Energetics of the Antarctic Silverfish, Pleuragramma antarctica, from the Western Antarctic Peninsula

Chapter
Part of the Advances in Polar Ecology book series (AVPE, volume 3)

Abstract

The nototheniid Pleuragramma antarctica, commonly known as the Antarctic silverfish, dominates the pelagic fish biomass in most regions of coastal Antarctica. In this chapter, we provide shipboard oxygen consumption and nitrogen excretion rates obtained from P. antarctica collected along the Western Antarctic Peninsula and, combining those data with results from previous studies, develop an age-dependent energy budget for the species. Routine oxygen consumption of P. antarctica fell in the midrange of values for notothenioids, with a mean of 0.057 ± 0.012 ml O2 g−1 h−1 (χ ± 95% CI). P. antarctica showed a mean ammonia-nitrogen excretion rate of 0.194 ± 0.042 μmol NH4-N g−1 h−1 (χ ± 95% CI). Based on current data, ingestion rates estimated in previous studies were sufficient to cover the metabolic requirements over the year classes 0–10. Metabolism stood out as the highest energy cost to the fish over the age intervals considered, initially commanding 89%, gradually declining to 67% of the annual energy costs as the fish aged from 0 to 10 years. Overall, the budget presented in the chapter shows good agreement between ingested and combusted energy, and supports the contention of a low-energy lifestyle for P. antarctica, but it also resembles that of other pelagic species in the high percentage of assimilated energy devoted to metabolism. It differs from more temperate coastal pelagic fishes in its large investment in reproduction and its pattern of slow steady growth throughout a relatively long lifespan.

Keywords

Fish metabolism Energy budget Antarctic fishes 

References

  1. Ainley DG, DeMaster DP (1990) The upper trophic levels in polar marine ecosystems. In: Smith WO Jr (ed) Polar oceanography, part B, chemistry, biology, and geology. Academic, San Diego, pp 599–630CrossRefGoogle Scholar
  2. Barham EG (1971) Deep-sea fishes: lethargy and vertical orientation. In: Farquhar GB (ed) Proceedings of an international symposium on biological sound scattering in the ocean US Government Printing Office, Washington, DC, pp 100–118Google Scholar
  3. Boyce S (1999) Nitrogenous excretion in the Antarctic plunderfish. J Fish Biol 54:72–81CrossRefGoogle Scholar
  4. Brett J, Groves T (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic, New York, pp 279–352Google Scholar
  5. Brett J, Shelbourn JE, Shoop CT (1969) Growth rate and body composition of fingerling sockeye salmon, Oncorhynchus nerka, in relation to temperature and ration size. J Fish Res Board Can 26:2363–2394CrossRefGoogle Scholar
  6. Butler J, Granados M, Barnes J et al (1996) Age composition, growth, and maturation of the Pacific sardine (Sardinops sagax) during 1994. Calif Coop Oceanic Fish Invest Rep 37:152–159Google Scholar
  7. Childress J, Somero G (1979) Depth-related enzymic activities in muscle, brain and heart of deep-living pelagic marine teleosts. Mar Biol 52:273–283CrossRefGoogle Scholar
  8. Childress JJ, Nygaard MH (1973) The chemical composition of midwater fishes as a function of depth of occurence off southern California. Deep-Sea Res Oceanogr Abstr 20(12):1043–1143CrossRefGoogle Scholar
  9. Cullins TL, Devries AL, Torres JJ (2011) Antifreeze proteins in pelagic fishes from Marguerite Bay (Western Antarctica). Deep Sea Res Part 2 Top Stud Oceanogr 58:1690–1694CrossRefGoogle Scholar
  10. Daniels RA (1982) Feeding ecology of some fishes of the Antarctic peninsula. Fish Bull 80:575–588Google Scholar
  11. Daniels RA, Lipps JH (1982) Distribution and ecology of fishes of the Antarctic peninsula. J Biogeogr 9:1–9CrossRefGoogle Scholar
  12. DeVries AL, Eastman JT (1978) Lipid sacs as a buoyancy adaptation in an Antarctic fish. Nature 271:352–353CrossRefGoogle Scholar
  13. De Witt HH (1970) The character of the midwater fish fauna of the Ross Sea, Antarctica. In: Holdgate MW (ed) Antarctic ecology, vol 1. Academic, London, pp 305–314Google Scholar
  14. De Witt HH, Hopkins T (1977) Aspects of the diet of the Antarctic silverfish, Pleuragramma antarcticum. In: Llano GA (ed) Adaptations within Antarctic ecosystems. Gulf Publishing CO, Houston, pp 557–568Google Scholar
  15. Donnelly J, Torres JJ (2008) Pelagic fishes in the Marguerite Bay region of the West Antarctic Peninsula continental shelf. Deep Sea Res Part 2 Top Stud Oceanogr 55:523–539CrossRefGoogle Scholar
  16. Donnelly J, Torres JJ, Hopkins T et al (1994) Chemical composition of Antarctic zooplankton during austral fall and winter. Polar Biol 14:171–183CrossRefGoogle Scholar
  17. Donnelly J, Torres JJ, Sutton T et al (2004) Fishes of the eastern Ross Sea, Antarctica. Polar Biol 27:637–650CrossRefGoogle Scholar
  18. Duhamel G, Kock K-H, Balguerias E et al (1993) Reproduction in fish of the Weddell Sea. Polar Biol 13:193–200CrossRefGoogle Scholar
  19. Durbin E, Durbin A (1981) Assimilation efficiency and nitrogen excretion of a filter-feeding planktyvore, the Atlantic menhaden, Brevoortia tyrannus (Pisces: Clupeidae). Fish Bull U.S 79:601–616Google Scholar
  20. Eastman JT, DeVries AL (1982) Buoyancy studies of notothenioid fishes in McMurdo Sound. Antarctica Copeia:385–393Google Scholar
  21. Eastman JT, DeVries AL (1989) Ultrastructure of the lipid sac wall in the Antarctic notothenioid fish Pleuragramma antarcticum. Polar Biol 9:333–335CrossRefGoogle Scholar
  22. Eastman JT, Witmer LM, Ridgely RC et al (2014) Divergence in skeletal mass and bone morphology in antarctic notothenioid fishes. J Morphol 275:841–861CrossRefGoogle Scholar
  23. Elliot J (1975a) The growth rate of brown trout (Salmo trutta L.) fed on maximum rations. J Anim Ecol 44:805–821CrossRefGoogle Scholar
  24. Elliot J (1975b) The growth rate of brown trout (Salmo trutta L.) fed on reduced rations. J Anim Ecol 44:823–842CrossRefGoogle Scholar
  25. Elliott JM, Davison W (1975) Energy equivalents of oxygen consumption in animal energetics. Oecologia 19:195–201Google Scholar
  26. Faleeva TI, Gerasimchuk V (1990) Features of reproduction in the Antarctic sidestripe, Pleuragramma antarcticum (Nototheniidae). J Ichthyol 30:67–79Google Scholar
  27. Forster M, Franklin C, Taylor H et al (1987) The aerobic scope of an Antarctic fish, Pagothenia borchgrevinki and its significance for metabolic cold adaptation. Polar Biol 8:155–159CrossRefGoogle Scholar
  28. Fuiman L, Davis R, Williams T (2002) Behavior of midwater fishes under the Antarctic ice: observations by a predator. Mar Biol 140:815–822CrossRefGoogle Scholar
  29. Gartner JV (1993) Patterns of reproduction in the dominant lanternfish species (Pisces: Myctophidae) of the eastern Gulf of Mexico, with a review of reproduction among tropical-subtropical Myctophidae. Bull Mar Sci 52:721–750Google Scholar
  30. Gartner JRJ, Crabtree RE, Sulak KJ (1997) Feeding at depth. In: Randall D, Farrell A (eds) Deep-sea fishes. Academic, New York, pp 115–193CrossRefGoogle Scholar
  31. Gerasimchuk V (1986) Characteristics of Antarctic silverfish, Pleuragramma antarcticum (Nototheniidae), from Olaf-Pruds Bay (Commonwealth Sea, eastern Antarctica) with notes on the identification of the species. J Ichthyol 26:10–17Google Scholar
  32. Gerasimchuk V (1987) On the fecundity of the Antarctic silverfish Pleuragramma antarcticum. Voproci Ikhtiologii 27:858–860Google Scholar
  33. Gerasimchuk V (1992) A brief outline of the biology of the Antarctic silverfish, Pleuragramma antarcticum Boulenger, 1902 (Nototheniidae) from the Antarctic Indian Ocean. Document WG-FSA-92/11 rev. 1. CCAMLR, Hobart, p 53Google Scholar
  34. Ghigliotti L, Gerasimchuk VV, Kock H-K et al (2017) Reproductive strategies of the Antarctic silverfish: known knowns, known unknowns and unknown unknowns. In: Vacchi M, Pisano E, Ghigliotti L (eds) The Antarctic silverfish. A keystone species in a changing ecosystem. Advances in Polar Ecology 3. doi:  10.1007/978-3-319-55893-6_9
  35. Greely TM, Gartner JV, Torres JJ (1999) Age and growth of Electrona Antarctica (Pisces: Myctophidae), the dominant mesopelagic fish of the Southern Ocean. Mar Biol 133:145–158CrossRefGoogle Scholar
  36. Guidetti P, Ghigliotti L, Vacchi M (2015) Insights on spatial distribution patterns of early stages of the Antarctic silverfish, Pleuragramma antarctica, in the platelet ice of Terra Nova Bay, Antarctica. Polar Biol 38(3):333–342. doi: 10.1007/s00300-014-1589-4 CrossRefGoogle Scholar
  37. Hagen W, Kattner G, Friedrich C (2000) The lipid compositions of high-Antarctic notothenioid fish species with different life strategies. Polar Biol 23:785–791CrossRefGoogle Scholar
  38. Hagen W, Kattner G (2017) The role of lipids in the life history of the Antarctic silverfish Pleuragramma antarctica. In: Vacchi M, Pisano E, Ghigliotti L (eds) The Antarctic silverfish. A keystone species in a changing ecosystem. Adv Polar Ecol 3. doi: 10.1007/978-3-319-55893-6_7
  39. Handy R, Poxoxton M (1993) Nitrogen pollution in mariculture: toxicity and excretion of nitrogenous compounds by marine fish. Rev Fish Biol Fish 3:205–241CrossRefGoogle Scholar
  40. Hemmingsen EA, Douglas EL (1970) Respiratory characteristics of the hemoglobin-free fish Chaenocephalus aceratus. Comp Biochem Physiol 33:733–744CrossRefGoogle Scholar
  41. Holeton GF (1970) Oxygen uptake and circulation by a hemoglobinless Antarctic fish (Chaenocephalus aceratus Lonnberg) compared with three red-blooded Antartic fish. Comp Biochem Physiol 34:457–471CrossRefGoogle Scholar
  42. Hopkins T, Torres JJ (1988) The zooplankton community in the vicinity of the ice edge, western Weddell Sea, march 1986. Polar Biol 9:79–87CrossRefGoogle Scholar
  43. Hubold G (1982) Eggs and larvae of Engraulis anchoita Hubbs and Marini, 1935 in the Southwest Atlantic between 25°S S and 40°S. Meeresforschung 29(4):208–218Google Scholar
  44. Hubold G (1984) Spatial distribution of Pleuragramma antarcticum (Pisces: Nototheniidae) near the Filchner-and Larsen ice shelves (Weddell Sea/Antarctica). Polar Biol 3:231–236CrossRefGoogle Scholar
  45. Hubold G (1985) The early life-history of the high-Antarctic silverfish, Pleuragramma antarcticum. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 445–451CrossRefGoogle Scholar
  46. Hubold G (1992) Ecology of Weddell Sea fishes. Ber Polarforsch 103:1–157Google Scholar
  47. Hubold G, Ekau W (1987) Midwater fish fauna of the Weddell Sea, Antarctica. Proc 5th Congr Eur Ichthyol, Stockholm 1985, pp 391–396Google Scholar
  48. Hubold G, Hagen W (1997) Seasonality of feeding and lipid content in juvenile Pleuragramma antarcticum (Pisces: Nototheniidae) from the southern Weddell Sea. In: Battaglia B, Valencia J, Walton WH (eds) Antarctic communities. Species, structure and survival. Cambridge University Press, New York, pp 277–283Google Scholar
  49. Hubold G, Tomo A (1989) Age and growth of Antarctic silverfish Pleuragramma antarcticum Boulenger, 1902, from the southern Weddell Sea and Antarctic peninsula. Polar Biol 9:205–212CrossRefGoogle Scholar
  50. James A, Probyn T, Hutchings L (1989) Laboratory-derived carbon and nitrogen budgets for the omnivorous planktivore Engraulis Capensis Gilchrist. J Exp Mar Biol Ecol 131:125–145CrossRefGoogle Scholar
  51. Jones RD (1991) An improved fluorescence method for the determination of nanomolar concentrations of ammonium in natural waters. Limnol Oceanogr 36:814–819CrossRefGoogle Scholar
  52. Kellermann A (1987) Food and feeding ecology of postlarval and juvenile Pleuragramma antarcticum (Pisces; Notothenioidei) in the seasonal pack ice zone off the Antarctic peninsula. Polar Biol 7:307–315CrossRefGoogle Scholar
  53. Klink JM, Hofmann EE, Beardsley R C et al (2004) Water-mass properties and circulation on the west Antarctic Peninsula Continental Shelf in Austral Fall and Winter 2001. Deep Sea Res Part 2 Top Stud Oceanogr 51:1925–1946Google Scholar
  54. Kock K-H (1992) Antarctic fish and fisheries. Cambridge University Press, Cambridge UniversityGoogle Scholar
  55. Kock K-H, Kellermann A (1991) Reproduction in Antarctic notothenioid fish. Antarct Sci 3:125–150CrossRefGoogle Scholar
  56. Koubbi P, Vallet C, Razouls S et al (2007) Condition and diet of larval Pleuragramma antarcticum (Nototheniidae) from Terre Adélie (Antarctica) during summer. Cybium 31:67–76Google Scholar
  57. La Mesa M, Eastman JT (2012) Antarctic silverfish: life strategies of a key species in the high-Antarctic ecosystem. Fish Fish 13:241–266CrossRefGoogle Scholar
  58. La Mesa M, Riginella E, Mazzoldi C et al (2014) Reproductive resilience of ice-dependent Antarctic silverfish in a rapidly changing system along the western Antarctic peninsula. Mar Ecol 36(2):235–245CrossRefGoogle Scholar
  59. Lancraft TM, Torres JJ, Hopkins TL (1989) Micronekton and macrozooplankton in the open waters near Antarctic ice edge zones (AMERIEZ 1983 and 1986). Polar Biol 9:225–233CrossRefGoogle Scholar
  60. Lancraft TM, Reisenbichler KR, Robison BH et al (2004) A krill-dominated micronekton and macrozooplankton community in Croker Passage, Antarctica with an estimate of fish predation. Deep Sea Res Part 2 Top Stud Oceanogr 51:2247–2260CrossRefGoogle Scholar
  61. Lasker R (1970) Utilization of zooplankton energy by a Pacific sardine population in the California current. In: Steele JH (ed) Marine food chains. Oliver and Boyd, Edinburgh, pp 265–284Google Scholar
  62. MacDonald J, Montgomery J, Wells R (1987) Comparative physiology of Antarctic fishes. Adv Mar Biol 24:321–388CrossRefGoogle Scholar
  63. Marshall NB (1971) Explorations in the life of fishes. Cambridge, Harvard University PressCrossRefGoogle Scholar
  64. Masserini RT, Fanning KA (2000) A sensor package for the simultaneous determination of nanomolar concentrations of nitrite, nitrate, and ammonia in seawater by fluorescence detection. Mar Chem 68:323–333CrossRefGoogle Scholar
  65. McCarthy JJ, Whitledge TE (1972) Nitrogen Excretion by Anchovy Engraulis mordax and E. ringens and Jack Mackerel (Trahurus symmetricus). Fish Bull U.S 70:395–401Google Scholar
  66. Moreno C, Rueda T, Asencio G (1986) Nicho trófico de Pleuragramma antarcticum en la región del estrecho Bransfield, con una comparación cuantitativa con otras áreas del Océano Antártico. Inst Antárt Chileno Ser Cien:145–169Google Scholar
  67. Morris D, North A (1984) Oxygen consumption of five species of fish from South Georgia. J Exp Mar Biol Ecol 78:75–86CrossRefGoogle Scholar
  68. Near TJ, Jones CD, Eastman JT (2009) Geographic intraspecific variation in buoyancy within Antarctic notothenioid fishes. Antarct Sci 21:123–129CrossRefGoogle Scholar
  69. Olaso I, Lombarte A, Velasco F (2004) Daily ration of antarctic silverfish Pleuragramma antarcticum (Boulenger, 1902) in the eastern Weddell Sea. Sci Mar 68:419–424CrossRefGoogle Scholar
  70. Parker ML, Fraser WR, Ashford J et al (2015) Assemblages of micronektonic fishes and invertebrates in a gradient of regional warming along the western Antarctic peninsula. J Mar Syst 152:18–41CrossRefGoogle Scholar
  71. Pinkerton MH (2017) Diet and trophic ecology of adult Antarctic silverfish (Pleuragramma antarctica) In: Vacchi M, Pisano E, Ghigliotti L (eds) The Antarctic silverfish. A keystone species in a changing ecosystem. Springer series advances in polar ecology (in press)Google Scholar
  72. Radke RL, Hubold G, Folsom SD et al (1993) Otolith structural and chemical analyses: the key to resolving age and growth of the Antarctic silverfish, Pleuragramma antarcticum. Antarct Sci 5:51–62Google Scholar
  73. Ralph R, Everson I (1968) The respiratory metabolism of some Antarctic fish. Comp Biochem Physiol 27:299–307CrossRefGoogle Scholar
  74. Reinhardt S, Van Vleet E (1986) Lipid composition of twenty-two species of Antarctic midwater zooplankton and fish. Mar Biol 91:149–159CrossRefGoogle Scholar
  75. Reisenbichler KR (1993) Growth and chemical composition in two populations of the Antarctic silverfish, Pleuragramma antarcticum (Pisces, Notoheniidae). Master’s of arts in biology Master’s, University of California, USGoogle Scholar
  76. Robison BH (2003) What drives the diel vertical migrations of Antarctic midwater fish? J Mar Biol Ass UK 83:639–642CrossRefGoogle Scholar
  77. Sayer M, Davenport J (1987) The relative importance of the gills to ammonia and urea excretion in five seawater and one freshwater teleost species. J Fish Biol 31:561–570CrossRefGoogle Scholar
  78. Steffensen JF (2005) Respiratory systems and metabolic rates. In: AP Farrell, JF Steffensen (eds) Fish physiology: the physiology of polar fish. Elsevier, vol 22, pp 203–238Google Scholar
  79. Sutton C, Horn P (2011) A preliminary assessment of age and growth of Antarctic silverfish. CCAMLR Sci 18:75–86Google Scholar
  80. Tavernier E, Giraldo C (2017) Trophic ecology of early developmental stages of Antarctic silverfish. In: Vacchi M, Pisano E, Ghigliotti L (eds) The Antarctic silverfish. A keystone species in a changing ecosystem. Springer series advances in polar ecology (in press)Google Scholar
  81. Targett TE (1981) Trophic ecology and structure of coastal Antarctic fish communities. Mar Ecol Prog Ser 4:243–263CrossRefGoogle Scholar
  82. Torres J, Somero G (1988a) Metabolism, enzymic activities and cold adaptation in Antarctic mesopelagic fishes. Mar Biol 98:169–180CrossRefGoogle Scholar
  83. Torres J, Somero G (1988b) Vertical distribution and metabolism in Antarctic mesopelagic fishes. Comp Biochem Physiol B Biochem Mol Biol 90:521–528CrossRefGoogle Scholar
  84. Torres JJ, Donnelly J, Hopkins TL et al (1994) Proximate composition and overwintering strategies of Antarctic micronektonic Crustacea. Mar Ecol Prog Ser 113(3):221–232CrossRefGoogle Scholar
  85. Vacchi M, La Mesa M, Dalù M et al (2004) Early life stages in the life cycle of Antarctic silverfish, Pleuragramma antarcticum in Terra Nova Bay, Ross Sea. Antarct Sci 16:299–305CrossRefGoogle Scholar
  86. Vacchi M, Koubbi P, Ghigliotti L et al (2012) Sea-ice interactions with polar fish: focus on the Antarctic silverfish life history. In: Verde C, di Prisco G (eds) Adaptation and evolution in marine environments, From pole to pole series, vol 1. Springer, Berlin/Heidelberg, pp 51–73CrossRefGoogle Scholar
  87. Vallet C, Beans C, Koubbi P et al (2011) Food preferences of larvae of Antarctic silverfish Pleuragramma antarcticum Boulenger, 1902 from Terre Adélie coastal waters during summer 2004. Polar Sci 5:239–251CrossRefGoogle Scholar
  88. Vaughan DG, Marshall GJ, Connolley WM et al (2003) Recent rapid regional climate warming on the Antarctic peninsula. Clim Chang 60:243–274CrossRefGoogle Scholar
  89. Voskoboinikova O, Detrich HW III, Albertson C et al (2017) Evolution reshaped life for the water column: the skeleton of the Antarctic silverfish Pleuragramma antarctica Boulenger, 1902. In: Vacchi M, Pisano E, Ghigliotti L (eds) The Antarctic silverfish. A keystone species in a changing ecosystem. Advances in Polar Ecology 3. doi:  10.1007/978-3-319-55893-6_1
  90. Wells RM (1987) Respiration of antarctic fish from McMurdo sound. Comp Biochem Physiol A Physiol 88:417–424CrossRefGoogle Scholar
  91. Williams R (1985) Trophic relationships between pelagic fish and euphausiids in Antarctic waters. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin/Heidelberg, pp 452–459CrossRefGoogle Scholar
  92. Williams TD (1995) Bird families of the world. The penguins. Oxford University Press, New YorkGoogle Scholar
  93. Wohlschlag DE (1960) Metabolism of an Antarctic fish and the phenomenon of cold adaptation. Ecology 41:287–292CrossRefGoogle Scholar
  94. Wohlschlag DE (1963) An Antarctic fish with unusually low metabolism. Ecology 44:557–564CrossRefGoogle Scholar
  95. Wohlschlag DE (1964) Respiratory metabolism and ecological characteristics of some fishes in McMurdo sound, Antarctica. In: Lee MO (ed) Biology of the Antarctic seas. American Geophysical Union, Washington, DC, pp 33–62Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Natural and Environmental ResourcesGuánica Biosphere ReserveGuánicaUSA
  2. 2.College of Marine ScienceUniversity of South FloridaSaint PetersburgUSA

Personalised recommendations