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Movements of the white shark Carcharodon carcharias in the … · Mar Ecol Prog Ser 580: 1–16, 2017 to predictably encounter these sharks. Indeed, much of what is known of this

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  • MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

    Vol. 580: 116, 2017https://doi.org/10.3354/meps12306

    Published September 29

    INTRODUCTION

    The white shark Carcharodon carcharias is well-documented in the western North Atlantic Oceanfrom Newfoundland to the Gulf of Mexico, includingThe Bahamas and parts of the Caribbean (Bigelow &Schroeder 1948, Templeman 1963, Compagno 1984,Casey & Pratt 1985). Yet, despite a well-establishedpresence, efforts to study its life history and ecologyhave been hampered by the inability of researchers

    The authors 2017. Open Access under Creative Commons byAttribution Licence. Use, distribution and reproduction are un -restricted. Authors and original publication must be credited.

    Publisher: Inter-Research www.int-res.com

    *Corresponding author: [email protected]

    FEATURE ARTICLE

    Movements of the white shark Carcharodoncarcharias in the North Atlantic Ocean

    G. B. Skomal1,*, C. D. Braun2,3, J. H. Chisholm1, S. R. Thorrold4

    1Massachusetts Division of Marine Fisheries, 836 South Rodney French Blvd., New Bedford, MA 02744, USA2MIT-WHOI Joint Program in Oceanography, Massachusetts Institute of Technology, Cambridge, MA 02139, USA

    3MIT-WHOI Joint Program in Oceanography, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA4Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA

    ABSTRACT: In the western North Atlantic, much ofwhat is known about the movement ecology of thewhite shark Carcharodon carcharias is based on his-torical fisheries-dependent catch records, whichportray a shelf-oriented species that moves northand south seasonally. In this study, we tagged 32white sharks (16 females, 7 males, 9 unknown),ranging from 2.4 to 5.2 m total length, with satellite-based tags to investigate broad-scale movementsin the North Atlantic. Based on 10427 days of track-ing data, we found that white sharks are morebroadly distributed, both horizontally and vertically,throughout the North Atlantic than previouslyunderstood, exhibiting an ontogenetic shift fromnear-coastal, shelf-oriented habitat to pelagic habi-tat with frequent excursions to mesopelagic depths.During the coastal phase, white sharks migratedseasonally from the northeast shelf in the summer tooverwintering habitat off the southeastern US andthe Gulf of Mexico, spending 95% of their time at

  • Mar Ecol Prog Ser 580: 116, 2017

    to predictably encounter these sharks. Indeed, muchof what is known of this species in the North Atlanticcomes from the analysis of distribution records (Tem-pleman 1963, Casey & Pratt 1985), rare behavioralobservations (Carey et al. 1982, Pratt et al. 1982), andthe opportunistic examination of dead specimens(Pratt 1996).

    The distribution of the white shark in the westernNorth Atlantic (WNA) has been reviewed by Casey& Pratt (1985) and, more recently, Curtis et al.(2014) based on fisheries interactions, confirmedsightings, and published accounts. The rarity of thisspecies in the WNA is exemplified by the observa-tion that white sharks represented only 0.04% ofthe sharks taken by over 2.1 million hooks of pelagiclongline effort from the Grand Banks to the Gulf ofMexico (19631983, Casey & Pratt 1985) and theresulting compilation of only 649 records during theperiod 18002010 (Curtis et al. 2014). Nonetheless,these authors concluded that white sharks in theWNA are most abundant in continental shelf watersand ex hibit seasonal movements, presumably medi-ated by water temperature, into northern latitudesduring the summer months (Casey & Pratt 1985,Curtis et al. 2014). However, as noted by Curtis etal. (2014), the use of fisheries-dependent data todescribe the distribution of a species can be biasedby a number of factors including the temporal andspatial distribution of fishing effort and catchability.Hence, these records and the seasonal movementsderived from them may not accurately reflect theentire distribution and movement ecology of thewhite shark in the WNA.

    In the Pacific and Indian oceans, the ecology of thewhite shark is relatively well studied because indi-viduals aggregate on a seasonal basis at large pin-niped colonies for feeding (Klimley & Ainley 1996,Domeier 2012). The high seasonal abundance ofwhite sharks near seal and sea lion colonies has alsoallowed researchers in these regions to study the hor-izontal and vertical movements of white sharks overbroad spatial and temporal scales using satellite-based tag technology. For instance, white sharkshave been shown to exhibit deep-diving behaviorassociated with coastal and ocean basin-scale move-ments (Boustany et al. 2002, Bonfil et al. 2005, Bruceet al. 2006, Weng et al. 2007a,b, Domeier & Nasby-Lucas 2008, 2013, Nasby-Lucas et al. 2009, Jor-gensen et al. 2010, Duffy et al. 2012). This divingbehavior has been linked to feeding (Domeier &Nasby-Lucas 2008, Nasby-Lucas et al. 2009) andreproduction (Jorgensen et al. 2012), but with onlylimited evidence for either hypothesis.

    The only horizontal and vertical movement obser-vations of white sharks in the North Atlantic comefrom a single acoustic tracking study conducted byCarey et al. (1982). These researchers acousticallytagged a 4.6 m total length (TL) white shark that wasscavenging a fin whale Balaenoptera physalus car-cass 39 km southwest of Montauk Point, New York,and tracked the shark for 83 h as it moved 190 kmsouthwest along the 25 fathom (46 m) bathymetriccurve. The shark remained largely associated withthe thermocline at approximately 10 to 20 m, butmade periodic excursions to the bottom. At the time,Carey et al. (1982) noted that the seals, sea lions, andelephant seals, which are common items in the diet ofwhite sharks in other regions, are not available inthe WNA. Hence, they concluded that the observeddiving behavior may be associated with searching fordead whales, which were considered an importantfood resource for large white sharks (>3 m TL) on thecontinental shelf. Indeed, the presence of scavengingwhite sharks on whale carcasses is well-documentedin this region (Pratt et al. 1982).

    While seal populations were once decimated in theWNA, the protection of marine mammals afforded bythe US Marine Mammal Protection Act has led to arebound in the Atlantic gray seal Halichoerus grypuspopulation (NMFS 2009, Wood LaFond 2009). Thereis evidence that white sharks have, in turn, expandedtheir diet in response to regional changes in sealabundance (Skomal et al. 2012). The predictableabundance of white sharks off the coast of Cape Cod,Massachusetts, provided a research opportunity tostudy the ecology and life history of this species inthe North Atlantic Ocean. The objective of the cur-rent study was to deploy satellite-based tag tech -nology on white sharks to uncover, for the first time,the broad-scale 3-dimensional movements of whitesharks in the North Atlantic, and relate them to thenatural history of this species.

    MATERIALS AND METHODS

    Tagging

    White sharks were tagged off the coasts of CapeCod, Massachusetts (n = 31) during the summers(July to October) of 2009 to 2014 and Jacksonville,Florida (n = 1) in March, 2013 (Table 1). We deployedpop-up satellite archival transmitting (PSAT) tags(models MK10-PAT [MK10, n = 7], miniPAT [mP, n =16], MK10AF [n = 7], Wildlife Computers; modelSeaTag-MOD [STM, n = 4], Desert Star Systems LLC)

    2

  • Skomal et al.: White shark movements 3

    IDT

    ag t

    ype

    PT

    TT

    ag d

    ate

    Tag

    loc

    atio

    nT

    otal

    Sex

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    ate

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    ra-

    En

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    ion

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    itat

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    )(m

    )(d

    )(

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    )(m

    )(k

    m)

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    09-0

    1M

    K10

    7824

    905

    .09.

    2009

    41.6

    069

    .98

    3.0

    U24

    .01.

    2010

    141

    30.7

    180

    .20

    8830

    34C

    oast

    alG

    PE

    3W

    S09

    -02

    MK

    1095

    970

    05.0

    9.20

    0941

    .60

    69.9

    63.

    7U

    15.0

    1.20

    1013

    230

    .37

    80.5

    651

    241

    44C

    oast

    alG

    PE

    3W

    S09

    -03

    MK

    1067

    822

    08.0

    9.20

    0941

    .59

    69.9

    82.

    4U

    01.0

    3.20

    1017

    429

    .02

    80.5

    727

    240

    90C

    oast

    alG

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    3W

    S09

    -04

    MK

    1086

    228

    08.0

    9.20

    0941

    .62

    69.9

    63.

    8U

    13.0

    4.20

    1021

    736

    .06

    73.7

    396

    3872

    Coa

    stal

    GP

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    09-0

    5M

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    7824

    808

    .09.

    2009

    41.5

    969

    .99

    3.7

    U05

    .11.

    2009

    5841

    .11

    70.0

    148

    1710

    Coa

    stal

    GP

    E3

    WS

    10-0

    1m

    P95

    985

    27.0

    7.20

    1041

    .65

    69.9

    53.

    6F

    01.0

    2.20

    1118

    930

    .50

    80.9

    770

    060

    72C

    oast

    alG

    PE

    3W

    S10

    -02

    mP

    9598

    931

    .07.

    2010

    41.6

    369

    .95

    2.8

    U15

    .08.

    2010

    1541

    .46

    70.0

    848

    400

    Coa

    stal

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    10-0

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    K10

    AF

    6428

    221

    .08.

    2010

    41.6

    669

    .93

    3.7

    U13

    .10.

    2010

    5335

    .15

    75.6

    740

    018

    83C

    oast

    alG

    PE

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    S10

    -05a

    MK

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    318

    27.0

    8.20

    1041

    .63

    69.6

    15.

    3F

    05.0

    4.20

    1122

    131

    .15

    78.4

    083

    263

    13P

    elag

    icG

    PE

    3W

    S10

    -05b

    mP

    1104

    9413

    .09.

    2012

    41.6

    769

    .93

    5.3

    F30

    .09.

    2012

    1741

    .24

    68.1

    117

    680

    5N

    AG

    PE

    3W

    S10

    -06

    MK

    10A

    F64

    280

    01.0

    9.20

    1041

    .59

    69.9

    83.

    4U

    01.0

    1.20

    1112

    224

    .60

    86.0

    076

    054

    87C

    oast

    alG

    PE

    3W

    S12

    -01a

    MK

    1067

    833

    14.0

    8.20

    1241

    .60

    69.9

    93.

    7M

    10.0

    7.20

    1333

    040

    .28

    62.4

    288

    019

    97P

    elag

    icG

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    S12

    -01b

    mP

    1213

    2631

    .07.

    2014

    41.7

    369

    .92

    3.8

    MD

    NR

    NA

    NA

    NA

    NA

    NA

    NA

    NA

    WS

    12-0

    9M

    K10

    6781

    814

    .08.

    2012

    41.7

    469

    .92

    4.3

    UD

    NR

    NA

    NA

    NA

    NA

    NA

    NA

    NA

    WS

    12-1

    1m

    P11

    0495

    27.0

    8.20

    1241

    .58

    69.9

    94.

    3F

    27.0

    8.20

    120

    41.5

    869

    .99

    ND

    ND

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    NA

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    12-1

    3m

    P11

    0489

    30.0

    8.20

    1241

    .81

    69.9

    44.

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    7.20

    1330

    535

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    74.7

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    69.8

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    733

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    41.6

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    1567

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    .23

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    03.0

    3.20

    1330

    .39

    81.3

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    31.0

    8.20

    1318

    130

    .67

    79.9

    710

    8010

    735

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    NA

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    13-0

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    03.0

    3.20

    1330

    .39

    81.3

    84.

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    1.20

    1714

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    .86

    60.4

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    155

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    1104

    9215

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    41.6

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    259

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    197

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    1174

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    179

    .54

    NA

    3915

    5P

    elag

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    13-0

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    41.6

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    241

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    1128

    8400

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    41.5

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    269

    38.5

    274

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    1418

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    .09.

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    41.6

    969

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    3.7

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    NA

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    NA

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    14-1

    7m

    P95

    974

    04.0

    9.20

    1441

    .64

    69.9

    43.

    7M

    14.0

    4.20

    1522

    232

    .08

    79.0

    188

    896

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    oast

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    MK

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    26.0

    8.20

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    15.0

    3.20

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    129

    .45

    80.7

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    272

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    1009

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    41.6

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    201

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    41.7

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    541

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    41.6

    369

    .96

    3.7

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    1141

    .82

    70.0

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    9.20

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    .61

    69.6

    33.

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    ND

    ND

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    1067

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    41.6

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    2741

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    3741

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    235

    38.1

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  • Mar Ecol Prog Ser 580: 116, 2017

    on free-swimming white sharks using a modified har-poon technique with the assistance of a spotter plane(Chaprales et al. 1998). Tags were tethered withstainless steel wire to an intramuscular T-bar stylespear tip. Each tag was programmed to record depth(MK10, MK10AF: range = 01000 m, resolution =0.5 m 1.0%; mP: 01700 m, 0.5 m 1.0%), watertemperature (40 to +60C; 0.05 0.1C), and lightlevel (470 nm, logarithmic range = 5 1012W cm2 to5 102 W cm2) every 10 (MK10, MK10AF) or 15(mP) seconds. Archived depth and temperature datawere compiled and aggregated into 14 (MK10,MK10AF) or 12 (mP) bins every 12 (MK10, MK10AF)or 24 (mP) h. In addition, depthtemperature pro-files were compiled over a 12 (MK10, MK10AF) or24 (mP) h period, and light levels were concurrentlyrecorded with depth to incorporate attenuation inpost-processing. The PSAT tags were programmed todetach after periods of 122 to 308 d and transmit pre-processed data through the Argos satellite system.All shark TLs were estimated from aerial photosusing the vessel pulpit length (320 cm) for scale.Given the vertical distance from the pulpit to theshark of ~120 to 180 cm (depending on shark depth),shark size was likely underestimated and was sub -sequently considered a minimum estimate. Maturityclasses (juvenile [

  • Skomal et al.: White shark movements

    RESULTS

    Of the 37 tags deployed on 32 indi -vidual white sharks, we received datafrom 27 (84%) PSAT tags and all 5 SPOTtags showing the movements of 29 indi-viduals (Table 1). These results includeddata from a shark (WS10-05) taggedtwice with a PSAT tag (August, 2010and September, 2012) and 2 sharks(WS13-01, WS13-02) double-taggedwith both a PSAT tag and a SPOT tag.Estimated sizes of tagged sharks rangedfrom 2.4 to 5.3 m TL (mean SD, 4.0 0.65 m). We tagged 16 females (9 sub -adults, 7 adults, 4.4 0.53 m) and 7males (1 subadult, 6 adults, 3.8 0.19 m),with a resulting sex ratio (M:F) of 0.44(Fig. 1). We were unable to determinesex of the re maining 9 individuals(3 juveniles, 6 subadults/ adults).

    Deployment durations of the PSAT tags (n = 24)ranged from 0 to 330 d (mean = 151 d) and totaled4096 tracking days during which individualsmoved up to 12440 km (mean = 4973 km; range12212440 km) and dove to a maximum depth of1128 m (Table 1). SPOT tags (n = 5) spanned a totalof 6331 tracking days (with some temporal gapsbetween transmissions) with individual movementsas far as 56155 km in 3.8 yr (WS13-01) (mean =35865 km; range 1096856155 km). Movements de -rived from SPOT tags also provided accurate positioninformation for 2 individuals (WS13-01, WS13-02)also tagged with PSAT tags.

    The tracks indicated contrasting movement pat-terns among individuals that may reflect ontogeneticchanges in habitat use. Smaller individuals (3 m) more often exhibitedwide-ranging movements through offshore, pelagichabitats (Figs. 2 & 4). Based on previously publishedestimates of size at maturity (Francis 1996, Pratt 1996,Castro 2011) and life history stages as defined byBruce & Bradford (2012), the shelf- oriented sharks (n= 16) comprised juvenile (n = 3), subadult (n = 9), andadult (n = 4) sharks of both sexes, while those thatmoved into pelagic habitats (n = 10) were subadults(1 male, 2 females) and adults (1 male, 6 females) ofboth sexes (Fig. 2).

    Those individuals largely restricted to shelf habi-tats migrated seasonally between the tagging loca-tion and northern latitudes, including the Gulf ofMaine, in the summer, through the Mid-Atlantic

    Bight and past Cape Hatteras, North Carolina in thefall, to the South Atlantic Bight as far as the Gulf ofMexico during the winter and spring (Figs. 3 & 5). Ofthe 26 tagged white sharks yielding movement data,62% remained exclusively on the continental shelffor their entire tracks (up to 3 yr). The seasonal tran-sition from overwintering habitat off southeasternUSA (North Carolina, South Carolina, Georgia, andFlorida) was relatively rapid, with little time spent inbetween (Mid-Atlantic Bight) while the migrationfrom summer habitat off the northeastern US duringthe fall months was more gradual (Fig. 6).

    In contrast, individuals that moved off the conti-nental shelf into offshore habitats demonstrated amuch less defined seasonal pattern (Figs. 4 & 5),independent of year. Movements were wide-rangingover the WNA during most of the year, with theexception of the summer, during which the sharkswere shelf-oriented (Figs. 4 & 5). However, in con-

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    COASTAL PELAGIC

    Fig. 1. Total length (TL) frequency distribution of individual white sharkstagged off Massachusetts and Florida, 20092014. Dashed vertical lines

    represent estimated lengths at sexual maturity

    Fig. 2. Frequency distribution of individual white sharks by life history stage and habitat preference

  • Mar Ecol Prog Ser 580: 116, 20176

    Fig. 3. (A,E) Most probable track, (B,F) daily depth-temperature profiles, and (C,D,G,H) daily time-at-depth utilization fortagged white sharks WS13-02 (20132014) and WS14-18 (20142015) over the duration of tag deployment (C) and (G) arescaled to facilitate observation of surface occupancy in (D) and (H), respectively. Both tracks are GPE3 model-estimated tracks

    using known locations, when available (n = 12 and n = 2 for WS13-02 and WS14-18, respectively)

  • Skomal et al.: White shark movements 7

    Fig. 4. (A,E) Estimated movements, (B,F) daily depth-temperature profiles, and (C,D,G,H) daily time-at-depth utilization fortagged white sharks WS12-13 (20122013) and WS13-01 (2013) over the duration of tag deployment (C) and (G) are scaledto facilitate obser vation of surface occupancy in (D) and (H), respectively. The WS12-13 track was estimated using GPE3, and

    WS13-01 movements are Argos-based positions from a SPOT tag

  • Mar Ecol Prog Ser 580: 116, 2017

    trast to sharks that exhibited only shelf-orientedbehavior, subadult and adult sharks returning frompelagic habitat in the summer were all along thecoast from the Gulf of Mexico to New England(Fig. 5). During the fall, white sharks ranged from offthe coast of Georgia into the Sargasso Sea to as farnorth and east as Newfoundland, Canada, and theGrand Banks (Fig. 5). During the winter and springmonths, these individuals occupied a 30 latitudi -nal range (25 55N) from The Bahamas to an area930 km southeast of Greenland; sea surface temper-atures spanned 28C (230C) over this range. Longi-tudinally, these white sharks ranged from the UScoastline to the Mid-Atlantic Ridge and one of thesharks (WS13-01) moved into the eastern NorthAtlantic (30W) passing within 30 km of the island ofFlores in the Azores (Fig. 5). Three individuals, 2 con-sidered coastal (WS10-06, WS13-02) and one pe -lagic (WS13-03), also moved into the Gulf of Mexico

    during winter (WS10-06) or early spring (WS13-02,WS13-03) (Figs. 3 & 5).

    PSAT-tagged individuals (n = 24) transmitted>3000 d of dive data, with water column tempera-tures of 4 to 32C, and dives as deep as 1128 m (3 ind.> 1000 m) (Table 1). White sharks that remained onthe shelf moved throughout the entire water columnfrom the surface to the bottom, but were largely sur-face-oriented, spending, on average, 52 and 95% oftheir time in the top 10 m and

  • Skomal et al.: White shark movements

    and 79.2% (19 h) of each day at depthsof 200400 m and 400600 m, respec-tively, during their tracks (Fig. 4). Thepelagic white sharks also exhibited amuch flatter thermal distribution, spend-ing 95% of their time, on average, in thetemperature range of 11 to 27C (Fig. 8).This indicates that individuals occupieda wider range of temperatures more fre-quently as they spent more time, hori-zontally and vertically, in both warmerand colder water when away from theshelf (Fig. 8).

    DISCUSSION

    While over 300 satellite tags havebeen deployed on white sharks acrosstheir circumglobal range before thisstudy, there are currently no publishedtracking datasets in the Atlantic Ocean.In this study, we tagged juvenile, sub -adult, and adult white sharks of bothsexes at a seasonal aggregation site offthe coast of Cape Cod, Massachusetts,

    and one adult female off Jacksonville, Florida. Ashas been the case in numerous studies on whiteshark movements in the Pacific and Indian oceans(Boustany et al. 2002, Bonfil et al. 2005, Bruce et al.2006, Weng et al. 2007a,b, Jorgensen et al. 2010,2012, Nasby-Lucas et al. 2009, Domeier 2012,Bruce & Bradford 2012, Domeier & Nasby-Lucas2012, Duffy et al. 2012, Werry et al. 2012), wefound that white sharks tagged in the Atlanticexhibited coastal, shelf-oriented movements as wellas broad movements into oceanic habitat. Regard-less of size, all of our tagged white sharks spent atleast some proportion of their time on the con -tinental shelf off the US east coast, but movementsinto oceanic waters beyond the shelf edge wererestricted to the subadult and adult sharks of bothsexes (>3 m TL, Fig. 2).

    Shelf movements

    The coastal-oriented sharks exhibited pronouncedand consistent seasonal shifts in distribution, whichwere similar to previous observations derived fromfisheries-dependent historical sightings data (Casey& Pratt 1985, Curtis et al. 2014). During the summer,white sharks occupied Northeast Shelf waters be -

    9

    Time-at-depth (%)

    Dep

    th (m

    )

    Fig. 6. Boxplot showing monthly latitudinal shift by shelf-oriented (coastal)white sharks tagged in the western North Atlantic, 20092014, generated fromSPOT (n = 5) and PSAT (n = 24) tags. Sharks migrate northward rapidly duringthe late spring and southward more gradually during the autumn months.Boxes are interquartile range (IQR). Whiskers are 1.5 IQR; points beyondthe whiskers represent outliers. Horizontal line within each box represents

    median monthly latitude. Numbers at top of panel: monthly sample size

    Fig. 7. Time-at-depth (mean SE) histogram for on- and off-shelf movements of PSAT-tagged white sharks. Shark posi-tions were divided into spatial categories based on locationrelative to 200 m depth contour: Onshelf 200 m. Sharks 10-01 and 10-02 were removed from this

    dataset due to irregular summary bin spacing

  • Mar Ecol Prog Ser 580: 116, 2017

    tween Cape Hatteras and the Gulf of Maine, withmost individuals moving into the higher latitudes(Fig. 5). During the late fall, white sharks migratedsouth to the Southeast Shelf waters from North Caro -lina to Florida as far as the Gulf of Mexico. Move-ments between these 2 regions were relatively rapidfrom south to north in the late spring and early sum-mer, but more gradual in the fall as the emigrationfrom northern latitudes appeared to be staggeredamong individuals (Fig. 6). This broad-scale seasonalmigration is typical of numerous temperate marinespecies on the US east coast, and has been well-doc-umented in teleosts (Kneebone et al. 2014b), elasmo-branchs (Kohler et al. 1998, Kneebone et al. 2014a),sea turtles (Eckert et al. 2006), and cetaceans (Ken-ney & Winn 1986).

    Based on historical white shark records, Casey &Pratt (1985) and Curtis et al. (2014) suggested thatthis migration is driven by the interaction of seasonaltemperature change and prey availability. Duringthis study, we found that shelf-oriented white sharksoccupied a consistent temperature range, spending

    the bulk (85%) of their time between1323C, which is almost identical tothe preferred sea surface tempera-ture ranges of 1522C and 1423Creported by Casey & Pratt (1985) andCurtis et al. (2014), respectively.Casey & Pratt (1985) suggested thatthe north south seasonal shift in the15C isotherm approximates thenorthern latitudinal limit for whiteshark distribution on the continentalshelf and this ap peared to be the casefor our shelf-oriented sharks. In otherregions, white sharks spend mostof their time during their coastalphase in cooler water off California(1014C, Boustany et al. 2002, Wenget al. 2007a) and New Zealand(1016C, Francis et al. 2012), but ina similar temperature range at Gua -da lupe Island (1520C, Domeier &Nasby-Lucas 2008) and eastern Aus-tralia (1422C, Bruce & Bradford2012).

    On the continental shelf, whitesharks in this study traversed theentire water column, but spent almostall their time

  • Skomal et al.: White shark movements

    ulations in this region have responded to more than40 yr of protection, and have increased dramaticallyin numbers while geographically expanding andrecolonizing the Gulf of Maine (NMFS 2009, WoodLaFond 2009, Waring et al. 2016). These abundantresources on the Northeast Shelf, when coupled withwarmer water temperatures during the summer,likely draw juvenile, subadult, and adult whitesharks to this region to forage during the summermonths. Diet information for the white shark in theWNA is limited, but stomach contents (Casey & Pratt1985) and stable isotope (Estrada et al. 2006, Hamadyet al. 2014) analyses suggest that it is a generalistfeeding on a variety of fishes and cetaceans withincreasing trophic level through ontogeny (Estrada etal. 2006). Carey et al. (1982) hypothesized that deadwhales are an important source of food for whitesharks in the WNA due to the paucity of pinnipeds atthe time of their study. Indeed, the scavenging ofwhale carcasses by white sharks in this region hasbeen well-documented (Pratt et al. 1982, Casey &Pratt 1985). However, the increasing abundance ofpinnipeds, specifically gray seals, in the Gulf ofMaine has attracted the attention of white sharks,which are now augmenting their diet with this prey(Skomal et al. 2012).

    During the fall, tagged white sharks in this studymoved along the shelf to southern overwinteringhabitat south of Cape Hatteras, North Carolina. Al -though pinnipeds are largely absent from this region,productivity on the Southeast Shelf (Cape Hatteras toFlorida) peaks during the winter (Yoder et al. 1983),and this region supports diverse assemblages of trop-ical fauna as well as temperate species that over -winter in the region (Morley et al. 2017). This regionalso supports an abundant and diverse assemblage ofcetaceans (Mullin & Fulling 2003), including theNorth Atlantic right whale Eubalaena glacialis andbottlenose dolphins Tursiops truncatus truncatus.The coastal waters from northern Florida to southernNorth Carolina have been designated critical calvinghabitat for the North Atlantic right whale (Keller etal. 2012). In this region, white sharks have been doc-umented scavenging adult right whales, and there isindirect evidence that they actively prey upon new-born calves in winter (Taylor et al. 2013). The overlapof white sharks with right whales in this habitat, asderived from our tag results, sightings records (Curtiset al. 2014), and direct observations (Taylor et al.2013), suggests that right whales provide a viablefood source for white sharks during the winter. Thereis also some evidence that white sharks are exploit-ing the shallow waters adjacent to productive river

    mouths and estuaries in this region, which supportlarge numbers of bottlenose dolphins (Nekolny 2014,Waring et al. 2016). In this study, we observed 2white sharks, one of which we tagged (WS13-01), inthe winter off Jacksonville, Florida at the mouth ofthe St. Johns River, and observed 2 others at themouth of the St. Marys river off Fernandina Beach,Florida, 34 km to the north (G. B. Skomal unpubl.data). There is ample evidence that white sharksprey upon small odontocetes, including dolphins andporpoises (reviewed by Heithaus 2001), and the re -mains of a dolphin have been documented in thestomach of a white shark sampled off Florida (Adamset al. 1994).

    Pelagic movements

    While the convergence on coastal habitats duringsummer by all size classes in our study indicates thatthe WNA shelf provides important foraging habitatfor white sharks, 45% of our tagged sub-adults andadults also spent some fraction of each year inoceanic waters beyond the continental shelf. Similarbehavior has been observed in white sharks taggedin the eastern North Pacific (Weng et al. 2007a,b,Jorgen sen et al. 2010, 2012, Domeier 2012, Domeier& Nasby-Lucas 2012), off South Africa (Bonfil et al.2005), off Australia (Bruce et al. 2006, Bruce & Brad-ford 2012, Werry et al. 2012), and off New Zealand(Duffy et al. 2012, Francis et al. 2012), with smallerindividuals being largely restricted to coastal habi-tats and an ontogenetic shift toward increasing off-shore movements with size. However, both Bruce &Bradford (2012) and Duffy et al. (2012) have alsoobserved the movements of juveniles (as small as1.9 m TL) into pelagic habitat.

    While the movement of white sharks into oceanichabitat is well-documented globally, this migratorybehavior is generally more variable among studyregions than the more ubiquitous patterns of coastalresidency. For the white sharks tagged during thisstudy, the use of pelagic habitat was not spatially, nortemporally, well-defined, and there was no apparentsynchrony in their movement. With the exception ofthe summer months, during which they were on theshelf, pelagic behavior was observed throughoutthe year. In other regions, subadult and adult whitesharks have a distinct coastal phase, spending muchof the summer and fall in coastal waters off Gua -dalupe Island (Domeier & Nasby-Lucas 2008), Cali-fornia (Weng et al. 2007a, Jorgensen et al. 2010), andNew Zealand (Duffy et al. 2012), before making off-

    11

  • Mar Ecol Prog Ser 580: 116, 2017

    shore movements in the winter. These open-oceanmovements are characterized by rapid, directedmovements over deep water, and show some consis-tent migratory paths and destinations among individ-uals (Domeier & Nasby-Lucas 2008, Bonfil et al. 2010,Jorgensen et al. 2010). In contrast, white sharks inSouth Africa (Bonfil et al. 2005) and Australia (Bruceet al. 2006, Bruce & Bradford 2012) migrated be -tween temperate and tropical waters largely alongthe shelf. Occasional forays took individuals into theopen ocean, but without any generalizable patternfor the population.

    Oceanic movements demonstrated by individualsin our study were even more disparate than thosefrom South Africa and Australia (Fig. 3). In this study,white sharks moved throughout the WNA into chem-ically and biologically diverse temperate and sub-tropical habitats (McMahon et al. 2013), includingthe Gulf Stream, the Sargasso Sea, and the mid-Atlantic ridge. Individuals moved through 30 of lati-tude with sea surface temperatures ranging from 4Cat 55N in December to nearly 28C at 25N duringthe same month. Interestingly, 2 of the individualsthat made the majority of the wide-ranging oceanicmovements (WS13-01 and WS13-03) spent a consid-erable amount of time on and around the GrandBanks during fall and winter, with WS13-01 return-ing to the area 2 years in a row. It therefore appearswhite sharks are spending a significant amount oftime in oceanic waters in the WNA, as has beenhypothesized for white sharks in the Pacific.

    Although high-tech tags allow researchers to fol-low the movements of white sharks into oceanichabitat, they do not reveal what these sharks areactually doing. It is generally thought that pelagicbehavior is associated with foraging (Domeier 2012,Duffy et al. 2012), but mating has also been sug-gested (Jorgensen et al. 2010, 2012). In the easternPacific, subadult and adult white sharks move fromcoastal aggregation sites to a focal area referred to asthe Shared Offshore Foraging Area (Domeier &Nasby-Lucas 2008, 2012) or, more commonly, theWhite Shark Caf (Weng et al. 2007a, Jorgensen etal. 2010). While in this area, white sharks make con-tinuous rapid oscillatory dives presumably to feed atmesopelagic depths (Nasby-Lucas et al. 2009) or tomate (Jorgensen et al. 2012). However, during therelatively rapid migration to this area, white sharksexhibit a bimodal depth distribution, splitting theirtime between the surface and depths in excess of300 m (Weng et al. 2007a, Nasby-Lucas et al. 2009,Jorgensen et al. 2012). This bimodal depth distribu-tion was also observed in white sharks tagged off

    New Zealand and South Africa when migratingacross open ocean (Bonfil et al. 2005, Francis et al.2012). Based on PSAT data, we found that whitesharks that moved into oceanic waters of the Atlanticspent, on average, 77% of their time at the surface(200 m). It hasbeen suggested that deep-diving behavior in whitesharks is associated with prey searching and forag-ing, energy conservation, and navigation (reviewedby Francis et al. 2012). Our observation that whitesharks in the WNA moved over broad expanses ofthe open ocean and appeared to target specificdepths (Fig. 4) suggests foraging behavior. It is possi-ble that the sharks were profiling the water columnto detect cues for navigation (Carey & Scharold 1990,Klimley et al. 2002). However, considering the timespent at depth, we believe a more likely explanationis that the sharks are diving into the mesopelagiczone to forage (Howey et al. 2016). Oceanographicstudies of the region (Irigoien et al. 2014, Fennell &Rose 2015) have reported dense scattering layersthroughout the WNA that presumably indicate highabundance of mesopelagic fish, squid, or crustaceans(Fennell & Rose 2015). Pelagic movements exhibitedby sharks in this study occupied the same regions(e.g. Fig. 4) and depth levels (Fig. 7) in which recentacoustic surveys (Sargasso Sea, Irigoien et al. 2014;Grand Banks to Ireland, Fennell & Rose 2015) con-firmed significant scattering layers from 200 to 600 min the open ocean.

    It does not appear that the vertical movements ofwhite sharks in the WNA are limited significantlyby water temperature. Temperature data logged bythe PSAT tags indicated that white sharks spent95% of their time within a broad temperature rangeof 11 to 27C when in oceanic habitat with excur-sions into water as cold as 4C. Some of the lowesttemperatures encountered by sharks in this studywere by a large adult female (Fig. 4). The ability ofthis species (and other lamnid sharks) to occupycold deep water is related to its endothermic capac-ity (Carey et al. 1982, 1985). It is likely that the hori-zontal and vertical niche expansion by subadult andadult white sharks into offshore habitat that we ob -served is related to increases in thermal inertia andthermoregulatory abilities associated with ontogeny(Neill et al. 1976).

    One obvious biogeochemical difference betweenthe North Pacific and North Atlantic oceans is thepresence of cold hypoxic strata below a relativelyshallow thermocline in the former that likely restrictsthe depth distribution of pelagic animals. Low dis-solved oxygen (DO) levels (2 ml l1) below the

    12

  • Skomal et al.: White shark movements

    shallow thermocline is in stark contrast to the DOprofiles of the WNA, which decline slowly from val-ues that commonly exceed 4.0 ml l1 (Stramma et al.2008). Thus, while low DO has been hypothesized tocompress vertical habitat of other pelagic fishes(Prince & Goodyear 2006) and sharks (Abascal et al.2011), the relatively high DO levels in the WNA donot appear to constrain the depth preferences ofWNA white sharks.

    Life history in the WNA

    In the WNA, much of what is known about thenatural history of the white shark comes from the op -portunistic sampling of fisheries-dependent landings.Based on vertebral banding patterns and bombradio carbon, the species is slow-growing, lives inexcess of 70 yr (Hamady et al. 2014), and does notmature until much later (26 yr for males and 36 yr forfemales; Natanson & Skomal 2015) than originalage/ growth analyses suggested for other regions(Cailliet et al. 1985, Wintner & Cliff 1999, Tanaka etal. 2011). Size at maturity and litter size remainunknown for females in the WNA because pregnantindividuals have yet to be examined in this region.In this study, we have presumed that size at maturityin females is similar to that derived from samplescollected in the Pacific and Indian oceans (~4.5 mTL, Francis 1996). Based on clasper morphology,Pratt (1996) estimated size at maturity in males to be3.8 m TL in the WNA. Observations of matingbehavior and parturition are lacking for whitesharks, but it has been suggested, based on numer-ous capture records of young-of-the-year (~135 cmTL, Natanson & Skomal 2015) and juvenile whitesharks, that the New York Bight (off New York andNew Jersey) provides important nursery habitat dur-ing the spring and summer (Casey & Pratt 1985,Curtis et al. 2014). These re cords also suggest thatparturition occurs in the spring and summer months.Our observation that all tagged white sharks, includ-ing the return of pelagic adult females, were shelf-oriented during the summer months (Table 1, Fig. 5)suggests coastal parturition. However, we have noevidence that adult females aggregate in the NewYork Bight to give birth to their young. Althoughmore adult females need to be tagged, our findingssuggest that young-of-the-year white sharks are notborn in the New York Bight, but simply migrate intothis nursery habitat, like older juveniles (Curtis et al.2014), to take advantage of rich foraging opportuni-ties (Casey & Pratt 1985).

    The results of this study, when coupled with previ-ously reported capture records (Casey & Pratt 1985,Curtis et al. 2014), indicate that the continental shelfalong the US east coast provides important foraginghabitat for juvenile, subadult, and adult white sharks.It is also likely that adult white sharks mate oppor-tunistically while on the shelf, but mating groundshave yet to be identified. Domeier (2012) suggestedthat mating occurs at adult aggregation sites in theeastern North Pacific during the coastal phase (sum-mer and fall). While males return annually to thesesites, it has been suggested that females maintain a2-year reproductive cycle (Anderson & Pyle 2003;although see Chapple et al. 2016), during which theyremain, while pregnant, in offshore habitat over abroad geographic area before returning to coastalwaters for parturition (Domeier 2012, Domeier &Nasby- Lucas 2012). In the WNA, we found that all ofour adult white sharks were present on the shelf dur-ing the summer months. Pratt (1996) suggested thatmating occurs in the coastal waters off the north -eastern USA. The co-occurrence of adult whitesharks of both sexes in this region supports this hypo -thesis and fresh wounds possibly associated withmating have been observed on large females forag-ing at the white shark aggregation site off Cape Cod(G. B. Skomal & J. H. Chisholm unpubl. data). How-ever, the adults of both sexes overlap throughouttheir coastal range, so it is also plausible that matingis more temporally and spatially opportunistic andnot restricted to northeastern waters. Although evi-dence for sperm storage is lacking in lamnid sharks(Pratt 1993), opportunistic mating, sperm storage,and delayed fertilization would enhance reproduc-tive success in this apex predator.

    Adults of both sexes exhibited offshore movementsduring the fall, winter, and spring, but the most ex -pansive movements were made by 3 adult females(WS12-17, WS13-01, WS13-03). These extensive move -ments into oceanic waters may be associated withsexual segregation as a means for pregnant femalesto refuge from costly mating activities (Wearmouth &Sims 2008). Clearly, additional research is needed tofurther test this hypothesis. However, we must alsoacknowledge the limitations of our sample size andthe need to tag additional white sharks to furtherinvestigate these movements.

    Population dynamics and implications

    Mounting evidence for the global phylogeographyof the white shark suggests a complex population

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    structure. Phylogenetic analyses of mtDNA controlregions support 2 main lineages in (1) the Indo-Pacific and the Mediterranean, and (2) South Africaand the WNA (Pardini et al. 2001, Jorgensen et al.2010, Gubili et al. 2011). Within these groups, there issome evidence that WNA sharks are distinct fromSouth African haplotypes (OLeary et al. 2015, An -dreotti et al. 2016). Gubili et al. (2011) noted somesimilarity between western Indo-Pacific and Medi-terranean haplotypes, suggesting that the Medi terra -nean white shark population was founded by individ-uals from the Pacific during the Late Pleistocene.Clearly, white sharks are capable of migrationsacross ocean basins. Yet such movements may berare, as even low levels of connectivity across theNorth Atlantic would act to homogenize haplotypefrequencies between the WNA and Mediterraneanpopulations. Our results generally support the hypo -thesis of limited genetic connectivity between Atlan -tic populations, as even the most wide-ranging sharkin the study only traveled as far east as the Mid-Atlantic Ridge and the Azores.

    In the WNA, several studies have reported declin-ing white shark populations in the mid- to late 20th

    century from pelagic longline logbook data (Baumet al. 2003), opportunistic capture and sightings(McPherson & Myers 2009, Curtis et al. 2014), andgenetics (OLeary et al. 2015). Most recent informa-tion, however, suggests apparent increases in sight-ings (Skomal et al. 2012) and abundance (Curtis et al.2014). These increases may be at least partially at -tributed to legal protection prohibiting white sharksfrom harvest in the WNA since the late 1990s; how-ever, seascape-scale movements of large femalesdemonstrate the importance of international coordi-nation of management efforts to protect these highlymobile predators.

    Acknowledgements. We gratefully thank our fishing andtagging vessels: Captain Bill Chaprales, Nick Chaprales,and George Breen of the F/V Ezyduzit; Christopher Fischer,Captain Brett McBride, and the crew of the M/V Ocearch;and Captain John King, Pam King, Cynthia Wigren, andWayne Davis of the F/V Aleutian Dream. This research wascarried out under Exempted Fishing Permits (SHK-EFP-11-04, SHK-EFP-12-08, SHK-EFP-13-01, SHK-EFP-14-03) is -sued to the Massachusetts Division of Marine Fisheries bythe NMFS Highly Migratory Species Management Division.This research was funded by Federal Aid in Sport Fish Res-toration, the National Science Foundation (OCE-0825148),the John J. Sacco and Edith L. Sacco Charitable Foundation,the Atlantic White Shark Conservancy, the MassachusettsEnvironmental Trust, Discovery Communications, NationalGeographic, and the Woods Hole Oceanographic Institution.This is Massachusetts Division of Marine Fisheries Contri-bution No. 90.

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    Editorial responsibility: Scott Shaffer, San Jose, California, USA

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