Advertisement

Born among the ice: first morphological observations on two developmental stages of the Antarctic silverfish Pleuragramma antarcticum, a key species of the Southern Ocean

  • Massimiliano Bottaro
  • Diana Oliveri
  • Laura Ghigliotti
  • Eva Pisano
  • Sara Ferrando
  • Marino Vacchi
Research Paper

Abstract

The Antarctic silverfish Pleuragramma antarcticum is a keystone species in the Southern Ocean ecosystem, providing one of the major links between lower and higher trophic levels. Despite the importance of this species, surprisingly little is known of its early development. The first spawning area for the silverfish has been recently identified in the near-shore of Terra Nova Bay (Ross Sea). Evidence indicates that spawning and embryo development occurs in the cryopelagic environment, below the seasonal pack-ice. In order to contribute to the knowledge of the life cycle of this very important Antarctic species, we carried out the first histological characterization on pre-hatching embryos and newly hatched larvae. Embryonated eggs and larvae of P. antarcticum were collected between late October and November 2005 at TNB through holes drilled into the sea ice. Embryonic stage just before hatching and the first post-hatching stage were the most abundant within our samples and thus were analysed using both macroscopic and histological approaches. Early life stages of the Antarctic silverfish revealed interesting features: the sensory system, foraging apparatus and heart appeared well developed, whereas the liver and gills were underdeveloped. Morphological details of the organogenesis were performed, providing the first substantial information on the development of P. antarcticum and representing a further steps towards the knowledge of the life cycle of this important Antarctic key species.

Keywords

Antarctic waters Development Morphology Pleuragramma antarcticum Sea-ice 

Notes

Acknowledgments

This work was financially supported by the PNRA (Italian National Antarctic Research Program). We are grateful to Federico Mazzei (DIBIO, University of Genoa), Clive W. Evans, John A. Macdonald, Mike Taler (School of Biological Sciences, University of Auckland, NZ) and Arthur L. DeVries (Department of Animal Biology, University of Illinois at Urbana-Champaign, USA) for their work and invaluable collaboration in all the activities at Terra Nova Bay. We acknowledgment also Mario Pestarino (DIBIO, University of Genoa) for his comments. Special thanks to Carla J. L. Atkinson (School of Biomedical Sciences, University of Queensland, Australia) and Grazia Tagliafierro (DIBIO, University of Genoa) for their readily available help and suggestions during this study. We are also grateful to an anonymous reviewer who greatly improved our work. Experiments should be carried out in accordance with the European Communities Council Directive of 24 November 1986 (86/609/EEC).

References

  1. Alami-Durante H, Bergot P, Rouel M, Goldspink G (2000) Effects of environmental temperature on the development of the myotomal white muscle in larval carp (Cyprinus carpio L.). J Exp Biol 203:3675–3688PubMedGoogle Scholar
  2. Alami-Durante H, Rouel M, Kentouri M (2006) New insights into temperature-induced white muscle growth plasticity during Dicentrarchus labrax early life: a developmental and allometric study. Mar Biol (Berl) 149:1551–1565. doi: 10.1007/s00227-006-0304-6 CrossRefGoogle Scholar
  3. Bang PI, Sewell WF, Malicki JJ (2001) Morphology and cell type heterogeneities of the inner ear epithelia in adult and juvenile zebrafish (Danio rerio). J Comp Neurol 438:173–190. doi: 10.1002/cne.1308 PubMedCrossRefGoogle Scholar
  4. Blaxter JHS (1986) Development of sense organs and behaviour of teleost larvae with special reference to feeding and predator avoidance. Trans Am Fish Soc 115:98–114. doi: 10.1577/1548-8659(1986)115<98:NLFCDO>2.0.CO;2 CrossRefGoogle Scholar
  5. Blaxter JHS, Fuiman LA (1989) Function of the free neuromasts of marine teleost larvae. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line: neurobiology and evolution. Springer-Verlag, New York, pp 481–499Google Scholar
  6. Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an Antarctic fish: on ice for winter. PLoS ONE 3(3):e1743PubMedCrossRefGoogle Scholar
  7. Cziko PA, Evans CW, Cheng C-HC, DeVries AL (2006) Freezing resistance of antifreeze-deficient larval Antarctic fish. J Exp Biol 209:407–420. doi: 10.1242/jeb.02008 PubMedCrossRefGoogle Scholar
  8. DeVries AL, Eastman JT (1978) Lipid sacs as a buoyancy adaptation in an Antarctic fish. Nature 271:352–353. doi: 10.1038/271352a0 CrossRefGoogle Scholar
  9. DeWitt HH (1970) The character of the midwater fish fauna of the Ross Sea, Antarctica. In: Holdgate MW (ed) Antarctic ecology, vol 2. Academic Press, London, pp 305–315Google Scholar
  10. Diaz JP, Prié-Granié M, Kentouri M, Varsamos S, Connes R (2003) Development of the lateral line system in the sea bass. J Fish Biol 62:24–40. doi: 10.1046/j.1095-8649.2003.00004.x CrossRefGoogle Scholar
  11. Eastman JT (1985a) The evolution of neutrally buoyant notothenioid fishes: their specializations and potential interactions in the Antarctic marine food web. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin Heidelberg New York, pp 430–436Google Scholar
  12. Eastman JT (1985b) Pleuragramma antarcticum (Pisces, Nototheniidae) as food for other fishes in McMurdo Sound, Antarctica. Polar Biol 4:155–160. doi: 10.1007/BF00263878 CrossRefGoogle Scholar
  13. Eastman JT (1988) Ocular morphology in antarctic notothenioid fishes. J Morphol 196:283–306. doi: 10.1002/jmor.1051960303 CrossRefGoogle Scholar
  14. Eastman JT (1997) Phyletic divergence and specialization for pelagic life in the Antarctic notothenioid fish Pleuragramma antarcticum. Comp Biochem Physiol A 118:1095–1101. doi: 10.1016/S0300-9629(97)86798-9 CrossRefGoogle Scholar
  15. Eastman JT, DeVries AL (1989) Ultrastructure of the lipid sac wall in the Antarctic notothenioid fish Pleuragramma antarcticum. Polar Biol 9:333–335. doi: 10.1007/BF00287433 CrossRefGoogle Scholar
  16. Eastman JT, DeVries AL (1997) Morphology of the digestive system of Antarctic nototheniid fishes. Polar Biol 17:1–13. doi: 10.1007/s003000050098 CrossRefGoogle Scholar
  17. Efremenko VN (1983) Illustrated guide to fish larvae of the Southern Ocean. Cybium 7:1–74Google Scholar
  18. Falk-Petersen IB (2005) Comparative organ differentiation during early life stages of marine fish. Fish Shellfish Immunol 19:397–412. doi: 10.1016/j.fsi.2005.03.006 PubMedCrossRefGoogle Scholar
  19. Falk-Petersen IB, Hansen TK (2003) Early ontogeny of the spotted wolffish (Anarhichas minor Olafsen). Aquacult Res 34:1059–1067. doi: 10.1046/j.1365-2109.2003.00910.x CrossRefGoogle Scholar
  20. Feller G, Goessens G, Gerday C, Bassleer R (1985) Heart structure and ventricular ultrastructure of hemoglobin and myoglobin-free icefish Channichthys rhinoceratus. Cell Tissue Res 242:669–676. doi: 10.1007/BF00225436 PubMedCrossRefGoogle Scholar
  21. Franklin CE, Axelsson M, Davison W (2001) Constancy and control of heart rate during an increase in temperature in the Antarctic fish Pagothenia borchgrevinki. Exp Biol Online 6:1–8. doi: 10.1007/s00898-001-0001-3 CrossRefGoogle Scholar
  22. Fuiman LA (2002) Special considerations of fish eggs and larvae. In: Fuiman LA, Werner RG (eds) The unique contributions of early life stages. Blackwell Publishing Ltd, Oxford, UK, pp 1–32Google Scholar
  23. Granata A, Cubeta A, Guglielmo L, Sidoti O, Greco S, Vacchi M, La Mesa M (2002) Ichthyoplankton abundance and distribution in the Ross Sea during 1987–1996. Polar Biol 25:187–202Google Scholar
  24. Grøntvedt RN, Espelid S (2003) Immunoglobulin producing cells in the spotted wolffish (Anarhichas minor Olafsen): localisation in adults and during juvenile development. Dev Comp Immunol 27:569–578. doi: 10.1016/S0145-305X(03)00028-4 PubMedCrossRefGoogle Scholar
  25. Guglielmo L, Granata A, Greco S (1998) Distribution and abundance of postlarval and juvenile Pleuragramma antarcticum (Pisces, Nototheniidae) off Terra Nova Bay (Ross Sea, Antarctica). Polar Biol 19:37–51. doi: 10.1007/s003000050214 CrossRefGoogle Scholar
  26. Haddon C, Lewis J (1996) Early ear development in the embryo of the zebrafish, Danio rerio. J Comp Neurol 365:113–128. doi: 10.1002/(SICI)1096-9861(19960129)365:1&lt;113::AID-CNE9&gt;3.0.CO;2-6 PubMedCrossRefGoogle Scholar
  27. Hall TE, Johnston IA (2003) Temperature and developmental plasticity during embryogenesis in the Atlantic cod Gadus morhua L. Mar Biol (Berl) 142:833–840Google Scholar
  28. Harrison P, Zummo G, Farina F, Tota B, Johnston IA (1991) Gross anatomy, myoarchitecture, and ultrastructure of the heart ventricle in the haemoglobinless icefish Chaenocephalus aceratus. Can J Zool 69:1339–1347. doi: 10.1139/z91-189 CrossRefGoogle Scholar
  29. Harvey R, Blaxter JHS, Hoyt RD (1992) Development of superficial and lateral line neuromasts in larvae and juveniles of plaice (Pleuronectes platessa). and sole (Solea solea). J Mar Biol Assoc UK 72:651–668CrossRefGoogle Scholar
  30. Hubold G, Ekau W (1987) Midwater fish fauna of the Weddell Sea, Antarctica. In: Kullander SO, Fernholm B (eds) Proceedings of the fifth congress of the European Ichthyological Society. Swedish Museum of Natural History, Stockholm, pp 391–396Google Scholar
  31. Johnston IA (1999) Muscle development and growth: potential implications for flesh quality in fish. Aquaculture 177:99–115. doi: 10.1016/S0044-8486(99)00072-1 CrossRefGoogle Scholar
  32. Johnston IA, Hall TE (2004) Mechanisms of muscle development and responses to temperature change in fish larvae. Am Fish Soc Symp 40:85–116Google Scholar
  33. Johnston IA, Camm JP, White MG (1988) Specializations of swimming muscles in the pelagic Antarctic fish Pleuragramma antarcticum. Mar Biol (Berl) 100:3–12. doi: 10.1007/BF00392949 CrossRefGoogle Scholar
  34. Johnston IA, Strugnell G, McCracken ML, Johnstone R (1999) Muscle growth and development in normal-sex-ratio and all-female diploid and triploid Atlantic salmon. J Exp Biol 202:1991–2016PubMedGoogle Scholar
  35. Kellermann A (1990) Catalogue of early life stages of Antarctic notothenioid fishes. Ber Polarforsch 67:45–136Google Scholar
  36. Kelsh RN (2004) Genetics and evolution of pigment patterns in fish. Pigment Cell Res 17:326–336. doi: 10.1111/j.1600-0749.2004.00174.x PubMedCrossRefGoogle Scholar
  37. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310PubMedGoogle Scholar
  38. Kjørsvik E, Reiersen AL (1992) Histomorphology of the early yolk-sac larvae of the Atlantic halibut (Hippoglossus hippoglossus L.): an indication of the timing of functionality. J Fish Biol 41:1–19. doi: 10.1111/j.1095-8649.1992.tb03166.x CrossRefGoogle Scholar
  39. Kjørsvik E, Pittman K, Pavlov D (2004) From fertilization to the end of metamorphosis-functional development. In: Moksness E, Kjørsvik E, Olsen YA (eds) Culture of cold-water marine fish. Blackwell Publishing Ltd, Oxford, pp 204–269CrossRefGoogle Scholar
  40. Koubbi P, Vallet C, Razouls S, Grioche A, Hilde D, Courcot L, Janquin MA, Vacchi M, Hureau JC (2007) Condition and diet of larval Pleuragramma antarcticum (Nototheniidae) from Terre Adélie (Antarctica) during summer. Cybium 31:67–76Google Scholar
  41. La Mesa M, Eastman JT, Vacchi M (2004) The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol 27:321–338. doi: 10.1007/s00300-004-0599-z CrossRefGoogle Scholar
  42. Maes J, Van de Putte A, Hecq JH, Volckaert FAM (2006) State-dependent energy allocation in the pelagic Antarctic silverfish Pleuragramma antarcticum: trade-off between winter reserves and buoyancy. Mar Ecol Prog Ser 326:269–282. doi: 10.3354/meps326269 CrossRefGoogle Scholar
  43. Montgomery JC, Sutherland KBW (1997) Sensory development of the Antarctic silverfish Pleuragramma antarcticum: a test for the ontogenetic shift hypothesis. Polar Biol 18:112–115. doi: 10.1007/s003000050165 CrossRefGoogle Scholar
  44. Morales-Nin B, Garcia MA, Lopez O (1998) Distribution of larval and juvenile Nototheniops larseni and Pleuragramma antarcticum off the Antarctic Peninsula in relation to oceanographic conditions. Cybium 22:69–81Google Scholar
  45. Morrison M (1993) Histology of the Atlantic cod, Gadus morhua: an atlas. Part 4. Eleutheroembryo and larva. Can Spec Publ Fish Aquat Sci 119C:496Google Scholar
  46. Mukai Y (2006) Role of free neuromasts in larval feeding of willow shiner Gnathopogon elongatus caerulescenes Teleostei, Cyprinidae. Fish Sci 72:705–709. doi: 10.1111/j.1444-2906.2006.01207.x CrossRefGoogle Scholar
  47. Mukai Y, Yoshikawa H, Kobayashi H (1994) The relationship between the length of the cupulae of free neuromasts and feeding ability in larvae of the willow shiner Gnathopogon elongates caerulescens (Teleostei, Cyprinidae). J Exp Biol 197:399–403PubMedGoogle Scholar
  48. Mukai Y, Chai LL, Shaleh SRM, Senoo S (2007) Structure and Development of Free Neuromasts in Barramundi, Lates calcarifer (Block). Zoolog Sci 24:829–835. doi: 10.2108/zsj.24.829 PubMedCrossRefGoogle Scholar
  49. North AW, Kellermann A (1990) Key to the early stages of Antarctic fish. Ber Polarforsch 67:1–44Google Scholar
  50. Otsuka M (2003) Neuromast formation in the prehatching embryos of the Japanese flounder (Paralichthys olivaceus). Acta Zool 84:99–106. doi: 10.1046/j.1463-6395.2003.00134.x CrossRefGoogle Scholar
  51. Pankhurst NW, Montgomery JC (1990) Ontogeny of vision in the Antarctic fish Pagothenia borchgrevinki (Nototheniidae). Polar Biol 10:419–422Google Scholar
  52. Pellegrino D, Acierno R, Tota B (2003) Control of cardiovascular function in icefish Chionodraco hamatus: involvement of serotonin and nitric oxide. Comp Biochem Physiol A 134:471–480. doi: 10.1016/S1095-6433(02)00324-0 CrossRefGoogle Scholar
  53. Radtke RL, Hubold G, Folsom SD, Lenz PH (1993) Otolith structural and chemical analyses: the key to resolving age and growth of the Antarctic silverfish, Pleuragramma antarcticum. Antarct Sci 5:51–62. doi: 10.1017/S0954102093000082 CrossRefGoogle Scholar
  54. Regan CT (1916) Larval and postlarval fishes. British Antarctic (“Terra Nova”) Expedition 1910. Nat Hist Rep Zool 1:125–156Google Scholar
  55. Regoli F, Nigro M, Benedetti M, Fattorini D, Gorbi F (2005) Antioxidant efficiency in early life stages of the Antarctic silverfish, Pleuragramma antarcticum: responsiveness to pro-oxidant conditions of platelet ice and chemical exposure. Aquat Toxicol 75:43–52. doi: 10.1016/j.aquatox.2005.07.003 PubMedCrossRefGoogle Scholar
  56. Rowlerson A, Mascarello F, Radaelli G, Veggetti A (1995) Differentiation and growth of muscle in fish Sparus aurata (L.): II. Hyperplastic and hypertrophic growth of lateral muscle from hatching to adult. J Muscle Res Cell Motil 16:223–236. doi: 10.1007/BF00121131 PubMedCrossRefGoogle Scholar
  57. Tagliafierro G, Carlini M, Faraldi G, Gallus L (1998) The neuroendocrine system in the intestinal tract and pancreas of Antarctic fish. In: di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica. Springer, Milan, pp 247–256Google Scholar
  58. Tagliafierro G, Bruzzone F, Gallus L (2003) Morphophysiological adaptations in the digestive system of Antarctic Notothenioid fishes. In: Val AL, Kapoor BG (eds) Fish Adaptations. Science Publ, Enfield, pp 97–112Google Scholar
  59. Temple GK, Cole NJ, Johnston IA (2001) Embryonic temperature and the relative timing of muscle-specific genes during development in herring (Clupea harengus L.). J Exp Biol 204:3629–3637PubMedGoogle Scholar
  60. Tota B, Cerra MC, Mazza R, Pellegrino D, Icardo J (1997) The heart of Antarctic icefish as a paradigm of cold adaptation. J Therm Biol 22:409–417. doi: 10.1016/S0306-4565(97)00060-0 CrossRefGoogle Scholar
  61. Tytler P, Blaxter JHS (1988) Drinking in yolk-sac stage larvae of the halibut, Hippoglossus hippoglossus (L.). J Fish Biol 32:493–494. doi: 10.1111/j.1095-8649.1988.tb05388.x CrossRefGoogle Scholar
  62. Vacchi M, La Mesa M, Greco S (1999) Summer distribution and abundance of larval and juvenile fishes in the western Ross Sea. Antarct Sci 11:54–60. doi: 10.1017/S0954102099000085 CrossRefGoogle Scholar
  63. Vacchi M, La Mesa M, Dalù M, MacDonald J (2004) Early life stages in the life cycle of Antarctic silverfish, Pleuragramma antarcticum in Terra Nova Bay, Ross Sea. Antarct Sci 16:299–305. doi: 10.1017/S0954102004002135 CrossRefGoogle Scholar
  64. Van Raamsdonk W, Van der Stelt A, Diegenbach PC, Van de Berg W, De Bruyn H, Van Dijk J, Mijzen P (1974) Differentiation of the musculature of the teleost Brachydanio rerio. I. Myotome shape and movements in the embryo. Z Anat Entwickl-Gesch 145:321–342. doi: 10.1007/BF00519641 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Massimiliano Bottaro
    • 1
  • Diana Oliveri
    • 2
  • Laura Ghigliotti
    • 2
  • Eva Pisano
    • 2
  • Sara Ferrando
    • 2
  • Marino Vacchi
    • 1
  1. 1.ICRAM, c/o Museo Nazionale dell’Antartide (MNA)Università di GenovaGenoaItaly
  2. 2.Dipartimento di BiologiaUniversità di GenovaGenoaItaly

Personalised recommendations