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Metabolism of Gymnosomatous Pteropods in Waters of the Western Antarctic Peninsula Shelf During Austral Fall

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Metabolism of Gymnosomatous Pteropods in Waters of the Western Antarctic Peninsula Shelf During Austral Fall Vol. 518: 69–83, 2015 MARINE ECOLOGY PROGRESS SERIES Published January 7 doi: 10.3354/meps11050 Mar Ecol Prog Ser Metabolism of gymnosomatous pteropods in waters of the western Antarctic Peninsula shelf during austral fall Paul M. Suprenand1,2,*, Erica H. Ombres2, Joseph J. Torres2 1NMFS RTR Program, University of Florida, PO Box 110240, Gainesville, Florida 32611, USA 2College of Marine Science, University of South Florida, 140 7th Avenue South, St. Petersburg, Florida 33701, USA ABSTRACT: Two species of Southern Ocean gymnosomatous pteropods with dissimilar distribu- tional ranges were collected from western Antarctic Peninsula (WAP) shelf waters in the vicinity of Anvers, Lavoisier, Adelaide and Charcot Islands from March to April 2010 and between 0 and 500 m. The sub-Antarctic gymnosome species, Spongiobranchaea australis, typically occupies regions north of the Polar Front, whereas the true Antarctic gymnosome species, Clione antarc- tica, inhabits colder waters and higher latitudes. Oxygen consumption rates, ammonia excretion rates, proximate body compositions and the activities of 3 metabolic enzymes — lactate dehydro- genase, malate dehydrogenase, and citrate synthase (CS) — were determined in both gymnosome species. Oxygen consumption rates of S. australis and C. antarctica were found to be similar; how- ever, the mean ratio of oxygen consumed to ammonia excreted (O:N, 61.26 ± 18.68:1) indicated that S. australis was oxidizing primarily lipids while C. antarctica was oxidizing a mixture of proteins and lipids (26.41 ± 14.82:1). Proximate body compositions based on percent protein, per- cent lipid, and carbon to nitrogen ratios, suggested larger lipid storage in C. antarctica (~5%) than in S. australis (~3%). CS activities among gymnosomes were dissimilar, and comparisons of enzyme activities were made to other Antarctic organisms. Observed differences in S. australis’ physiological indicators may be related to prolonged starvation, whereas C. antarctica appears ready to survive overwintering in Antarctica. Water mass advection from the Antarctic Circum- polar Current is thought to be transporting S. australis onto the WAP shelf, and away from its typical sub-Antarctic habitat. KEY WORDS: Pteropod · Zooplankton · Western Antarctic Peninsula · Oxygen consumption rate · Starvation Resale or republication not permitted without written consent of the publisher INTRODUCTION Antarctica there are only 2 gymnosome species, Spongiobranchaea australis (d’Orbigny 1836), com- Pteropods are holoplanktonic gastropod molluscs mon north of the Polar Front (PF), and Clione divided into 2 orders, Thecosomata (shelled ptero - antarctica (Smith 1902), considered to be an exclu- pods) and Gymnosomata (naked pteropods), which sively Antarctic species (Hunt et al. 2008). Southern collectively are food for zooplankton (e.g. chaetog- Ocean gymnosomes have therefore likely adapted naths and heteropods), fish, whales, seals, and physiologically to live within narrow thermal birds (Lebour 1932, Dunbar 1942, LeBrasseur 1966, ranges called ‘climate envelopes’ as dictated by Lalli & Gilmer 1989, Hunt et al. 2008, Karnovsky their habitat (Pearson & Dawson 2003, Seibel et al. et al. 2008). In the Southern Ocean surrounding 2007). *Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 70 Mar Ecol Prog Ser 518: 69–83, 2015 Antarctic gymnosomes are physiologically special- may have two. Direct measurements of oxygen con- ized predators that have coevolved with their theco- sumption rates have been made on a few species of some prey (Lalli & Gilmer 1989). For instance, C. gymnosomes (Conover & Lalli 1974, Ikeda 1985, antarctica exhibits a suite of cold-adapted character- Seibel & Dierssen 2003, Seibel et al. 2007, Maas et al. istics including a single locomotory gait (Rosenthal et 2011a), but no physiological study, other than details al. 2009) and elevated oxygen consumption rates of lipid composition (e.g. Phleger et al. 1999), cur- (Seibel et al. 2007). Gymnosomes have greater abun- rently exists in the literature for S. australis from any- dances in colder, temperate, and polar waters (Lalli & where around Antarctica. Gilmer 1989, van der Spoel et al. 1999, Hunt et al. Measurements of the activities of key enzymes in 2008), which are geographic regions currently expe- the intermediary metabolism are useful as proxies for riencing rapid climate change (e.g. Meredith & King the whole animal metabolic rate and as indicators of 2005). Describing the physiology of Antarctic gymno- anaerobic and aerobic potential. Lactate dehydro- somes is an important first step for understanding genase (LDH), malate dehydrogenase (MDH), and their responses to a changing polar climate (e.g. Pört- citrate synthase (CS), because of their essential roles ner et al. 2007, Pörtner & Farrell 2008), and currently in producing ATP (Childress & Somero 1979, Seibel no studies have reported the physiological character- & Drazen 2007), are especially useful indicators. istics of any gymnosome pteropods along the western Maximal activities of the key enzymes LDH, MDH, Antarctic Peninsula (WAP), where they may experi- and CS have traditionally been used as proxies for ence higher seasonal temperatures than the previ- metabolic rate (Shapiro & Bobkova 1975, Torres & ously studied Ross Sea populations. Somero 1988, Seibel et al. 2000, González et al. The polar marine ecosystem is usually characterized 2008), but until now have only been measured in by permanently low, stable temperatures (Clarke & wing muscle of C. antarctica (Dymowska et al. 2012). Peck 1991), and a tradeoff for life adapted to perma- As S. australis and C. antarctica are reported to nently low temperatures is a decreased tolerance of have dissimilar distributional ranges around Ant- changing temperatures (Clarke 1988, Peck et al. 2004, arctica (Hunt et al. 2008), and because of the sea- Somero 2004, 2010, Cheng & Detrich 2007, Pörtner et sonal transition occurring during the time of the al. 2007). For the Antarctic gymnosome C. antarctica, present study, we also explored the physiological which lives permanently at temperatures near −1.89°C characteristics of both gymnosomes in relation to the over much of its range (Seibel et al. 2007), or the sub- latitudinal gradient of this study’s sampling sites Antarctic S. australis that experiences an annual along the WAP. In this exploration we postulated that water temperature range of 0 to 4°C from sea surface there would be significant differences in gymnosome to depth within the Antarctic Circumpolar Current physiology given their dissimilar distributional ran - (ACC) and near the WAP (Gordon et al. 1986), tem- ges around Antarctica. perature has a considerable potential for influencing both their physiological conditions and therefore their distributional ranges (e.g. Roy et al. 1998, Astorga et MATERIALS AND METHODS al. 2003, Pörtner et al. 2005). The purpose of the present study was to assess the Gymnosome and hydrographic data collection physiological characteristics of Southern Ocean gym- nosomes along the WAP. Specifically, we measured Gymnosomes were collected in MOCNESS (multi- the oxygen consumption rates, ammonia excretion ple opening and closing nets and environmental rates, atomic ratios of oxygen consumed to nitrogen sampling system) trawls from March to May 2010 excreted, proximate body compositions, carbon: along a latitudinal gradient in WAP shelf waters from hydrogen: nitrogen ratios, and enzymatic activities of the research vessel ice breaker (R.V.I.B.) ‘Nathaniel polar gymnosomes captured from a latitudinal gradi- B. Palmer’. The cruise track ranged from Charcot ent along the WAP. Oxygen consumption rates are Island in the south to Anvers Island in the north strongly influenced by growth, reproduction, activity (Fig. 1, Sites 1 to 4). A 10 m2 MOCNESS fitted with level, feeding rates, and resource utilization (Pörtner 3 mm mesh nets and capable of collecting vertically et al. 2007, Seibel & Drazen 2007). Most gymnosomes stratified samples was used for sample collection swim continuously (Lalli & Gilmer 1989, Seibel et al. (MOC-10; Wiebe et al. 1976, 1985, Donnelly & Torres 2007), and, while C. antarctica has only one swim- 2008, Parker et al. 2011). Vertically stratified sam- ming gait (Rosenthal et al. 2009), visual observations pling was performed within 5 discrete depth layers during the present study suggested that S. australis between 0 and 500 m. The initial, or drogue net, Suprenand et al.: Western Antarctic Peninsula pteropod metabolism 71 Fig. 1. Western Antarctic Peninsula (WAP) with inset map denoting sampling area from which gymnosomes were sampled for physiological determinations. Black diamonds at Sites 1 to 4 represent locations of the 10 m2 multiple opening and closing net and environmental sampling system (MOC-10) trawls. Circulation of the Antarctic Circumpolar Current and sub-gyres in the Bellingshausen Sea at 400 to 200 m along the WAP are adapted from Smith et al. (1999) and denoted by arrows trawled obliquely to 500 m, with subsequent nets were captured along the WAP during this study’s sampling 500−300, 300−200, 200−100, 100−50, and sampling period by either MOC-10 or MOC-1 trawls. 50−0 m (Nets 1–5, respectively). Towing speeds ranged from 1.5 to 2.5 knots. Upon retrieval, contents of each MOC-10 net were emptied into 19 l buckets, Respirometry (oxygen consumption rates) and and the gymnosomes present in each bucket were ammonia excretion measurements removed, enumerated, and identified to species
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