Spaulding Life Sciences Center 38 College Road Durham, NH 03824 USA E-mail: [email protected] O’Dor, Ron Census of Marine Life Secretariat Consortium for Oceanographic Research and Education, Suite 420 1201 New York Ave. NW Washington, DC 20036 USA E-mail: [email protected] Mamiit, Rusyan NOAA Fisheries Paciic Islands Fisheries Science Center 1711 East-West Road Honolulu, HI 96848 USA E-mail: [email protected] Olson, Robert Inter-American Tropical Tuna Commission 8604 La Jolla Shores Drive La Jolla, CA 92037 USA E-mail: [email protected] Markaida, Unai Departamento de Aprovechamiento y Manejo de Recursos Acuáticos El Colegio de la Frontera Sur Calle 10 No. 264, Col. Centro Campeche, CP 24000 México E-mail: [email protected] Pan, Minling NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Ming, Timothy NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Parry, Matthew NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Morales-Bojórquez, Enrique Instituto Nacional de la Pesca Centro Regional de Investigacion Pesquera Carratera a Pichilingue Km. 1 CP 23020 La Paz, BCS México E-mail: [email protected] Pierce, Graham University of Aberdeen School of Biological Sciences Tillydrone Avenue Aberdeen, AB24 2TZ UK E-mail: [email protected] Myers, Andy University of New Hampshire Large Pelagics Research Center G54 Spaulding Life Sciences Center 38 College Road Durham, NH 03824 USA E-mail: [email protected] Popp, Brian Department of Geology and Geophysics University of Hawaii 1680 East-West Road Honolulu, HI 96822 USA E-mail: [email protected] 93 The role of squid in open ocean ecosystems, 16-17 November 2006, Hawaii, USA Senina, Inna Pelagic Fisheries Research Program Joint Institute for Marine and Atmospheric Research University of Hawaii at Manoa 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] Pradhan, Naresh Dept. of Molecular Biosciences and Bioengineering University of Hawaii 1955 East-West Road Honolulu, HI 96822 USA E-mail: [email protected] Rieser, Alison University of Hawaii at Manoa Department of Geography 440 Saunders Hall 2424 Maile Way Honolulu, HI 96822 USA E-mail: [email protected] Sibert, John Pelagic Fisheries Research Program Joint Institute for Marine and Atmospheric Research University of Hawaii at Manoa 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] Rosa, Rui Biological Sciences Center University of Rhode Island 100 Flagg Road Kingston, RI 02881 USA E-mail: [email protected] Swimmer, Yonat NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Ruiz-Cooley, Iliana New Mexico State University Department of Biology MSC 3AF Las Cruces, NM, 88001 USA E-mail: [email protected] Walsh, William Pelagic Fisheries Research Program Joint Institute for Marine and Atmospheric Research c/o NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Sakurai, Yasunori Graduate School of Fisheries Sciences Hokkaido University Hakodate, Hokkaido 041-8611 Japan E-mail: [email protected] Wong, John Pelagic Fisheries Research Program Joint Institute for Marine and Atmospheric Research c/o NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Salinas-Zavala, César Centro de Investigaciones Biológicas del Noroeste, S.C. (CIBNOR) Centenario Norte 53, Col Prados del Centenario CP 83260, Hermosillo, Sonora, México E-mail: [email protected] Young, Jock CSIRO Marine & Atmospheric Research GPO Box 1538 Hobart, Tasmania, 7001 Australia E-mail: [email protected] Seki, Michael NOAA Fisheries Paciic Islands Fisheries Science Center 2570 Dole Street Honolulu, HI 96822 USA E-mail: [email protected] Young, Richard Department of Oceanography University of Hawaii 1000 Pope Road Honolulu, HI 96822 USA E-mail: [email protected] 94