Journal of Fish Biology (2015) 86, 1867–1872 doi:10.1111/jfb.12679, available online at wileyonlinelibrary.com

In situ observations of a possible skate nursery off the western Antarctic Peninsula M. O. Amsler*†, K. E. Smith‡, J. B. McClintock*, H. Singh§, S. Thatje‖, S. C. Vos‡, C. J. Brothers*, A. Brown‖, D. Ellis‡, J. Anderson¶ and R. B. Aronson‡ *Department of Biology, University of Alabama at Birmingham, Birmingham, AL 35294, U.S.A., ‡Department of Biological Sciences, Florida Institute of Technology, 150 West University Boulevard, Melbourne, FL 32901, U.S.A., §Department of Applied Ocean Physics and Engineering, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, U.S.A., ‖Ocean and Earth Science, University of Southampton, European Way, Southampton SO14 3ZH, U.K. and ¶Nature Imagery, under contract to Department of Applied Ocean Physics and Engineering, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, U.S.A.

(Received 12 November 2014, Accepted 25 February 2015) A dense aggregation of skate egg cases was imaged during a photographic survey of the sea floor along the western Antarctic Peninsula in November 2013. Egg cases were noted in a narrow band between 394 and 443 m depth. Although some skate species in other oceans are known to utilize restricted areas to deposit eggs in great numbers, such nurseries have not been described in the Southern Ocean. © 2015 The Fisheries Society of the British Isles

Key words: Antarctica; Elasmobranchii; oviparity; Rajidae; skate egg case.

Among the elasmobranchs, skates are the only group that are strictly oviparous (Conrath & Musick, 2012): in all species, the female releases yolky eggs encased in a tough, leathery capsule. The eggs are large when spawned and the tough egg case provides protection during the lengthy embryonic developmental period, ranging from months to years depending on the species (Hoff, 2008). Some species aggregate to deposit eggs and densities as great as 800 000 egg cases km−2 have been reported for the Alaska skate Bathyraja parmifera (Bean 1881) in the Bering Sea (Hoff, 2009). Many skate species are known to demonstrate site fidelity, returning to the same depositional area or nursery on an annual basis (Hoff, 2010). Nurseries are typically small in area, situated on continental slopes, and usually discovered during exploratory trawling (Hitz, 1964). Known continental slope nursery areas include the Bering Sea for several species of Bathyraja (Hoff, 2010) and the north Pacific for Raja binoculata Girard 1855 (Hitz, 1964). In the Atlantic Ocean, a nursery site was discovered by trawling off North Carolina, U.S.A., for Fenestraja plutonia †Author to whom correspondence should be addressed. Tel.: +1 205 934 1034; email: [email protected]

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(Garman 1881) (Quattrini et al., 2009), and numerous nursery sites off Portugal have been reported for seven Raja species (Serra-Pereira et al., 2014). Nurseries are also discovered during photographic or video surveys of the sea floor, especially around deep bathymetric features inaccessible to trawling. Known skate nurseries discovered via imagery include one at the base of a seamount in the Sea of Japan for Bathyraja smirnovi (Soldatov & Pavlenko 1915) (Hunt et al., 2011), one in a submarine canyon in the Southern California Bight for Raja rhina Jordan & Gilbert 1880 (Love et al., 2008) and others near cold-water seeps in the Mediterranean Sea for Bathyraja spp. (Treude et al., 2011). The distributions and reproductive habits of many Rajidae are generally understood in much of the world ocean, but similar details are lacking in the Southern Ocean; the continental slopes of Antarctica are among the most under-explored marine habitats with respect to fishes (Eastman et al., 2013). Currently, nine skate species are recognized from Antarctica: Amblyraja georgiana (Norman 1938), Amblyraja taaf (Merisner 1987), Bathyraja meridionalis Stehmann 1987, Bathyraja eatonii (Günther 1876), Bathyraja irrasa Hureau & Ozouf-Costaz 1980 and Bathyraja murrayi (Günther 1880) are found in the South Atlantic and Indian Ocean sectors, and Bathyraja maccaini Springer 1971, Bathyraja sp. (cf. eatonii) and Bathyraja sp. (dwarf) are circumpolar (Duhamel et al., 2014). The reproductive habits of all of these species are largely unknown. In November 2013, the R.V. Nathaniel B. Palmer conducted a photographic survey of benthic communities on the continental shelf and slope west of Anvers Island, Antarctica (cruise NBP13-10: 63⋅53∘ S; 66⋅05∘ W to 64⋅30∘ S; 67⋅43∘ W) [Fig. 1(a)]. SeaSled, a towed-camera vehicle (Singh et al., 2007; Eastman et al., 2013), imaged nine benthic transects that were roughly isobathic, in four depth-ranges: 400–700, 700–1100, 1100–1600 and 1600–2100 m. An additional vertical transect cut across depth contours spanning 400–1500 m. SeaSled was equipped with two cameras (1⋅4 megapixel, or 1360 × 1024 pixels, and 2⋅0 megapixel or 1620 × 1220 pixels) and two strobes (150 W-s), all of which fired synchronously every 6 s to yield slightly overlapping, paired stereo images. An onboard acoustic Doppler current profiler (ADCP; 1200 kHz Teledyne RD Instruments; www.rdinstruments.com) enabled SeaSled to be maintained at an altitude of 3–6 m above the sea floor. Continuous conductivity-temperature-depth (CTD) data were gathered onboard with a Seabird SBE-49 Fast CAT 16-Hz recorder (www.seabird.com) provided continuous conductivity, temperature and salinity depth data. Each photographic transect was conducted over a surface distance of c. 9 km and imaged a corridor of the sea floor that was on average 3⋅3 m wide. During an intensive, 5 day survey, over 14 000 paired images were amassed, visualizing c. 135 000 m2 of the sea floor. Each image was corrected for the non-linear attenuation of the colour spectrum in seawater (Eustice et al., 2002). A total of 185 skate egg cases were observed along one transect (A1) run on the continental shelf at 400–445 m depth, with the greatest concentration at 394–443 m [Fig. 1(b)]. Egg cases were first observed 3 km into the transect and were present throughout the remaining 5 km of the dive. Overall, the imaged area had an estimated 20 000 egg cases km−2 . Water temperature was mean ± s.d. 1⋅27 ± 0⋅01∘ C and salinity was constant at 35. An additional eight egg cases were imaged in three other transects within the study area. Three egg cases were noted in the vertical transect at 427, 435 and 535 m depth. The remaining five egg cases were imaged in two transects at 700–1100 m and all were widely dispersed between 723 and 937 m.

© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 1867–1872

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Fig. 1. (a) Area of the photographic survey ( ), south-west of Anvers Island, Antarctica (c. 64∘ S; 66∘ W) ( ) (modified from Smith et al., 2014). (b) Frequency and number of skate egg cases imaged on sea floor every 500 m during transect A1 conducted at 400–450 m depth south-west of Anvers Island, Antarctica. Images obtained by SeaSled every 6 s at a tow speed of c. 0⋅56 m s−1 . Total area surveyed was c. 843 m2 . (c) Nine skate egg cases photographed in situ at 424 m from an altitude of 2⋅61 m above the sea floor.

Egg cases were noted in 93 of the 2260 paired images in the A1 transect. Of those 93 images, 35 had multiple egg cases (maximum n = 9) [see Fig. 1(c) for representative image]. Egg-case colour ranged from golden to dark brown, although the observed colour was somewhat dependent on camera angle. Many of the egg cases (n = 95) appeared bright gold and shiny. The majority (n = 145) were various shades of brown, had visible longitudinal striations and lacked apparent evidence of fouling. Seven egg cases appeared damaged with portions frayed or missing. An average egg case length of 14 cm was determined using Coral Point Count with Excel Extensions (CPCe) software (Kohler & Gill, 2006) and based on metrics defined by Ebert & Davis (2007). The length of each egg case was streamlined and lacked a prominent lateral keel. Anterior and posterior horns appeared to be approximately the same length and curved inward. Obvious attachment structures, either tendril-like fibres or tissue veils, were noted on the presumed posterior horns of 86 egg cases. Of the remaining egg cases, 47 lacked clear attachment features and 52 were not sufficiently resolved to determine attachment status. The egg cases appeared to be randomly strewn across the sea floor with no discernible pattern of orientation. In images containing multiple egg cases, 22 were in direct contact with a neighbouring egg case. Although 60 egg cases appeared to be in direct physical contact with other fauna, there was no suggestion that egg case horns were hooked to an organism. The majority lay flat on the sea floor, presumably on the ventral side. Egg cases observed tipped onto a lateral side (n = 18) were against or among drop-stones.

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Egg case age, time of spawning and even the identity of the source skate species can only be tentatively inferred from clues in the photographs. The range of colour and apparent condition of the egg cases photographed correlate with a three-stage scoring system established for B. parmifera, in which shiny, golden egg cases are newly deposited. Darker ones are previously deposited, and very dark, weathered and fouled egg cases are either old or empty. All three stages can co-occur, although the last stage was least abundant in B. parmifera nurseries (Hoff, 2009). The mean embryonic development time for B. parmifera in the Bering Sea is the longest known for any oviparous elasmobranch: 1290 days at an ambient 4⋅4∘ C. Another Bering Sea species, Raja radiata, requires an average of 912 days at 4⋅6∘ C for complete development (Hoff, 2008). Assuming the ambient water temperature of 1⋅27∘ C remained constant year-round and a development rate similar to B. parmifera in the Bering Sea, even a conservative correlation between temperature and embryonic development would suggest that >4 years would be required for the most recently deposited egg cases imaged to fully develop and hatch. The morphology of egg cases photographed in the A1 transect appears consistent with the genus Bathyraja (Ishihara et al., 2012). It has been suggested that the egg case morphology of Bathyraja is highly conserved within and between species of the south-western Atlantic and northern hemisphere oceans (Mabragaña et al., 2011). Evidence presented here suggests that the similarity may extend to species in the Southern Ocean. Assuming that the imaged egg cases are those of a Bathyraja, the probable candidates, based on reported adult geographic and bathymetric distribution (Duhamel et al., 2014), are B. maccaini, Bathyraja sp. (cf. eatonii) or Bathyraja sp. (dwarf). No juvenile or adult skates were observed in transect A1, but in six of the other transects, including the three transects with occasional egg cases, 11 adult skates, most likely B. maccaini (Eastman et al., 2013), were noted in a depth range of 497–1257 m. Eight adults were imaged between 497 and 834 m depth and three adults at 1184–1229 m depth. Several images from the deeper areas surveyed also showed a cloud of disturbed substratum, suggesting that an animal on the bottom had moved off rapidly. The presence of adult skates is underestimated in any photographic survey, due to their skittish nature and rapid escape speed (Cailliet et al., 2005). Compared with known skate nurseries, this possible nursery off Anvers Island, Antarctica, is quite small, even assuming that densities were underestimated because of momentary gaps in imaging due to the recharge time of the strobes and cameras. A site in the eastern Bering Sea, sampled by trawling throughout the reproductive season, yielded a broad range of 362–148 957 egg cases km−2 (Hoff, 2008). The highest reported density is 800 000 egg cases km−2 in a Bering Sea canyon nursery (Hoff, 2010). In other imaging surveys, estimated densities and numbers of egg cases observed per unit time are less than those estimated by trawl data, but still exceed the densities estimated in this study (Love et al., 2008; Hunt et al., 2011). It is possible that the phototransect off Anvers Island imaged the periphery of the main nursery area, which could have contained even higher concentrations of egg cases as observed in an Alaskan nursery site (Hoff, 2010). The foregoing observations in the Southern Ocean are consistent with general aspects of skate nurseries in other oceans. Features in common with Bering Sea nurseries include egg cases encountered in a narrow depth range on the continental shelf, close to the shelf break and in waters with relatively constant bottom temperatures throughout the year (Hoff, 2010). The varied colour and condition of egg cases within a single

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nursery represent multiple generations of developing embryos and underscore the fidelity of spawning females to a particular depositional site. The abrupt or prolonged appearance of high numbers of egg cases in a single transect compared with other transects within the study area has been observed in imaging surveys of other regions. Love et al. (2008) had conducted 362 dives off southern California and noted just 44 cases before encountering a region of high egg-case density. In a survey of the Shiribeshi Seamount in the Sea of Japan, only one in four transects imaged skate egg cases (Hunt et al., 2011). Photographic images of the sea floor off Anvers Island, Antarctica, represent the first known visual record of skate egg deposition in the Southern Ocean and strongly suggest the discovery of a skate nursery. It is unclear what special features attracted females, possibly Bathyraja spp., to this particular area for egg release. Future photographic or video surveys of this area should provide additional insights into the little known reproductive habits of skate species in Antarctica. The research reported in this paper was supported by National Science Foundation grants ANT-0838846 and ANT-1141877 to R.B.A., and ANT-0838844 and ANT-1141896 to J.B.M. This is contribution 130 from the Institute for Research on Global Climate Change at the Florida Institute of Technology. Comments from several anonymous reviewers are greatly appreciated.

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Hoff, G. R. (2010). Identification of skate nursery habitat in the eastern Bering Sea. Marine Ecology Progress Series 403, 243–254. Hunt, J. C., Lindsay, D. J. & Shahalemi, R. R. (2011). A nursery site of the golden skate (Rajiformes: Rajidae: Bathyraja smirnovi) on the Shiribeshi Seamount, Sea of Japan. Marine Biodiversity Records 4, e70. doi: 10.1017/S1755267211000728 Ishihara, H., Treloar, M., Bor, P., Senou, H. & Jeong, C. (2012). The comparative morphology of skate egg capsules (Chondrichthyes: Elasmobranchii: Rajiformes). Bulletin of Kanagawa Prefectural Museum (Natural Science) 41, 9–25. Kohler, K. E. & Gill, S. M. (2006). Coral Point Count with Excel Extensions (CPCe): a visual basic program for the determination of coral and substrate coverage using random point count methodology. Computers and Geosciences 32, 1259–1269. Love, M. S., Schroeder, D. M., Snook, L., York, A. & Cochrane, G. (2008). All their eggs in one basket: a rocky reef nursery for the longnose skate (Raja rhina Jordan & Gilbert, 1880) in the southern California Bight. Fishery Bulletin 106, 471–475. Mabragaña, E., Figueroa, D., Scenna, L., Díaz de Astarloa, J., Colonello, J. & Delpiani, G. (2011). Chondrichthyan egg cases from the south-west Atlantic Ocean. Journal of Fish Biology 79, 1261–1290. Quattrini, A. M., Partyka, M. L. & Ross, S. W. (2009). Aspects of the reproductive biology of the skate Fenestraja plutonia (Garman) off North Carolina. Southeastern Naturalist 8, 55–70. Serra-Pereira, B., Erzini, K., Maia, C. & Figueiredo, I. (2014). Identification of potential essential fish habitats for skates based on fishers’ knowledge. Environmental Management 53, 985–998. Singh, H., Roman, C., Pizarro, O. & Can, A. (2007). Towards high resolution imaging from underwater vehicles. International Journal of Robotics Research 26, 55–74. Smith, K. E., Thatje, S., Singh, H., Amsler, M. O., Vos, S. C., McClintock, J. B., Brothers, C. J., Brown, A., Ellis, D. & Anderson, J. (2014). Discovery of a recent, natural whale fall on the continental slope off Anvers Island, western Antarctic Peninsula. Deep Sea Research I 90, 76–80. Treude, T., Kiel, S., Linke, P., Peckmann, J. & Goedert, J. L. (2011). Elasmobranch egg capsules associated with modern and ancient cold seeps: a nursery for marine deep-water predators. Marine Ecology Progress Series 437, 175–181.

© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 1867–1872

In situ observations of a possible skate nursery off the western Antarctic Peninsula.

A dense aggregation of skate egg cases was imaged during a photographic survey of the sea floor along the western Antarctic Peninsula in November 2013...
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