Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

Contents lists available at SciVerse ScienceDirect

Journal of Experimental Marine Biology and Ecology

j ourna l homepage: www.e lsev ie r .com/ locate / jembe

Investigating the movements and behaviour of Patagonian toothfish(Dissostichus eleginoides Smitt, 1898) around the Falkland Islandsusing satellite linkedarchival tags

Judith Brown a,c,d,⁎, Paul Brickle b,c,d, Beth E. Scott c

a St. Helena Government, Essex House, Jamestown STHL 1ZZ, Saint Helenab South Atlantic Environment Research Institute, P.O. Box 609, Stanley FIQQ 1ZZ, Falkland Islandsc University of Aberdeen, School of Biological Sciences (Zoology), Tillydrone Ave., Aberdeen AB24 2TZ, UKd Falkland Islands Fisheries Department, P.O. Box 598, Stanley FIQQ 1ZZ, Falkland Islands

⁎ Corresponding author at: St. Helena Government, essSaint Helena. Tel.: +290 2270.

E-mail address: jude@dicksonandbrown.com (J. Bro

0022-0981/$ – see front matter © 2013 Elsevier B.V. Allhttp://dx.doi.org/10.1016/j.jembe.2013.02.029

a b s t r a c t

a r t i c l e i n f o

Article history:Received 22 April 2012Received in revised form 12 February 2013Accepted 13 February 2013Available online 19 March 2013

Keywords:Archival pop-up tagsFalkland IslandsFeeding behaviourPatagonian toothfishSpawning migration

Knowledge of the seasonal movements of Patagonian toothfish is an essential component for understandingtheir ecology and fisheries management. As only one demersal longline vessel participates in this fishery inFalkland's waters, over a vast slope area, the use of conventional tags to provide data on migration or stockassessment is not viable. In contrast, archival pop-up tags have enabled the examination of toothfishmovementswithout having to recapture tagged individuals with reasonably high success rates. Patagonian toothfish (n=30,>127 cm LT) were tagged with pop-up satellite tags between 19/09/2007 and 7/07/2010 in the South Atlanticclose to the Falkland Islands. The data from 16 tags that successfully released and uploaded data (plus onerecapturedfish) revealed strong site fidelity,with eleven toothfishmoving less than 50 km from their release po-sition over a 6 month period. Furthermore, depth data inferred three behavioural patterns showing seasonalbathymetric movements, foraging and spawning activities. Coinciding with the reported spawning months ofJuly–August, spawning movements were recorded with fish moving repeatedly into shallower waters of 900–1200 m. Foraging behaviours were also evident with differences in the scale of foraging movement related tofish size, possibly linked to a shift in diet with size. Fish were found to move deeper during December andthese are potentially post-spawningmovements allowing the fish to take advantage of different prey availability.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

The Patagonian toothfish (Dissostichus eleginoides) is a deepwater longlived notothenid (Collins et al., 2010) which has been exploited commer-cially around the Falkland Islands since 1994 (Laptikhovsky and Brickle,2005). Due to its longevity and growing commercial value gathering in-formation on the movements of Patagonian toothfish and understandingtheir ecology and behaviour are essential components of their fisheriesmanagement. Advances in technology in recent years have seen the de-velopment of archival pop-up tagswhich allow for the examination ofmi-gratorymovements of fish and sharks (Pade et al., 2009), aswell as givinginsights into behaviour (Seitz et al., 2005; Stevens et al., 2010), withoutrequiring retrieval of the tagged animal.With only one demersal longlineroperating in Falkland's waters and a vast slope area (approximately150,000 km2), the use of conventional (T-bar) tags would not be viablefor studying toothfish as a huge number of fish would need to be taggedto guarantee returns which would be uneconomic commercially. Hence,

ex House, Jamestown STHL 1ZZ

wn).

rights reserved.

archival tags provide a fishery-independent means of studying toothfisharound the Falklands in their natural environment.

Fish often migrate to find favourable conditions for spawning anddevelopment of their young (e.g. Atlantic salmon, Salmo salar; eels,Anguilla anguilla) however, the energetic investment in large distancefishmigration is high (Crossin et al., 2004). A triangularmigration pat-tern was suggested by Harden Jones (1968) to occur in many specieswith adults swimming ‘up current’ to spawn, then the young are car-ried to good feeding areas by the currents and then once the younggrow to become larger active swimmers they move to adult feedinggrounds. In the case of Patagonian toothfish, juveniles are known tomigrate from the shelf and slope (at depths of 150–400 m) intodeeper water (400–>2000 m) as they become adults and they alsochange their diet (Arkhipkin et al., 2003). From examination oftoothfish maturity, Laptikhovsky et al. (2006) reported toothfish tomigrate from the Burdwood Bank after spawning, northward to 40–45°, westwards to Chilean waters and eastwards to the Scotia ridge.In other areas toothfish are reported as non-migratory (DeWitt et al.,1990; Williams et al., 2002).

Previous tagging experiments on Patagonian toothfish (using con-ventional t-bar tags) have provided data on the dispersal of fish, growthduring deployment time and for use in stock assessment (via mark

66 J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

recapture studies). This range of studies on both D. eleginoides and itssister species Dissostichus mawsoni, have revealed that generally fishshow strong site fidelitywith individuals remaining near to their releasepoint usually b50 km (Dunn et al., 2007; Marlow et al., 2002; Williamset al., 2002) with a mean annual movement rate of 10 km/year (Agnewet al., 2006) These studies all showed that a few individuals, however,moved much greater distances between 200 and 2300 km. Geneticstudies investigating differentiation between toothfish stocks haveshown very restrictive gene flow, also suggesting limited adult migra-tions throughout the region (Appleyard et al., 2002; Rogers et al.,2006; Shaw et al., 2004; Smith and McVeagh, 2000).

The only study of D. eleginoides using archival tags (DST milli datastorage tags not popup) was trialled at Heard Island by Williams andLamb (2002) and data were collected from fish over periods of 27–59 days in depths of 400–780 m (N=7, 71–81 cm LT). They concludedtoothfish behaviour was complex with movements driven by a combi-nation of factors including environmental parameters (day and lunarphase), behaviour of prey species and bottom topography.

This study aimed to investigate routes and extent of migration ofadult toothfish in Falkland's waters. Knowledge of toothfish migrationbehaviour is vital for stock assessment. As far as we are aware this isthe first time archival tags have been used for prolonged periods (upto 180 days) at depths of >1000 m and hence, as well as gaining in-sight into migration of D. eleginoides around the Falklands these tagsallowed data to be gathered on daily behaviours of adult toothfish intheir natural environment.

2. Materials and methods

Toothfish for the purpose of tagging with pop-up tags, were cap-tured during commercial fishing and experimental research cruisesonboard the longliner CFL Gambler, using traditional Spanish long-lines. Fish were tagged in two separate areas (Fig. 1), in the north of

Fig. 1. Driftmovements ofMK10 satellite tags used for taggingDissostichus eleginoides after pop

the Falklands Outer Conservation Zone (FOCZ) (north of 53.5°S, 054–060°W), and one fish on the north of Burdwood Bank, in the expectedfeeding grounds of toothfish (eight fish tagged in March 2008 and fivein April/May 2009) and in the south of the FOCZ (south of 53.5°S, 054–058.5°W), along the south of Burdwood Bank during the spawningseason (two fish tagged in September 2007, five in August 2008, fivein September 2009 and five in May 2010). As the tagged fish swamto the seabed on release, the lines were set at depths between 750and 1460 m (i.e. b1800 m) to prevent the activation of the 1800 mdepth release device which is part of the pop-up tag. For each taggedfish, LT (cm), Floy tag number, pop-up satellite tag number, oxytetra-cycline dose (20 mg OTC per kg — acts not only as an antibiotic butalso marks the fish otolith should the fish be recaptured at a laterdate), station number, release date and time, water depth at releasesite and release location (from the vessels global positioning system)were noted. Due to the risk of losing the tagged fish to predation bysperm (Physeter macrocephalus) or killer whales (Orcinus orca), ifany whales were seen during a line being hauled the tagging wasabandoned for that line.

Thirty Wildlife Computers Limited Mk10 — Popup Archival Tags(PAT) were used during this study. They were programmed to recorddepth, external (environmental temperature) and light level (used tocalculate end location position) with sampling frequency of 1 s, 1 sand 10 s respectively. The Mk10 tags have a temperature resolutionof 0.05 °C from −40 °C to 60 °C and they are calibrated to 0.1 °Cfrom 2 °C to 40 °C. For depth, the tags are calibrated from 0 to1000 m with a resolution of 0.5 m, ±1%. Tags were programmed tosummarise data in histograms in 6 hourly periods with temperaturebins set at 0, 0.5, 1, 1.5, 2, 2.5, 3, 3.5, 4, 5, 6, 7, 8 and >8 °C and depthbins set at 0, 500, 600, 700, 800, 900, 1000, 1100, 1200, 1300, 1400,1500, 1600 and >1600 m. Tags were attached to the fish in the dorsalmuscle using a flat titanium dart and 10 cm of high strength clear1 mm diameter monofilament fishing line. The MK-10 PAT's were

-up andwhilst on the surface around the Falkland Islands. Square donates pop-up position.

67J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

programmed to detach after 180 days deployment or if the fish haddied (tag stationary for greater than a preset time — set at 48 h). Thetags were deployed with an RD1800 release device which has a me-chanical guillotine activated by water pressure when depths exceed1800 m. Once on the surface tags relayed data via the Argos satellitesystem.

Using bathymetric data collected on research cruises (conducted bythe Falkland Islands Fisheries Department between 1998 and 2009)depth contourmapswere constructed (showing200 mdepth contours)in Surfer® using a griddingmethod (using a standard kriging algorithmwith a linear variogram model for interpolation of the data). Surfaceplots for tag depth data for each fish were produced in Excel® to allowthe rapid identification of periods of relative quiescence and times offish behaviourwhere therewere greatermovements. Periods of relativequiescence (i.e. when the fishmoves less than 100 m either through thewater column or upslope/downslope) were examined at a higher tem-poral resolution for links with lunar phase and direction of movementusing a two way ANOVA. This was conducted by taking the mean ofthe depths recorded within a 6 h period, then using the data for thewhole deployment a time period, which showed relative quiescence,was selected and the mean (base depth) worked out over that period.The change in the mean vertical depth for the 6 h period compared tothemean “base” depth gave either an upward or downwardmovementwhich was then compared with lunar/tidal phase.

To examine any difference in foraging behaviours related to size aMann Whitney test was used to examine the vertical movement fortwo size categories of fish (data pooled for fish 130–148 cm and forfish 149–160 cm). These data were non-parametric as determinedby a Shapiro–Wilk test. For this analysis, only fish in the south wereexamined as the bathymetry is different to that in the north; i.e. inthe south the slopes are steep and fish can move both upwards anddownwards along the seabed or into the water column whereas inthe north, the seabed is more gently sloping and so only movementsup into the water column are possible.

3. Results

3.1. Tag deployment information

Details from the 30 deployed tags and, where successful, informa-tion after the tag has released from the host fish and transmitted itsdata via the Argos system are given in Table 1. In all cases after tag-ging and releasing, the fish was seen swimming off in a downwardsdirection.

3.2. Tag losses/problems

Of the 30 tags deployed eight did not transmit at all, one fish wasrecaptured by the fishing vessel (Floy Tag 1758) without the satellitetag and five tags popped-up the same day or next day after deploy-ment (two due to activation of the RD1800). Of the 16 tags whichdownloaded data, seven popped up on their due date 180 days afterdeployment. Nine tags popped up early (between 59 and 132 daysprematurely) and of these three were due to the activation of theRD1800 device when the fish went deeper than 1800 m; two poppedup when the longline vessel was fishing nearby; and the remainingfour the reason for premature release is unknown (two downloadedinsufficient data).

Three tags had a delay between the pop-up date and the date offirst position (7–11 days). An estimation of the pop-up position waspossible using the drift patterns from the other tags once they wereon the surface and the knowledge of oceanographic current patternsin the area (Glorioso et al., 2005). Fig. 1 shows all the drift movementsof the tags and it can be seen that tags which popped up on theBurdwood Bank drifted northwards through the gap between theBurdwood Bank and the Scotia Ridge carried by the Falklands current.

3.3. Fish movements

All five fish tagged to the north and east of the Falklands showedstrong site fidelity, with all moving less than 130 km (four fishmoved less than 30 km) from their deployment location over a sixmonth period from March/April (Fig. 2A). The fish which moved126.8 km swam to the north west of its deployment position. Fivetags deployed on the Burdwood Bank showed another five fish withstrong site fidelity, all moving less than 50 km from their deploymentlocation over a six month period from August/September (Fig. 2B).Three tagged fish moved from the Burdwood Bank eastwards towardsthe Scotia Ridge and one tagged fishmoved 129 km to the north of theBurdwood Bank over a six month period from August (Fig. 2C). Ofthese four tagged fish which moved distances of >100 km from thesouth of the Burdwood Bank, one tag only provided a final position(Tag 86847) but as there was an incomplete data record for this tagit could have drifted for a few days before the pop-up position wasdetected. The other three tags all spent 7–11 days drifting on the sur-face prior to giving an initial position. Therefore surface drift patterns,depth data combined with bottom bathymetry and knowledge of cur-rents have been used to estimate the point the tag popped up. Takingthis into account it appears that the fish with Tags 86848 and 86849had moved less than 50 km eastwards along the Burdwood Bank(after 85 and 139 days at liberty respectively). For all tags, as the ini-tial tag depth data matched the contour depth at deployment positionand the last bottom depth matched the depth at end pop-up position,it was possible to use the depth data and the bathymetry to plot a po-tential migration route of the fish to the end location position.

3.4. Temperature data

Water temperatures recorded by the tags ranged from 1.8 to 4.4 °C(mean ranged from2.3 to 3.2 °C)with the lower temperatures recordedat the greater depths and during winter (June–August).

3.5. Behaviour patterns from depth data

Three different vertical movement patterns were detected whichare interpreted as seasonal, foraging and spawning behaviour.

3.5.1. Seasonal behaviourThe first of these vertical movement patterns occurred on certain

months and involved changes in depth from a base depth (basedepth refers to a depth from which the fish makes small (b60 m)daily upwards or downwards movements but returns to the meanbase depth), moving deeper or shallower and then remaining at thisnew mean base depth for some time. For example, many of the fish(6 tags) appeared to settle at a slightly greater depth initially after tag-ging and then moved slightly shallower (1–10 days later). Three fish(Tags 77209, 77210 and 86849) alsomoved 250–400 mdeeper duringDecember, with two of these moving shallower again in January(Fig. 3).

3.5.1.1. Foraging behaviour (in the south). The second distinctive move-ment pattern we attributed to foraging behaviour and involved pe-riods of relative quiescence, remaining at a constant base depth butwith movements of up to 60 m although generally less, over a 6 h pe-riod (Fig. 4A and B).

Investigating relationships between these small movements withlunar phase showed that in five fish, out of twelve, there was a signif-icant link (i.e. Pb0.05) (Table 2).

Examining relationships between vertical movement and fish size(Fig. 5) showed that for fish in the south, larger fish (149–160 cm)made smaller movements, median vertical movement 24 m (IQR 16–32 m) over a 6 h period, than smaller fish (130–148 cm), mean verticalmovement 40 m (IQR 32–56 m). Difference in vertical movement was

Table 1Pop-up information from satellite tags deployed on Dissostichus eleginoides around the Falkland Islands.

ARGOS PTTnumber

Pop-up date FishLength

Days at liberty(days)

Reason for pop-up Pop-up position Distance moved(km)

Days on surface tillfirst position

Zone

77206 Not recovered 145 – – – – – –

77207 Not recovered 141 – – – – – –

77208 Not recovered 146 – – – – – –

77209 18/01/08 155 121 Fish went >1800 m 54.41°S 051.78°W 281.9 11 South (Scotia Ridge)77210 17/03/08 150 180 Due 54.87°S 056.00°W 5.4 0 South (Burdwood Bank)77211 Not recovered 189 – – – – – –

77212 Not recovered 132 – – – – – –

77213 14/09/08 149 180 Due 54.64°S 055.29°W 1.9 0 South (Burdwood Bank)77214 Not recovered 150 – – – – – –

77215 25/09/08 136 180 Due 48.96°S 055.15°W 10.9 0 North86846 09/02/09 138 180 Due 54.87°S 056.30°W 15.2 0 South (Burdwood Bank)86847 13/11/08 134 92 ? 53.95°S 050.23°W 417.2 ? South (Scotia Ridge)86848 13/11/08 138 85 ? 54.74°S 054.46°W, 129 7 South (Burdwood Bank)86849 06/01/09 152 139 Fish went >1800 m 54.30°S 055.52°W 100 7 South (Burdwood Bank)86850 06/02/09 154 177 Fish caught (no satellite tag) 55.09°S 057.19°W 48.1 0 South (Burdwood Bank)86851 27/10/09 127 180 Due 49.61°S 054.79°W 8.4 0 North86852 07/08/09 132 98 Fishing nearby 48.92°S 055.75°W 126.8 0 North86853 29/10/09 129 180 Due 50.22°S 054.86°W 28.2 0 North86854 Not recovered 143 – – – – – –

86855 26/08/09 140 114 Fishing nearby 51.28°S 055.17°W 13.4 0 North96253 07/09/09 129 0.5 Tag not in correctly 55.11°S 055.60°W 92.3 4 South (Burdwood Bank)96254 07/09/09 127 0 Tag not in correctly 55.14°S 055.52°W 97.9 4 South (Burdwood Bank)96255 29/06/10 140 48 55.02°S 055.52°W South (Burdwood Bank)96256 14/07/10 147 63 54.53°S 056.26°W South (Burdwood Bank)96257 23/07/10 139 7296258 13/05/10 159 1 Fish went 1792 m 55.43°S 054.56°W 0 South (Burdwood Bank)96259 Not recovered 139 – – – – – –

96260 07/09/09 135 0.5 Fish went 1768 m 55.30°S 054.98°W 87.6 5 South (Burdwood Bank)96261 06/03/10 134 180 Due 55.06°S 057.02°W 14.5 0 South (Burdwood Bank)96262 07/09/09 172 0.5 Tag not in correctly 54.86°S 055.59°W 78.6 4 South (Burdwood Bank)

68 J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

significantly different (Pb0.001;MannWhitney U=84,590 n=677 for130–148 cm and n=619 for 149–160 cm).

3.5.1.2. Foraging behaviour (in the north). The five fish deployed in thenorth of Falkland's waters generally remained at a constant depth (fishwith Tag 77215 at 1400 m (±20 m), fish with Tag 86851 at 1200 m,fish with Tag 86852 at 1260 m, fish with Tag 86853 at 1410 m andfish with Tag 86855 at 1180 m) and making numerous, usually up-wards, movements of 20–150 m for short periods before returning tothe original depth (generally less than 6 h).

3.5.2. Spawning behaviourThe third type of movement corresponded to the known spawning

period of toothfish and comprised of numerous depths changes of100–580 m but returning to the base depth (Fig. 6). These activitiesweremovements up into shallower water of 900–1200 m and occurredduring February/March (fish with Tag 77210), May–August (fish withTag 77213) and August (fish with Tags 86846 and 86848).

For the fish with Tag 77213 these upwards movements occurredmainly during the late afternoon (14.00) with the returning downwardmovement to the base depth occurring during the night (02.00 am) andearly morning (08.00 am).

4. Discussion

With the advancements in technologies, it is no longer necessary torecapture tagged fish to retrieve data about their movements (Pade etal., 2009). As far as we are aware this investigation is the first usingsatellite pop-up tags to study fish which spend prolonged periods atdepths of >1000 m and the successful recovery of data from 16 tags(plus one recovered fish) has allowed the examination of both hori-zontal movement and behavioural patterns of toothfish.

Toothfish survived the tagging procedure well, (the main disadvan-tage was the risk of whale predation on release) and Agnew et al.(2006) and Williams et al. (2002) also reported high levels of post-tagging survivorship of toothfish. Eight tags did not transmit at allwhich is most likely due to sperm whale predation or tag failure andthree tags popped-up the same day as deployment probably due tonot being tethered properly in the fish. Hays et al. (2007) identified an-tenna breakage, animal mortality and premature detachment as someof the prime reasons why Argos satellite tags stop transmitting. Theone tagged fish recaptured by the fishing vessel possibly lost its satellitetag during the hauling process. One notable post-tagging effect (ob-served in six fish) appeared to be that the fish initially descended to agreater depth, moving slightly shallower 1–10 days later. Tagging stud-ies of cod (Gadus morhua) using data storage tags also showed the fishto often exhibit unusual behaviour for several days (no longer than14 days) after tagging, with fish ascending or descending abnormally(Godo and Michalsen, 2000; Neat et al., 2006).

Although it is impossible to sex a toothfish from external morpholo-gy female fish are generally larger thanmales. 82.8% of fish over 127 cmare females (Brown unpublished data) so there is a higher probabilitythat most of the tagged fish were females. The single 150 cm taggedfish which was recaptured however was a male (maturity stage 3)weighing 42 kg.

4.1. Seasonal behaviour

Single large depth movements from one base depth to another arelikely to be due to the fish following the seabed topography. Three fishin the south moved into deeper water during December, these werethree of the four larger fish (the fourth was not tagged over December/January) which made smaller foraging movements than the fish sized130–149 cm and it is possible that this movement into deeper waterwas as a result of following their prey or switching their prey type during

A

- 54ºS

| 56̊ W

B

Tag 77213

Tag 77210

Tag 86846

Tag 86850Tag

96261

| 58̊ W

Tag 86855

Tag 86853

Tag 86851

Tag 86852

Tag 77215

- 50˚S

C

| 56°W

54˚S-Tag 86847

Tag 77209

Tag 86849

Tag 86848

Fig. 2.Mapof theMK10 satellite tagging locations ofDissostichus eleginoides around the Falkland Islands. Black circles showdeployment positions and grey circles depict pop-up locations.Dotted lines show drift on surface to first location position.

69J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

900

1000

1100

1200

1300

1400

1500

1600

1700

1800

15/0

9/07

20/0

9/07

25/0

9/07

30/0

9/07

05/1

0/07

10/1

0/07

15/1

0/07

20/1

0/07

25/1

0/07

30/1

0/07

04/1

1/07

09/1

1/07

14/1

1/07

19/1

1/07

24/1

1/07

29/1

1/07

04/1

2/07

09/1

2/07

14/1

2/07

19/1

2/07

24/1

2/07

29/1

2/07

03/0

1/08

08/0

1/08

13/0

1/08

18/0

1/08

23/0

1/08

28/0

1/08

02/0

2/08

Dep

th (

m)

Date

Feeding behaviour

Movementinto deeper water

Fig. 3. Depth movements showing different behaviours of one Dissostichus eleginoides (Tag 77209) on Burdwood Bank.

70 J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

the Austral summer. This assertion is supported by seasonal variations inthe diet of toothfish sized 57–161 cm, in waters deeper than 500 m, offthe coast of Chile whichwere reported by Murillo et al. (2008) and theyfound these also variedwith geographical range. They found toothfish tohavemore ophidiids present in the diet in spring/summer than autumn/winter and a greater number andmore species of cephalopod present inthe diet in autumn/winter. Murillo et al. (2008) described toothfish as ahigh level predator that is capable of moving up into the water column,with aminimumexpenditure of energy, to feed on organisms that live inthis environment and showing both seasonal and geographical varia-tions in diet.

A

B

Fig. 4. Daily depth movements during periods of relative quiescence

Toothfish feeding movements linked to lunar phase or tidal statewere inconsistent and only found in very few fish. From archival dataWilliams and Lamb (2002) found a weak correlation between moonphase and periods of activity, however they concluded behaviour wasmore complex and was driven by a combination of factors includingtime of day and lunar phase, behaviour of prey species and bottom to-pography. Williams and Lamb (2002) carried out their study inshallower water (around 500 m) whereas the current study was onfish in much deeper water (1000–1800 m) and at these greater depthsthere would be a total lack of light and hence lunar light related behav-iour is unlikely to occur. Bottom topography is likely to have a larger

for Dissostichus eleginoides with A) Tag 86846 and B) Tag 86848.

Table 2Lunar and tidal related behaviour from data from satellite tags deployed on Dissostichus eleginoides around the Falkland Islands.

Tag number Significant movement ANOVA

77215 •more upwards movements during a full moon compared to a new moon Pb0.05, F=26.9•more downward movements during a new moon compared to a full moon Pb0.05, F=26.4

77209 •more downward movements than upward movements during a new moon Pb0.05, F=16•more downward movements during spring tides Pb0.05, F=14.5

86851 •more upward movements than downward movements during a full moon Pb0.05, F=43.2•more upward movements during spring tides Pb0.05, F=26.7

86848 •more upwards movements during a new moon and more downward movements during a full moon Pb0.05, F=2586853 •more upward movements than downward movements during both full and new moon Pb0.05, F=43.2

•more upward than downward movements for spring tides Pb0.05, F=13.9•more upward than downward movements for neap tides Pb0.05, F=50.6

96261 •more upward movements during spring tides Pb0.05, F=29.986852 •more upward movements during neap tides Pb0.05, F=115.1

71J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

impact on whether there are more upwards or downward movementsthan tidal influence, which will be reduced at depth (Glorioso, 2000),e.g. the fish with Tag 86853 made more upward movements duringboth spring and neap tides — this fish was in the north of the Falklandswhere bottom topography is gently sloping and hence less likely for thefish to make downward movements.

From the depth data, it appears that the daily movements are rela-tively rapid over a short period of time and are movements up intothe water column rather than remaining on the seabed and movingup or down slope. It is likely that a majority of these daily movementsare the fish swimming off bottom in search of prey. The depth changes,which occur from when the fish is at one base depth to another, aremost likely to occur as the fish follows the bathymetry, these are gener-ally slower movements and the pelagic daily movements are still seenoccurring simultaneously. At the start and end positions, the tag depthsmatched the bathymetric depths from oceanographic data and there-fore it is possible to map the route the toothfish has potentially takenduring deployment. In the north of the zone the fish are on a gentleslope and the fish mainly made upward daily movements, whereasfish around the Burdwood Bank, where the slope is much steeper, al-though they mainly made upward daily movements, they also madegreater downward movements. Toothfish, like all notothenioids areneutrally buoyant (Eastman and Devries, 1981) and this allows themto make upward or downward movements through the water columnwith ease and to feed both benthically and pelagically. Seitz et al.(2005) observed large depths changes in archival tagged halibut overshort time periods and concluded that these were vertical foragingmovements rather than benthic travel; this is also consistent with pe-lagic prey occurring in the halibut diet.

4.2. Foraging behaviour

Examination of the depth data allowed us to infer different types ofbehaviour. Sub-daily small movements of toothfish are likely to be

Fig. 5. Average difference in depth over 6 h periods during periods of regular movementsfor Dissostichus eleginoides tagged on the Burdwood Bank.

foraging behaviour and as these movements are rapid (occur within a6 h period and return to a similar depth) it is likely that these move-ments are off the bottom into the water column rather than remainingon the seabed but moving up or down the slope. This type of foragingmovement is corroborated by diet studies and Arkhipkin et al. (2003)examined prey types and identified the feeding areas of Patagoniantoothfish as on the shelf and upper slope of the Falkland Islands to bein the water column near the bottom. Toothfish show a shift in dietafter they have migrated into deeper water switching from active pred-ators on the shelf to scavengers and more opportunistic predators withdepth (Arkhipkin et al., 2003; Pilling et al., 2001). There are periods of nodepth change which are likely to be due to the fish resting after taking alarge prey item (rarely longer than 4 days). For example in cod fed ex-perimentally on sprats (Sprattus sprattus), complete digestion couldtake up to 3 days (Daan, 1973) and in cod fed experimentally on herring(Clupea harengus) there were still fish remains in the cod stomach after4 days (Salvanes et al., 1995). In several studies (e.g. cod or perch (Percafluviatilis)) higher food rations were found to take exponentially longerto digest than smaller rations due to a lag in the first part of digestion(Persson, 1980; Salvanes et al., 1995). Garcia de la Rosa (1997) identi-fied a difference in diet between two groups of adult toothfish aroundSouth Georgia. He found that fish 130–149 cm fed mainly on squidand Natantia shrimp whereas toothfish 150–200 cm fed on more ben-thic species including fish and lithodid crabs and this difference in dietcould explain these differences in movements which are evident inthe tagged fish. Ontogenetic changes in diet help to reduce competitionbetween conspecifics and this shift in diet could be due to the fact thatlarger fish can tackle larger, harder to catch prey as they have improvedlocomotory ability and have biggermouths. Predators generally take thelargest prey items available that they can manage with larger individ-uals consuming larger prey (Kock, 1992).

Williams and Lamb (2002) recorded more regular daily feedingmovements in some of their tagged toothfish compared to this study.They tagged smaller fish (71.7–81.4 cm — at this size these fish are ator just below size at maturity Everson and Murray, 1999; Laptikhovskyet al., 2006) and at shallower depths (400–780 m). Larger fish willhave a larger ration size, however the range of prey size also increases,with larger fish taking both small and large prey items (Collins et al.,2007) and therefore their periods of resting between feeding will bemore variable than smaller fish which take smaller similar sized preymore regularly. As fish get older and larger growth rate slows (Postand Lee, 1996) therefore the smaller young fish are growing faster andhave higher mass specific metabolic requirements. Garcia de la Rosa(1997) examined the feeding ecology of toothfish around South Georgiaand the Argentinean Shelf and reported that larger fish had a higher pro-portion of full stomachs than smaller fish (up to 100% in fish 70–95 cmcompared to 52.4% infish 30–39 cm). This is the opposite towhatwouldbe expected however they did not have any fish less than 30 cmand thesample sizeswere small (e.g. n=12 for 70–95 cmfish)whichwould in-fluence the results. Tomeet these higher energetic requirements smallerfish will require food more regularly and hence the more regular

800

900

1000

1100

1200

1300

1400

13/0

3/08

23/0

3/08

02/0

4/08

12/0

4/08

22/0

4/08

02/0

5/08

12/0

5/08

22/0

5/08

01/0

6/08

11/0

6/08

21/0

6/08

01/0

7/08

11/0

7/08

21/0

7/08

31/0

7/08

10/0

8/08

20/0

8/08

30/0

8/08

09/0

9/08

19/0

9/08

Dep

th (

m)

Date

900

1000

1100

1200

1300

1400

1500

1600

1700

1800

15/0

9/07

25/0

9/07

05/1

0/07

15/1

0/07

25/1

0/07

04/1

1/07

14/1

1/07

24/1

1/07

04/1

2/07

14/1

2/07

24/1

2/07

03/0

1/08

13/0

1/08

23/0

1/08

02/0

2/08

12/0

2/08

22/0

2/08

03/0

3/08

13/0

3/08

23/0

3/08

02/0

4/08

Dep

th (

m)

Date

900

950

1000

1050

1100

1150

1200

07/0

5/08

09/0

5/08

11/0

5/08

13/0

5/08

15/0

5/08

17/0

5/08

19/0

5/08

21/0

5/08

23/0

5/08

25/0

5/08

27/0

5/08

29/0

5/08

31/0

5/08

02/0

6/08

04/0

6/08

06/0

6/08

Dep

th (

m)

Date

1100

1150

1200

1250

1300

1350

1400

1450

1500

07/0

2/08

09/0

2/08

11/0

2/08

13/0

2/08

15/0

2/08

17/0

2/08

19/0

2/08

21/0

2/08

23/0

2/08

25/0

2/08

27/0

2/08

29/0

2/08

02/0

3/08

04/0

3/08

06/0

3/08

08/0

3/08

10/0

3/08

12/0

3/08

14/0

3/08

16/0

3/08

18/0

3/08

Dep

th (

m)

Date

BA

Fig. 6. Observations of spawning behaviour of Dissostichus eleginoides tagged on Burdwood Bank. A) Tag 77213; B) Tag 77210.

72 J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

foraging movements. It is possible that larger fish are taking a variety ofprey sizes and so have an irregular pattern of foraging movements anddue to taking larger prey items have longer digesting periods betweenfeedings.

4.3. Spawning behaviour

The vertical movements by four tagged fish into shallower waters ofdepths of 900–1200 m during March and May–August coincides withpreviously recorded spawning months (small spawning peak inMarch/April and main spawning event in July/August; Laptikhovsky etal., 2006) and with the predicted spawning depths of 800–1000 m.These movements were only recorded in fish deployed on theBurdwood Bank (where spawning fish have been recorded by ob-servers; Laptikhovsky et al., 2006), the five fish from the north did notshow these vertical movements over the spawning months. Agnew etal. (1999) observed no pre-spawning migrations of toothfish aroundSouth Georgia to Shag rocks, instead they found Patagonian toothfishmoved upslope (females) and down slope (males) to spawn at around800–1200 m. Seitz et al. (2005) used electronic tags to successfullyidentify spawning behaviour in Pacific halibut (Hippoglossus stenolepis)with changes in depth being assumed to be the spawning rise. Loherand Seitz (2008) observed these spawning rises in 63% of tagged Pacifichalibutwithfish ascending 100–200 m in a short time period. They alsosuggested that the vertical rise for spawning is to ensure transport ofeggs by currents to suitable juvenile nursery grounds. Live toothfishkept for aquaculture were observed making vertical movements intothe water column prior to the spawning season (Paul Howes perscomm.) Relatively shallower waters will be slightly warmer for theeggs (in August temperatures at 1000 m are approximately 3.0–3.2 °Ccompared to 2.6–2.8 °C at 1450 m). This behaviour could also be advan-tageous to the fish to ensure good dispersion of the pelagic eggs into thewater column where they may take advantage of currents carryingthem to the productive areas of the Falklands Shelf.

4.4. Site fidelity

Strong site fidelity was evident in 79% of the tags recovered, withthese fish remaining within 50 km from their deployment position.The ability of a fish to undertake long-distance migration is deter-mined by its body shape and other physiological adaptations, in par-ticular its muscular makeup (Kock, 1992). Myotomal white musclesare designed for short bursts of high poweredmotion for active preda-tion or as an escape response from predators (Kock, 1992). Red mus-cle, which generally powers the pectoral fins in adult notothenids isused for sustained swimming. Although D. mawsoni is seen as one ofthe more active notothenids due to its high P50 value (i.e. higheroxygen affinity of haemoglobin (Kock, 1992)), both D. mawsoni andD. eleginoides are comprised of a large percent of white muscle (51%of the body weight in D. mawsoni (Eastman and DeVries, 1981)) andso much of their movement will be dominated by small periods ofrapid movements. Their reduced amount of red muscle for sustainedlow speed swimming may explain the lack of large scale migrationin this species and why toothfish show strong site fidelity. The lowsea temperatures around the Falkland Islands and also the shorttime period of this study may also be reasons for not detecting largerhorizontal movements.

The individual fish whichmoved 126.8 km in the north of Falklandswaters, moved north-westwards and not southwards towards thespawning area. Of the fish which had moved greater distances in thesouth, for two (which had moved 129 km and 100 km) their tags haddrifted for 7 days on the surface prior to giving a first location positionso it is more likely that these fish had actually only moved about50 km and had headed in an easterly direction to the eastern edge ofthe Burdwood Bank. Delay in transmission was caused by the depthsensor being under a large amount of pressure for a long time periodwhich caused the depth sensor to drift resulting in the surface depthreading being greater than 0 m (Steve Lambert, Product Specialist,Wildlife Computers pers. comm.). The tag recalibrated itself (zerodepth correction feature) and then began to transmit, a process which

73J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

took 7–11 days and caused the delayed transmission time. The two fishwhich had moved greater distances (281.9 km and 417.2 km) out tothe Scotia Ridge also had tags which had drifted on the surface for11 days and an unknown number of days respectively prior to givinga first location position. Therefore, these fish were likely to havemoved shorter distances than reported, however due to surface driftpatterns they must have moved at least to the edge of the ScotiaRidge (minimum 190 km from deployment).

In general, species can be classified along a spectrum from thosewhich show a high level of site fidelity to those which migrate predict-ably to spawning or feeding grounds (Quinn and Brodeur, 1991). The re-sults of this study match those of Marlow et al. (2002) around SouthGeorgia and Williams and Lamb (2002) around Heard Island in thatthemajority of fish showed very little or nomigration, butwith some in-dividuals in the population appearing to make much larger migrations.Possibly this is a developed trait for gene dispersal and broadening thespecies range and perhaps migrations of many toothfish only occurover smaller distances when environmental parameters are suitable.Maybe the main migrations of toothfish occur as juveniles for the sepa-ration of life history stages with juveniles migrating into deeper watersas adults. Dunn et al. (2007) found for tagged D. mawsoni the greatestdistances moved between release and recapture were for juvenile andsub-adult fish (b100 cm total length). Studies on migration routes ofanother deep sea benthopelagic species, Sablefish (Anoplopoma fimbria),found although it generally moves less than 50 km some individualsmoved as far as 4400 km from the Bering Sea to San Francisco duringa six year period (Sasaki, 1985). In a large number of species (e.g. salmonsharks Lamna ditropis; Hulbert et al., 2005) there is a split in themethods of dispersion within a population with themajority of animalsremaining within their resident territory and not moving too far butwith a few individuals making large dispersing migrations. This couldbe a valuable trait to extend the species range, to reduce inbreedingand spread the genes, to reduce competition for mates or resources orto help reinvade areas which have been disturbed (Howard, 1960).

The data from this study indicated there are no regular large scalemigrations of toothfish from the north of Falkland's waters to theBurdwood Bank spawning areas or vice versa which is contrary toLaptikhovsky et al. (2006) proposition of migration of toothfish aroundthe Falkland's Shelf. This apparent lack of spawningmigrations from in-dividuals in the north could be due to the fact toothfish are long livedanimals and may not need to spawn every year (Laptikhovsky andBrickle, 2005). It is possible that individuals away from the BurdwoodBank may migrate to spawn only a handful of times over their lifespan and hence not within the period of this study. Although maturingfish have been found in the north of the zone no spawning fish haveever been recorded in this area. Histological analysis has found toothfishundergoing skipped spawningwith all thematuring oocytes in a state ofreabsorption (Brown, 2011). Peaks in recruitment have also been iden-tified occurring approximately every 4 years (Laptikhovsky and Brickle,2005), indicting spawning may not occur in all mature fish every yearand Everson and Murray (1999) also reported in one year that 25–43% of toothfish did not come into spawning condition. Laptikhovsky(2011) reported for another deepwater species, Macrourus carinatus,that the juveniles migrate northwards with the Falklands Current butthen as adults they return to spawning sites on the Burdwood Bankand then remain there. This could also be the case for the Patagoniantoothfish.

With all studies using technologies at the edge of their testedrange, we must be aware of the limitations. The MK10 tags are onlycalibrated for depth readings to 1000 m, however, as the calibrationis a linear relationship readings over 1000 mwill still be relatively ac-curate (Heather Baer, Product specialist, Wildlife Computers percomm.). The increased time the tag was at depth also caused a delayin retrieval of accurate pop-up positions for three of the tags meaningthey had drifted on the surface for several days. This study has shownit is possible to retrieve data from fish that have been brought up from

depths of up to 1459 m and then tagged and released. As technologiesadvance with greater resolution and accuracy of data, the use of satel-lite tags for data acquisition from fish at depths may prove invaluablefor gaining a deeper understanding of their behaviours and in turntheir life histories.

5. Conclusions

As far as we are aware, this study is the first of its kind using satel-lite pop-up tags to study fishwhich spend prolonged periods at depthsof >1000 m. This is also the first time that Patagonian toothfish havebeen satellite tagged at these depths giving new movement data andan insight into their adult behaviours. Results from this study showhow data from a few individuals can expose behaviour patterns forthe species with foraging and spawning behaviours identified. Forag-ing behaviour highlighted the fact that toothfish make vertical move-ments into the water column to feed and showed differences in dietbetween fish 130–148 cm and fish >149 cm. The foraging behaviourvaried both between and within individual fish. Archival tagging hasallowed the identification of season and depths of spawning withspawning behaviour only recorded on the Burdwood Bank occurringin depths of 900–1200 m during March and May–August. Evidenceof no spawning behaviour in the north coupled with lack of regularmigration has strong implications for fisheries management in termsof discrete manageable units on this part of the Patagonian Shelf.

Acknowledgements

We gratefully acknowledge funding of this work by ConsolidatedFisheries Limited and the invaluable assistance of the Captain andcrew of the CFL Gambler without them this work would not have beenpossible. Thanks to Luke Kenny, Gemma French andSarahHearne for as-sistancewith the tagging procedure and to John Barton, Director of Fish-eries, Falkland Islands Government Fisheries Department for supportingthis work. Valuable comments from Jonathan Houghton and two anon-ymous reviewers have helped greatly improve the manuscript. [SS]

References

Agnew, D.J., Heaps, L., Jones, C., Watson, A., Berkieta, K., Pearce, J., 1999. Depth distributionand spawning pattern ofDissostichus eleginoides at South Georgia. CCAMLR Sci. 6, 19–36.

Agnew, D.J., Clark, J.M., McCarthy, P.A., Unwin, M.J., Ward, M., Jones, L.A., 2006. A study ofPatagonian toothfish (Dissostichus eleginoides) post-tagging survivorship in subarea48.3. CCAMLR Sci. 13, 279–289.

Appleyard, S.A., Ward, R.D., Williams, R., 2002. Population structure of the Patagoniantoothfish around Heard, McDonald and Macquarie Islands. Antarct. Sci. 14, 364–373.

Arkhipkin, A., Brickle, P., Laptikhovsky, V., 2003. Variation in the diet of the Patagoniantoothfish with size, depth and season around the Falkland Islands. J. Fish Biol. 63,428–441.

Brown, J., 2011. Ecology and life history of a deepwater notothenid,Dissostichus eleginoidesSmitt 1898, around the Falkland Islands, SW Atlantic Ocean. University of AberdeenPhD Thesis.

Collins, M.A., Brickle, P., Brown, J., Belchier, M., 2010. The Patagonian toothfish: biology,ecology and fishery. Adv. Mar. Biol. 58, 227–300.

Collins, M.A., Ross, K.A., Belchier, M., Reid, K., 2007. Distribution and diet of juvenile Pat-agonian toothfish on the South Georgia and Shag Rock shelves (Southern Ocean).Mar. Biol. 152, 135–147.

Crossin, G.T., Hinch, S.G., Farrell, A.P., Higgs, D.A., Lotto, A.G., Oakes, J.D., Healey, M.C.,2004. Energetics and morphology of sockeye salmon: effects of upriver migratorydistance and elevation. J. Fish Biol. 65, 788–810.

Daan, N., 1973. A quantitative analysis of the food intake of North Sea cod, Gadus morhua.Neth. J. Sea Res. 6, 479–517.

DeWitt, H.H., Heemstra, P.C., Gon, O., 1990. Nototheniidae. Fishes of the Southern Ocean.JLB Smith Institute of Ichthyology, Grahamstown, South Africa, pp. 279–331.

Dunn, A., Hanchet, S.M., Ballara, S.L., 2007. An updated descriptive analysis of thetoothfish (Dissostichus spp.) tagging programme in subareas 88.1 and 88.2 for2006–07, pp. 1–21.

Eastman, J.T., Devries, A.L., 1981. Buoyancy adaptations in a swim-bladderless Antarcticfish. J. Morphol. 167, 91–102.

Everson, I., Murray, A., 1999. Size at sexual maturity of Patagonian toothfish (Dissostichuseleginoides). CCAMLR Sci. 6, 37–46.

Garcia de la Rosa, S.B., 1997. Comparative feeding ecology of Patagonian toothfish(Dissostichus eleginoides) in the southwestern Atlantic. CCAMLR Sci. 4, 105–124.

Glorioso, P.D., 2000. Patagonian Shelf 3D tide and surge model. J. Mar. Syst. 24, 141–151.

74 J. Brown et al. / Journal of Experimental Marine Biology and Ecology 443 (2013) 65–74

Glorioso, P.D., Piola, A.R., Leben, R.R., 2005. Mesoscale eddies in the Subantarctic Front —southwest Atlantic. Sci. Mar. 69, 7–15.

Godo, O.R., Michalsen, K., 2000. Migratory behaviour of north-east Arctic cod, studied byuse of data storage tags. Fish. Res. 48, 127–140.

Harden Jones, F.R., 1968. Fish Migration. Edward Arnold Press, London.Hays, G.C., Bradshaw, C.J.A., James, M.C., Lovell, P., Sims, D.W., 2007. Why do Argos sat-

ellite tags deployed on marine animals stop transmitting? J. Exp. Mar. Biol. Ecol.349, 52–60.

Howard, W.E., 1960. Innate and environmental dispersal of individual vertebrates. Amer.Midl. Natur. 63, 152–161.

Hulbert, L., Aires-Da-Silva, A., Gallucci, V., Rice, J., 2005. Seasonal foragingmovements andmigratory patterns of female Lamna ditropis tagged in PrinceWilliam Sounds, Alaska.J. Fish Biol. 67, 490–509.

Kock, K.H., 1992. Antarctic Fish and Fisheries. Cambridge University Press.Laptikhovsky, V., 2011. Migrations and structure of the species range in ridge-scaled rattail

Macrourus carinatus (southwest Atlantic) and their application to fisheries manage-ment. ICES J. Mar. Sci. 68, 309–318.

Laptikhovsky, V., Brickle, P., 2005. The Patagonian toothfish fishery in Falkland Islands'waters. Fish. Res. 74, 11–23.

Laptikhovsky, V., Arkhipkin, A., Brickle, P., 2006. Distribution and reproduction of the Pat-agonian toothfish Dissostichus eleginoides Smitt around the Falkland Islands. J. FishBiol. 68, 849–861.

Loher, T., Seitz, A., 2008. Characterisation of active spawning season and depth for easternPacific Halibut (Hippolossus stenolepis), and evidence of probable skipped spawning.J. Northwest Atl. Fish. Sci. 41, 23–36.

Marlow, T.R., Agnew, D.J., Everson, I., 2002. Movement and growth of tagged toothfisharound South Georgia and Shag rocks (Subarea 48.3). CCAMLR 1–13.

Murillo, C., Oyarzun, C., Fernández, I., 2008. Latitudinal and temporal variation in the dietof Dissostichus eleginoides Smitt, 1898 (Perciformes: Nototheniidae) in deep environ-ments of the south and centre coast of Chile. Gayana 72, 94–101.

Neat, F.C., Wright, P.J., Zuur, A.F., Gibb, I.M., Gibb, F.M., Tulett, D., Righton, D.A., Turner, R.J.,2006. Residency and depth movements of a coastal group of Atlantic cod (Gadusmorhua L.). Mar. Biol. 148, 643–654.

Pade, N.G., Queiroz, N., Humphries, N.E., Witt, M.J., Jones, C.S., Noble, L.R., Sims, D.W., 2009.First results from satellite-linked archival tagging of porbeagle shark, Lamna nasus:

area fidelity, wider-scale movements and plasticity in diel depth changes. J. Exp. Mar.Biol. Ecol. 370, 64–74.

Persson, L., 1980. The effects of temperature and meal size on the rate of gastric evacua-tion in perch (Perca fluviatilis) fed on fish larvae. Freshw. Biol. 11, 131–138.

Pilling, G.M., Purves, M.G., Daw, T.M., Agnew, D.A., Xavier, J.C., 2001. The stomach contents ofPatagonian toothfish around South Georgia (South Atlantic). J. Fish Biol. 59, 1370–1384.

Post, J.R., Lee, J.A., 1996. Metabolic onotogeny of teleost fishes. Can. J. Fish. Aquat. Sci.53, 910–923.

Quinn, T.P., Brodeur, R.D., 1991. Intra-specific variations in the movement patterns ofmarine animals. Am. Zool. 31, 231–241.

Rogers, A.D., Morley, S., Fitzcharles, E., Jarvis, K., Belchier, M., 2006. Genetic structure ofPatagonian toothfish (Dissostichus eleginoides) populations on the Patagonian Shelfand Atlantic and western Indian Ocean Sectors of the Southern Ocean. Mar. Biol.149, 915–924.

Salvanes, A.G.V., Aksnes, D.L., Giske, J., 1995. A surface-dependent gastric evacuationmodel for fish. J. Fish Biol. 47, 679–695.

Sasaki, T., 1985. Studies on the Sablefish Resources in the North Pacific Ocean, 22.Seitz, A., Wilson, D., Norcross, B., Neilsen, J., 2005. Pop-up Archival Transmitting (PAT)

tags: a method to investigate the migration and behaviour of Pacific halibtHippoglossus stenolepis in the Gulf of Alaska. Alsk. Fish. Res. Bull. 10, 124–136.

Shaw, P.W., Arkhipkin, A.I., Al-Khairulla, H., 2004. Genetic structuring of Patagoniantoothfish populations in the Southwest Atlantic Ocean: the effect of the AntarcticPolar Front and deep-water troughts as barriers to genetic exchange. Mol. Ecol.1–11. http://dx.doi.org/10.1111/j.1365-294X.2004.02327.x.

Smith, P., McVeagh, M., 2000. Allozyme and microsatellite DNA markers of toothfishpopulation structure in the Southern Ocean. J. Fish Biol. 57, 1–12.

Stevens, J.D., Bradford, R.W., West, G.J., 2010. Satellite tagging of blue sharks (Prionaceglauca) and other pelagic sharks off eastern Australia: depth behaviour, temperatureexperience and movements. Mar. Biol. 157, 575–591.

Williams, R., Lamb, T., 2002. Behaviour of Dissostichus eleginoides fitted with archival tagsat Heard Island: preliminary results. CCAMLR 1–16 (WG-FSA-02/60).

Williams, R., Tuck, G.N., Constable, A., Lamb, T., 2002. Movement, growth and availableabundance to the fishery of Dissostichus eleginoides Smitt, 1898 at Heard Island, de-rived from tagging experiments. CCAMLR Sci. 9, 33–48.