Cephalopods caught on theouter Patagonian shelf and its upper and medium slope in relation to the main oceanographic features

Ángel Guerraa, *, Julio M.Portelab, José Luis del Ríob

a Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, 36208 Vigo, Spain

b Instituto Español de Oceanografía (IEO) , C. O. de Vigo.P. O. Box 1552, 36200 Vigo, Spain.

Abstract

Ninety cephalopod specimens were collected in 71 of 132 hauls (54%) during the bottom trawl survey ATLANTIS 2009 undertaken between 24 February and 1 April 2009. The surveyed area was the zone between parallels 44° and 48°South, east of the Argentinean Exclusive Economic Zone down to the 1500m depth contour on the high seas of the Southwest Atlantic.The collection was composed of 16 species of squids and 5 of octopods. The best represented groups were Histioteuthidae (5 species) and Octopodidae (5).The most abundant species were Gonatus antarcticus (25.5%), Histioteuthis atlantica (11.1%), andMuusoctopus eureka (8.9%), which were also the most widely encountered.The geographic and/or bathymetric distribution ranges of 9 species are extended, and this is the first record ofGaliteuthis glacialisoutside circumpolar Antarctic waters. Our data show that several species, mainly of octopuses, penetrate the area studied as theplume of cold sub-Antarcticwatersis pushed far into the South Atlantic by the Falkland (Malvinas) Current.

Keywords: Cephalopods, Biogeography, Patagonian slope, Southwest Atlantic.

Running title: Cephalopods from the Patagonian slope

* Corresponding author at: Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, 36208 Vigo, Spain. Tel.+34 986231939 ext. 180; Fax: +34 986 292762

E-mail address: (A. Guerra).

1. Introduction

The Southwest Atlantic Ocean (SWA) supports two major cephalopod fisheries. One is focused on the Patagonian long-finned squidLoligo gahi and the other on the Argentine short-finned squid Illex argentinus. Although there is considerable information on these 2 species along the continental shelf within the Argentinean and UruguayanExclusive Economic Zones (EEZ) (Nigmatullin, 1989; Basson et al., 1996; Agnew et al., 1998;Haimovici et al.,1998; Bunetti et al.,1999; Agnew et al., 2005; Portela et al., 2010), mainly around the Falkland (Malvinas) Islands (e.g. Arkhipkin et al., 2004; Bazino et al., 2005; Sacau et al., 2005), very little research has been carried out on the High Seas (HS) region.The recently developed Falkland (Malvinas) fishery regularly catchesoctopuses during survey trawls as does the Falkland Islands Government Fisheries Department (FIGFD)through observers attending commercial trawling operations on the South American continental shelf in the SWA, and research received a further boost when the FIGFD funded a study to identify the octopuses in their fisheries collection (Gleadall et al., 2010). Recently, L. gahi, I. argentinus, Onykia ingens, and Gonatus antarcticus have also been shown to occupy the ecological niche of epipelagic fish on the Falkland (Malvinas) shelf and slope (Laptikhovsky Arkhipkin, 2010).

Many papers have been devoted to discovering knowledge of the teuthofauna from the Antarctic waters (see, for example, Rodhouse, 1989, andGleadall et al., 2010, and the literature cited therein). However, little attentionhas been paid to the cephalopod species from the Argentinean shelf and even less to the biodiversity presentin the Patagonian upper and medium slope. Practically the only data available came from the cruises carried out by Rodhouse et al. (1992) devoted to the early life cycle of cephalopods, which surveyed a wide area using RMT8 and Bongo nets, and associated the captures withthe major oceanographic features of the SWA.

This paper examines the collection of cephalopod gathered in the cruise ATLANTIS 2009 carried out in the HS of the SWA, including the outer Patagonian shelf and the upper and medium slope, in relation to the main oceanographic features of the SWA. It also aims to contribute to the knowledge of the teuthofauna in the region, the taxonomy of the material collected, as well as its geographical and bathymetric distribution.

2. Study area

The area surveyedwas the zone between parallels 44° and 48°South, east of the Argentinean EEZ down to the 1500m depth contour (Fig. 1), and the depth of the trawls ranged from 107 to 1527m. The physical oceanography of this area—virtually opposite the Gulf of San Jorge on the Argentinean coast—is complex.We therefore present a schematic scenario, which will allow us to understand the main features that occur in the study area. The major oceanographic features of the SWAare the Brazil Current (BC), the Falkland (Malvinas) Current(FMC),and their confluence region. The BC originates as a branch of the South Equatorial Current (around 08°South) and runs poleward almost parallel to the shelf break. It is tropical in origin and is therefore warm, saline, and relatively oligotrophic.The southern limit of the warm water associated with the BC fluctuates between 36°-38°and 46°South, and is accompanied by the intermittent formation of warm-core, anti-cyclonic eddies (Campos et al., 1995).The encounter between the warm southward flowing BC and the cold northward flow of the FMC, at approximately 38°South, generates a strong thermohaline front: the Subtropical Convergence or Subtropical Zone (STZ).The cool, nutrient-rich FMC branches off the Antarctic Circumpolar Current and flows northward along the Patagonian continental slope.This current flows round both sides of the Falkland Islands before turning northward once again as a single flow, approximately 100km wide. The FMC is the dominant circulation feature along the Falkland Shelf Break.The sub-Antarctic waters from the FMC flow along the shelf as far north as 32°South before returning south as the Falkland (Malvinas) Return Current and flowing offshore at the confluence zone. Thesurface water temperatures in the northerly flowing coastal current, between 24° and 33°South, are several degrees lower than the Brazil Current and consist of a mixture of cool water from the FMC and warm water being recirculated from the BC.Brazil Current waters have a temperature of>20.0°C and salinity of >36.0, while FMC waters have a large temperature range between 4.0 and 15.0°C, but a narrow salinity signal between 33.7 and 34.1. Because of the large differential between these salinity ranges specified for the Brazil and FMCurrents, a large proportion of the water sampled can be expected to have mixed characteristics(Wilson and Rees, 2000 and references therein).

Using the nomenclature for the fronts and zones adopted by Peterson and Whitworth (1989), the three zones south of the STZ associated with the Antarctic Circumpolar Current are, from north to south, the Sub-Antarctic Zone (SAZ), the Polar Frontal Zone (PFZ),and the Antarctic Zone (AZ). These zones are associated with fronts (Fig 2).

3. Material and methods

A multidisciplinary research cruise was conducted by the Spanish Institute of Oceanography (IEO) to assess the biomass of the main commercial fish stocks on the HS of the SWA and to identify Vulnerable Marine Ecosystems (VME). The multidisciplinary bottom trawl survey (ATLANTIS 2009), undertaken between 24 February and 1 April 2009on board the RV Miguel Oliver, included 132 trawl stations (Fig.3 Table 1). The survey used a stratified random design with strata boundaries defined by latitude and depth ranges. Scheduled fishing stations (hauls of 30 min) were performed using a LOFOTEN type net fitted with a “Rockhopper” mix train with bobbins and rubber separators, suitable for deepwater fishing over irregular bottoms. The headline height averaged 6.1m, with a wing spread of 20m. Mesh size rangedfrom160mm in the upper wings to 40mm in the codend liner. Trawling was restricted to daylight hours. The positions of the hauls were randomly chosen prior to starting each stratum survey.

Thirteen depth strata were defined in the study area (Table 1) and were further subdivided into 2571 grids of around 5 square nautical miles (nm2). Finally, 147 hauls were randomly allocated according to the following criteria:

i) The number of hauls in each stratum was proportional to its surface, with a minimum of 2 hauls per stratum; ii) For each stratum, hauls were randomly allocated among all possible grids, excluding those in adjacent squares; iii) When fishing was not possible in a selected grid due to bottom characteristics, the haul was put in the nearest square allowing for bottom trawling.

Only 132 hauls were performed out of the 149 planned, as characteristics of the seafloor hindered bottom trawling, mainly in stratum 7 (1001-1500m depth). Moreover, 5 of the hauls were considered null for different reasons, such as net breakage or net entanglement. Table 1 shows the scheme of fishing stations by depth stratum and summarizes their main characteristics: depth range (m), surface(nm2), and number of grids per stratum.Hydrographical parameters (sea surfacetemperature [SST],sea bottom temperature [SBT], and salinity) were collected during the cruise using a CTD-probe.

Catches were sorted immediately after capture. Cephalopods were stored in labelled plastic boxes and frozen at -20ºC on board. Specimens were taken by the vessel to Vigo (Spain) where the samples were transported to the Instituto de Investigaciones Marinas (IIM, CSIC) marine research laboratory for detailed examination.

After defrosting at room temperature, cephalopods were identified from published guides,and old (e.g. Nesis, 1987; G. Voss, 1978; N. Voss et al., 1998) and recent papers (e.g. Guerra et al., 2000; Lipinski, 2001; Allcock et al., 2004; Vecchione et al., 2005; Gleadall et al., 2010). Total length (TL), dorsal mantle length (ML),and wet weight were measured immediately, and the sex was also determined.

All the material caught on this cruise, except Batoteuthis skolops,which is in the National Museum of Natural History (WashingtonD.C., USA), has been deposited at the Museo do Mar de Galicia (Vigo, Spain-

4. Results

Locations of trawls conducted during the ATLANTIS 2009 survey are shown in Fig.3. The typical range of SST, SBT, and salinity at the different zones, or the oceanographic features cited in the text and Fig.2 are shown in Table 2.

During the cruise, 90cephalopod specimens, comprising 16 squids and 5 octopods, were collected. Depth ranges of capture and numbers of hauls with cephalopods catches are shown in Table 3. Cephalopods were present in 71 of the 127 valid hauls (56%) carried out during the cruise. The family of squids best represented was Histioteuthidae with 5 species,while the Octopodidae was represented with 5 species (Table 3).The most abundant squids were of the Gonatus antarcticus Lönngerg, 1898, species(25.5%), followed byHistioteuthis atlantica(Hoyle, 1885) (11.1%). The most abundant octopus species (8.9%) was Muusoctopus eureka (Robson, 1929).G. antarcticusalso appears to be the most diverse spatially and was captured at 14 stations (Table 3). However, the distribution of H. atlantica and M. eureka, which appear in 8 stations, respectively, also have a wide geographical area of distribution within the limits of the total area explored.

Size and some other biological data of captured specimens and families (10) of each species are detailed in Table 4.

Table 5 shows the cephalopod distribution caught during this cruise in relation to the major oceanographic features of the study area.

5. Discussion

Six specimens of Brachioteuthidaeshare the diagnostic characters ofSlosarczykovia circumantarctica Lipinski, 2001. This is one of the most common squids in Antarctic waters (Lipinski and Young,

Until now, very few specimens of Batoteuthis skolopsYoung and Roper, 1968 have been collected (Young Roper, 1968;Rodhouse et al., 1992; Young and Roper The speciesis found only in Antarctic and sub-Antarctic waters and little is known of its biology. Due to the interest in our specimen, we plan to present a detailed description and discussion elsewhere.

The taxonomy of the octopuses is still undergoing majorrevision (see,for example, Norman Hochberg, 2005)and to date incirrate octopuses have yet to be the subjectof a comprehensive study using nucleotide sequencedata. Such data are now being collected and research isalso under way to provide clear species re-descriptionsbased upon morphometric data, leading to a much betterunderstanding of the major groups and biodiversity ofshallow water octopuses (Gleadall et al., 2010).These authors have describedthree inkless octopodids from the continental shelf off south-easternSouth America. These octopuses are a non-commercial by-catch in the Falkland (Malvinas) fishery. Muusoctopus eureka (Robson, 1929) is one of two common inkless octopuses, is of medium size, withorange-pink skin, and a distinctive pattern of irregular dark markings, interspersed with white spotsvisible only in living or freshly dead specimens. Eight specimens caught in our cruise belong to this species. Another 4 specimens also captured during our cruise belong to Muusoctopus longibrachus akambeiGleadall et al., 2010.

Two specimens (21-30mm ML) of the Patagonian bobtail squidSemirossia patagonica(Smith, 1881) were caught on the Falkland (Malvinas) shelf by an RMT8 net from the surface to the bottom (Rodhouse et al., 1992). The species have also been collected on the Argentinean shelf (Reid Jereb, 2005). The records presented here represent an expansion of the geographical range of the species eastwards. According to depth, SST, and SBT (Table 2),our specimens werecaught in theSTZ, usually located between 35°and 45°South, where the average SST changes from about 12°C to 7-8°C(Campos et al., 1995). One specimen of the bobtail Austrorossia mastigophora (Chun, 1915) was also captured in this STZ (45°46'30'' South -60°27' 29'' West). The known geographical distribution of this bobtail squid was western, southern, and eastern Africa (from Guinea and Somalia to the Cape of Good Hope), but doubtful in Chilean waters (Reid and Jereb, 2005). Therefore, this is the first time that the speciesis caught in the western part of the South Atlantic Ocean. The Carol bobtail squidNeorossia caroli(Joubin, 1902) was caught south more frequently than the previous bobtail squids (47°32' 60'' South -60°14' 19'' West) and inthe deeper, cooler waters (Table 2) of the FMC. This speciesis representedon the Patagonian slope north of the Falkland (Malvinas) Islands by the subspecies N.caroli jeannae Nesis et al., 2001, while our specimenwas recorded much further north than any other until now.

The jewel squidsHistioteuthis reversa (Verrill, 1880), H. atlantica (Hoyle, 1885), H. bonnelli (Férussac, 1834), and H. eltaninae N. Voss, 1969 caught are common in the area explored by our cruise, showing an already well-known vertical and geographic distributioninside the FMC (Voss et al., 1998). However, this is the most southern record (45°13' 52'' South -59°24' 04'' West)of Histioteuthis arcturi(Robson, 1948), which had previously only been registered between 28°North and 25°South (Voss etal., 1998).

To date, the known distribution of the squidSlosarczykonia circumantarctica was off Wilkes Land (Australian Antarctic Territory) and in circumpolar Antarctic waters (Lipinski and Young Our findings extend the geographical distribution area of the species towards the north and east of the SWA, occupying the western border of the FMC (from approximately 46°54' South - 59°49' West to 45°17' South -59°33' West), at depths ranging from 881 to 1224m, and SST and SBT between 11.9 and 2.3ºC, respectively (Table 2).

According to the map of the records of B. skolops provided by Young and Roper ( record is the most northern for this species (44° 30' 22'' -44°29' 54'' South).

The glacial cranch squid Galiteuthis glacialis (Chun, 1906) is found throughout the circumpolar Antarctic waters where it is one of the most abundant (Nesis, 1987). According to the map given by Young and Mangold ( our records are the first outside circumpolar Antarctic waters, thus expanding the geographical distribution of the species towards the north, at least until 44° 02' 95'' South. SST and SBT seem to indicate that this species was caught along the western border of the FMC.

Type locality of Graneledone antarctica Voss, 1976 is theRossSea (74°05' 06'' South, 175°05' 02'' West) (Voss, 1976). However, Kubodera and Okutani (1994) captured1 specimen at 45°44' South, 59°46' West at 858m depth, which is close to our area of study and within the bathymetric range of our specimens (Table 3). Despite the resemblance of theKubodera and Okutanispecimen toG. antarctica, these authors did not risk identifying it as such. Their argument was that it was captured near the CrozetIslandsat such a considerable distance that they hesitate to conclude that the material was conspecific. Nevertheless, the coordinates ofcapture that the authors givetwice (their Table I and on page 214) do not correspond to these islands but to the Patagonian shelf or south-eastern Argentinean EEZ waters, where they also obtained some samples. Our specimens (1 juvenile and 2 immature female, Table 4) share the diagnostic characters of the species. Considering this information, we therefore believe that the species is present off the Patagonian shelf at depths of1156-1461(Table 3) and from 44º to 47º South.The species was found in the western boundary (59º25' West) of the FMC, where the SST was 9.7ºC and the SBT 2.4ºC (Table 2).

The large-tuberculate octopusGraneledone macrotyla Voss, 1976 was for many years only known bytype-locality (54°43' South, 55°30' West in 1647-2044m) (Voss, 1976, 1988). However, the collection studied by Kubodera and Okutani (1994) extended the known distribution of the species to the north of 45°South along south-eastern Argentina, at depths ranging from 858 to 2044m, which agrees with the latitudinal distribution shown by the present sample (from 45° to 47° South). The western range where this species was caught (59° 32' -60°01' West) and the SST and SBT (Table 2) suggest that it inhabits the northern part of the FMC.

Our 4 mature males of Thaumeledone gunteriRobson, 1930 share the main characters given by Allcock et al. (2004). These authors indicated that the distribution of this species is probably restricted to South Georgia and Shang Rocks at a depth of 366-964m and probably deeper. However, we found this inkless octopus further north, at depths ranging from 855 to 1190m, with a sea surface temperature of 9.6ºC, and a sea bottom temperature of 2.6ºC (Table 3).

Laptikhovsky (2001) reported 32 females of Benthoctopus eureka collected on the Falkland (Malvinas) shelf (48°40' -52°59' South, 56°51' -60°15' West, depth range 125-344m) during expeditions on board the RV Dorada. Gleadall et al. (2010) are currently proposinga new taxonomic combination for eureka, which is Muusoctopus eureka (Robson, 1929). The species was caught in the same area explored by our cruise. However, the specimens were mainly on the 200mdepth contour (Gleadall et al., 2010), whereas the bathymetric range of the 8 specimens included in this paper was111 to 1156m.Therefore, it seems that this species is adapted to a relatively wide range of temperature, possibly from 8ºC to -0.8ºC (Tables 2 and 5).