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Title: In situ observations of a possible skate nursery off the western Antarctic Peninsula
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Authors: M.O. Amslera *, K.E. Smithb, J.B. McClintocka, H. Singhc, S. Thatjed, S.C. Vosb, C.J.
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Brothersa, A. Brownd, D. Ellisb, J. Andersone, R.B. Aronsonb
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aDepartment
of Biology, University of Alabama at Birmingham, Birmingham, AL 35294, USA
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bDepartment
of Biological Sciences, Florida Institute of Technology, 150 West University
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Boulevard, Melbourne, FL 32901, USA
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cDepartment
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Woods Hole, MA 02543, USA
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dOcean
of Applied Ocean Physics and Engineering, Woods Hole Oceanographic Institution,
and Earth Science, University of Southampton, European Way, Southampton, SO14 3ZH,
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UK
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eNature
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Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
Imagery, under contract to Department of Applied Ocean Physics and Engineering,
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Running Head: In situ observations of Antarctic skate nursery
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*Corresponding author email; phone : [email protected]; 1 205 934 1034
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Key words: Elasmobranchii; Rajidae; Antarctica; skate-egg case; oviparity
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Abstract:
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A dense aggregation of skate-egg cases was imaged during a photographic survey of the
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seafloor along the western Antarctic Peninsula in November 2013. Egg cases were noted in a
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narrow band between 394 and 443 m depth. Although some skate species in other oceans are
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known to utilize restricted areas to deposit eggs in great numbers, such nurseries have not
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been described in the Southern Ocean.
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In situ observations of a possible skate nursery off the western Antarctic Peninsula
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Running Head: In situ observations of Antarctic skate nursery
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Among the elasmobranch fishes, skates are strictly oviparous (Conrath and Musick, 2012): in all
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species, the female releases yolky eggs encased in a tough, leathery capsule. The eggs are large
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when spawned and the tough egg case provides protection during the lengthy embryonic
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developmental period, ranging from months to years depending on the species (Hoff, 2008).
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Some species aggregate to deposit eggs and densities as great as 800 000 egg cases /km2 have
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been reported for the Alaska skate Bathyraja parmifera (Bean 1881) in the Bering Sea (Hoff,
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2009). Many skate species are known to demonstrate site-fidelity, returning to the same
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depositional area or nursery on an annual basis (see Hoff, 2010).
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Nurseries are typically small in area, situated on continental slopes, and are usually discovered
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during exploratory trawling (Hitz, 1964). Known continental-slope nursery areas include the
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Bering Sea for several species of Bathyraja (Hoff, 2010) and the north Pacific for Raja binoculata
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(Girard 1855) (Hitz, 1964). In the Atlantic Ocean a nursery site was discovered by trawling off
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North Carolina, USA for Fenestraja plutonia (Garman 1881) (Quattrini et al., 2009), and
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numerous nursery sites off Portugal have been reported for seven Raja species (Serra-Pereira et
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al., 2014). Nurseries are also discovered during photographic or video surveys of the seafloor,
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especially around deep bathymetric features inaccessible to trawling. Known skate nurseries
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discovered via imagery include one at the base of a seamount in the Sea of Japan for B. smirnov
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(Soldatov and Pavlenko 1915) (Hunt et al., 2011), in a submarine canyon in the Southern
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California Bight for R. rhina (Jordan & Gilbert 1880) (Love et al., 2008), and others near cold-
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water seeps in the Mediterranean Sea for Bathyraja spp. (Treude et al., 2011).
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The distributions and reproductive habits of many Rajidae are generally understood in much of
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the world ocean, but similar details are lacking in the Southern Ocean; the continental slopes of
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Antarctica are among the most under-explored marine habitats with respect to fishes (Eastman
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et al., 2013). Currently nine skate species are recognized from Antarctica: Amblyraja georgiana
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(Norman 1938), A. taff (Merisner 1987), Bathyraja meridionalis (Stehmann 1987), B. eatonii
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(Günther 1876), B. irasa (Hureau and Ozouf-Costaz 1980), and B. murrayi (Günther 1880) are
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found in the South Atlantic and/or Indian Ocean sectors, and B. maccaini (Springer 1971), B. sp.
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(cf. eatonii) and B. sp. (dwarf) are circumpolar (Duhamel et al., 2014). The reproductive habits
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of all of these species are largely unknown.
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In November 2013 the RV Nathaniel B. Palmer conducted a photographic survey of benthic
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communities on the continental shelf and slope west of Anvers Island, Antarctica (cruise
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NBP13-10: 63.53°S, 66.05°W to 64.30°S, 67.43°W) [Fig. 1(a)]. SeaSled, a towed-camera vehicle
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(see Singh et al., 2007; Eastman et al., 2013), imaged nine benthic transects that were roughly
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isobathic, in four depth-ranges: 400‒700 m, 700‒1100 m, 1100‒1600 m, and 1600-2100 m. An
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additional ‘vertical’ transect cut across depth-contours spanning 400‒1500 m. SeaSled was
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equipped with two cameras ( 1.4-megapixel, or 1360 x 1024 pixels, and 2.0-megapixel or 1620
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x 1220 pixels) and two strobes (150 w-s), all of which fired synchronously every 6 sec to yield
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slightly overlapping, paired stereo images. An onboard acoustic-doppler current profiler (ADCP;
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1200 kHz Teledyne RD Instruments) enabled SeaSled to be maintained at an altitude of 3‒6 m
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above the sea floor. An onboard CTD (Seabird SBE-49 Fast CAT 16-Hz) provided continuous
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temperature and salinity data. Each photographic transect was conducted over a topside
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distance of approximately 9 km and imaged a corridor of the sea floor that was on average 3.3
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m wide. During an intensive, five-day survey, over 14 000 paired images were amassed,
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visualizing approximately 135 000 m2 of the seafloor. Each image was corrected for the non-
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linear attenuation of the color spectrum in sea water (Eustice et al., 2002).
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A total of 185 skate-egg cases were observed along one transect (A1) run on the continental
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shelf at 400‒445 m depth, with the greatest concentration at 394 m to 443 m [Fig. 1(b)]. Egg
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cases were first observed 3 km into the transect and were present throughout the remaining 5
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km of the dive. Overall, the imaged area had an estimated 20 000 egg cases per km2 . Water
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temperature averaged 1.27° C ± 0.009 SD and salinity was constant at 35 psu. An additional
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eight egg cases were imaged in three other transects within the study area. Three egg cases
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were noted in the vertical transect at 427, 435 and 535 m depth. The remaining five egg cases
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were imaged in two transects at 700‒1100 m and all were widely dispersed between 723 and
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937 m.
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Egg cases were noted in 93 of the 2260 paired images in the A1 transect. Of those 93 images,
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35 had multiple egg cases (maximum n=9) [see Fig. 1 (c) for representative image]. Egg-case
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color ranged from golden to dark brown, although the observed color was somewhat
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dependent on camera angle. Many of the egg cases (n=95) appeared bright gold and shiny. The
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majority (n=145) were various shades of brown, had visible longitudinal striations and lacked
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apparent evidence of fouling. Seven egg cases appeared damaged with portions frayed or
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missing.
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An average egg-case length of 14 cm was determined using Coral Point Count with Excel
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Extensions (CPCe) software (Kohler and Gill, 2006) and based on metrics defined by Ebert &
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Davis ( 2007). The length of each egg case was streamlined and lacked a prominent lateral keel.
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Anterior and posterior horns appeared to be approximately the same length and curved
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inward. Obvious attachment structures, either tendril-like fibers or tissue veils, were noted on
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the presumed posterior horns of 86 egg cases. Of the remaining egg cases, 47 lacked clear
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attachment features and 52 were not sufficiently resolved to determine attachment status.
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The egg cases appeared to be randomly strewn across the seafloor with no discernible pattern
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of orientation. In images containing multiple egg cases, 22 were in direct contact with a
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neighboring egg case. Although 60 egg cases appeared to be in direct physical contact with
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other fauna, there was no suggestion that egg-case horns were hooked to an organism. The
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majority lay flat on the seafloor, presumably on the ventral side. Egg cases observed tipped
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onto a lateral side (n=18) were against or among dropstones.
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Egg-case age, time of spawning, and even the identity of the source skate species can only be
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tentatively inferred from clues in the photographs. The range of color and apparent condition
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of the egg cases photographed correlates with a three-stage scoring system established for B.
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parmifera, in which shiny, golden egg cases are newly deposited; darker ones are previously
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deposited; and very-dark, weathered and/or fouled egg cases are either old or empty. All three
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stages can co-occur, although the latter stage was least abundant in B. parmifera nurseries
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(Hoff, 2009).
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The mean embryonic development-time for B. parmifera in the Bering Sea is the longest known
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for any oviparous elasmobranch: 1290 days at ambient 4.4° C. Another Bering Sea species, R.
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radiata, requires an average 912 days at 4.6° C for complete development (see Hoff, 2008).
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Assuming the ambient water temperature of 1.27° C remained constant year-round and a
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development rate similar to B. parmifera in the Bering Sea, even a conservative correlation
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between temperature and embryonic development would suggest that more than four years
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would be required for the most recently deposited egg cases imaged to fully develop and hatch.
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The morphology of egg cases photographed in the A1 transect appears consistent with the
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genus Bathyraja (Ishihara et al., 2012). It has been suggested that the egg-case morphology of
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Bathyraja is highly conserved within and between species of the southwestern Atlantic and
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Northern Hemisphere oceans (Mabragaña et al., 2011). Evidence presented herein suggests
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that the similarity may extend to species in the Southern Ocean. Assuming the imaged egg
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cases are those of a Bathyraja, the likely candidates, based on reported adult geographic and
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bathymetric distribution (Duhamel et al. 2014), are B. maccaini, B.sp. (cf. eatonii) or B. sp.
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(dwarf).
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No juvenile or adult skates were observed in transect A1, but in six of the other transects,
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including the three transects with occasional egg cases, 11 adult skates, most likely B. maccaini
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(see Eastman et al. 2013), were noted in a depth-range of 497‒1257 m. Eight adults were
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imaged between 497 and 834 m depth and three adults at 1184–1229 m depth. Several images
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from the deeper areas surveyed also showed a cloud of disturbed substrate, suggesting that an
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animal on the bottom moved off rapidly. The presence of adult skates is underestimated in
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any photographic survey, due to their skittish nature and rapid escape-speed (Cailliet et al.,
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1999).
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Compared to known skate nurseries, this possible nursery off Anvers Island, Antarctica is quite
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small, even assuming that densities were underestimated because of momentary gaps in
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imaging due to the recharge-time of the strobes and cameras. A site in the eastern Bering Sea,
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sampled by trawling throughout the reproductive season, yielded a broad range of 362‒
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148,957 egg cases/km2 (Hoff, 2008). The highest reported density is 800,000 egg cases/km2 in a
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Bering Sea canyon nursery (Hoff, 2010). In other imaging surveys, estimated densities and/or
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numbers of egg cases observed per unit time are less than those estimated by trawl data but
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still exceed the densities estimated in this study (Love et al., 2008; Hunt et al., 2011). It is
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possible that the photo-transect off Anvers Island imaged the periphery of the main nursery
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area, which could have contained even higher concentrations of egg cases as observed in an
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Alaskan nursery site (Hoff, 2010).
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The foregoing observations in the Southern Ocean are consistent with general aspects of skate
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nurseries in other oceans. Features in common with Bering Sea nurseries include egg cases
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encountered in a narrow depth range on the continental shelf, close to the shelf break, and in
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waters with relatively constant bottom temperatures throughout the year (Hoff, 2010). The
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varied color and condition of egg cases within a single nursery represent multiple generations
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of developing embryos and underscores the fidelity of spawning females to a particular
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depositional site. The abrupt or prolonged appearance of high numbers of egg cases in a single
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transect compared to other transects within the study area has been observed in imaging
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surveys of other regions. Love et al. (2008) had conducted 362 dives off Southern California
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and noted just 44 cases before encountering a region of high egg-case density. In a survey of
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the Shiribeshi Seamount in the Sea of Japan, only one in four transects imaged skate-egg cases
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(Hunt et al., 2011).
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Photographic images of the seafloor off Anvers Island, Antarctica represent the first known
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visual record of skate-egg deposition in the Southern Ocean and strongly suggest the discovery
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of a skate nursery. It is unclear what special feature(s) attracted females, possibly Bathyraja
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spp., to this particular area for egg release. Future photographic or video surveys of this area
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should provide additional insights into the little-known reproductive habits of skate species in
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Antarctica.
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Acknowledgements:
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The research reported in this paper was supported by National Science Foundation grants ANT-
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0838846 and ANT-1141877 to R.B.A., and ANT-0838844 and ANT-1141896 to J.B.M. This is
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contribution 130 from the Institute for Research on Global Climate Change at the Florida
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Institute of Technology. Comments from several anonymous reviewers are greatly appreciated.
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Figure Caption:
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Figure 1. (a) Area of the photographic survey, denoted by rectangle, southwest of Anvers Island,
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Antarctica (approximately 64° S, 66° W), indicated by arrow (modified from Smith et al., 2014).
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(b) Frequency and number of skate-egg cases imaged on seafloor every 500 m during Transect
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A1 conducted at 400–450 m depth southwest of Anvers Island, Antarctica. Images obtained by
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SeaSled every 6 sec at a tow-speed of ~0.56 m/sec. Total area surveyed was ~843 m2. (c) Nine
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skate-egg cases photographed in situ at 424 m from an altitude of 2.61 m above the seafloor.
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