Ocean and Polar Research

Korea Institute of Ocean Science & Technology (한국해양과학기술원)
권호 표지
DOI QR코드

DOI QR Code

Otolith Microstructural Organization in the South Georgia Icefish Pseudochaenichthys georgianus (Channichthyide) and Cautious Considerations on How Otoliths Can Provide Clues on a Species' Distribution and Migration in Antarctic Waters

  • Received : 2021.12.01
  • Accepted : 2022.01.24
  • Published : 2022.03.30
Download PDF
⟨ Previous Next ⟩

Abstract

How in the Antarctic icefish, generally, and Pseudochaenichthys georgianus, in particular, otoliths increase in size and build new material as the fish ages and passes through different life phases is largely unexplored. Morphometric details of 3418 otoliths of Ps. georgianus from S. Georgia and 318 from S. Shetland, were processed and proportions of the amounts of collagen and aragonite removed by EDTA were determined for different age groups. Microstructural investigations showed that characteristics of the 3-dimensinal collagen net are the reason for the radial direction and orientation of the aragonite needles of approximately 1.0 ㎛ in length in larval and 2.3 ㎛ in length in adult specimens. Earlier generated increment layers from the primordial centre (PC) in the dorsal direction restrict those of the secondary centre (SC), causing new growth layer accretion in different directions. In the otoliths of larval Ps. georgianus, aragonite layers are 0.89 ㎛ wide while in juveniles and adults they measure 1.45-2.86 ㎛. Otoliths change from a sphere shape in the larvae to a longish object of irregular outline in the older stages. It is tentaively suggested that the observed otolith shape differences at distinct growth stages are due to physical effects related to swimming speeds at particular water depths and locations. To confirm that otoliths, apart from being useful for age analyses, could also serve to establish correlations between developmental stage and the oceanic environment the fish spend time in, further analyses using additional species and state-of-the-art methods like µCT imaging to evaluate otolith volumes and shapes are required.

Keywords

Acknowledgement

We thank all those that were involved with the collection of the material, and all who offered help and advice throughout this study. RT in particular further gratefully acknowledges the support received from the Sea Fisheries Institute, Imperial College, University of London, the British Antarctic Survey and the University of Gdańsk. For their hospitality during a brief visit in the Austral summer of the year 2000, VBM-R thanks the staff of Poland's Antarctic Arctowski Base and acknowledges the support received from Professor Chuleui Jung via the Basic Science Research Program of the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2018R1A6A1A03024862) to complete this study.

References

  1. Agnew DJ, Gutierrez NL, Stern-Pirlot A, Hoggarth DD, (2017) The MSC experience: developing an operational certification standard and a market incentive to improvefishery sustainability. J Mar Sci 71:216-225
  2. Anonymous (1991) Stratgraphics version 5. Reference manual. STSC, Inc., Rockville, 555 p
  3. Bargagli R, Agnorelli C, Borghini F, Monaci F (2005) Enhanced deposition and bioaccumulation of mercury in Antarctic terrestrial ecosystems facing a coastal polynya. Environ Sci Technol 39(21):8150-8155. doi:10.1021/es0507315
  4. Borghesi N, Corsolini S, Leonards P, Brandsma S, de BoerJ, Focardi S (2009) Polybrominated diphenyl ether contamination levels in fish from the Antarctic and the Mediterranean Sea. Chemosphere 77(5):693-698 https://doi.org/10.1016/j.chemosphere.2009.07.035
  5. Braun CB, Sand O (2013) Functional overlap and nonoverlap between lateral line and auditory systems. In: Coombs C, Bleckmann H, Fay RR, Popper AN (eds) The lateral line system. Springer-Verlag, New York, pp 281-312
  6. Bruus H (2012) Acoustofluidics 7: the acoustic radiation force on small particles. Lab Chip 12:1014-1021 https://doi.org/10.1039/c2lc21068a
  7. CCAMLR (2019) CCAMLR Statistical Bulletin, Vol 31. Convention on The Conservation of Antarctic MarineLiving Resources. https://www.ccamlr.org/en/document/data/ccamlrstatistical-bulletin-vol-31 Accessed 29 Aug 2020
  8. Efremenko VN (1983) Atlas of fish larvae of the Southern Ocean. Cybium 7:1-74
  9. Erren T, Koch MS, Meyer-Rochow VB (2013a) Common sense: folk wisdom that ethnobiological and ethnomedical research cannot afford to ignore. J Ethnobiol Ethnomed 2013, 9:80. https://doi.org/10.1186/1746-4269-9-80
  10. Erren T, Zeusz D, Steffany F, Meyer-Rochow VB (2013b) Oceans of plastics. In: Allodi S, Nazari EM (eds) Exploring themes on aquatic toxicology. Research Signpost Publication, Trivandrum, pp 51-74
  11. Florin AB, Hussy K, Blass M, Oesterwind D, Puntila R, Ustups D, Albrecht C, Heimbrand Y, Knospina E, Koszarowski K, Odelstrom A (2018) How old are you - evaluation of age reading methods for the invasive round goby (Neogobius melanostomus, Pallas 1814). J Appl Ichthyol 34:653-658 https://doi.org/10.1111/jai.13596
  12. Gabriel B (1982) Biological scanning electron microscopy. Van Nostrand Reinhold Company, New York, 186 p
  13. Gauldie RW (1988) Function, form and timekeeping properties of fish otoliths. Comp Biochem Phys A 91(2):395-402 https://doi.org/10.1016/0300-9629(88)90436-7
  14. Geissinger HD (1976) Intermicroscopic (LM, SEM, TEM) correlation. In: Hayat MA (ed) Principles and techniques of scanning electron microscopy, Vol 5. Van Nostrand Reinhold, New York, pp 94-121
  15. Hawkins AD, Popper AN (2018) Direcional hering and sound source localization by fishes. J Acoust Soc Am 144(6):3329-3350. doi:10.1121/1.5082306
  16. Hecht T (1987) A guide to the otoliths of Southern Oceanfishes. South African J Antarctic Res 17:1-87
  17. Holcomb M, Cohen AL, Gabitov RI, Hutter JL (2009) Compositional and morphological features of aragonite precipitated experimentally from seawater and biogenically by corals. Geochim Cosmochim Ac 73:4166-4179. doi:10.1016/j.gca.2009.04.015
  18. Horrobin DF (1990) The philosophical basis of peer review and the suppression of innovation. JAMA 263(10):1438-1441 https://doi.org/10.1001/jama.1990.03440100162024
  19. Jolivet A, Bardeau J-F, Fablet R, Paulet Y-M, de Pontual H (2008) Understanding otolith biomineralization process: new insights into microscale spatial distribution of organic and mineral fractions from Raman microspectrometry. Anal Bioanal Chem 392(3):551-560 https://doi.org/10.1007/s00216-008-2273-8
  20. Jolivet A, Fablet R, Bardeau J-F, de Pontual H (2013) Preparation techniques alter the mineral and organic fractions of fish otoliths: insights using Raman micro-spectrometry. Anal Bioanal Chem 405(14):4787-4798 https://doi.org/10.1007/s00216-013-6893-2
  21. Jones CD, Kock K-H, Balguerias E (2000) Changes in biomass of eight species of finfish around the South Orkney Islands (subarea 48.2) from three bottom trawl surveys. CCAMLR Sci 7:53-74
  22. Jones GP, Lukashkina VA, Russell IJ, Lukashkin AN (2010) The Vestibular system mediates sensation of low-frequency sounds in mice. J Assoc Res Oto 11(4):725-732 https://doi.org/10.1007/s10162-010-0230-7
  23. Justice J (2017) Converting chemical signatures in vaterite otoliths to aragonite otoliths in steelhead trout: developing a partition coefficient. https://scholarworks.bgsu.edu/honorsprojects/243 Accessed 12 Mar 2018
  24. Kellermann KA, Gauldie RW, Ruzicka JJ (2002) Otolith microincrements in the Antarctic fishes Notothenia coriiceps and Pseudochaenichthys georgianus. Polar Biol 25:799-807 https://doi.org/10.1007/s00300-002-0432-5
  25. Kock K-H (1989) Results of the CCAMLR Antarctic fish otoliths/scales/bones exchange system. Commission for the Conservation of Antarctic Marine Living Resource, Hobart, pp 197-226
  26. Kock K-H, Kellermann A (1991) Reproduction in Antarctic notothenioid fish. Antarct Sci 3:125-150 https://doi.org/10.1017/s0954102091000172
  27. La Mesa M, De Felice A, Jones CD, Kock KH (2009) Ageand growth of spiny icefish (Chaenodraco wilsoni Regan, 1914) off Joinville-D'Urville Islands (AntarcticPeninsula). CCAMLR Sci 16:115-130
  28. Lacerda ALDF, Rodrigues LDS, van Sebille E, Rodrigues FL, Ribeiro L, Secchi ER, Proietti MC (2019) Plastics in sea surface waters around the Antarctic Peninsula. Sci Rep 9(1):1-12. doi:10.1038/s41598-019-40311-4
  29. Lombarte A, Cruz A (2007) Otolith size trends in marine fish communities from different depth strata. J Fish Biol 71(1):53-76 https://doi.org/10.1111/j.1095-8649.2007.01465.x
  30. Lombarte A, Palmer M, Matallanas J, Goez-Zurita J, MoralesNin B (2010) Ecomorphological trends and phylogenetic inertia of otolith sagittae in Nototheniidae. Environ Biol Fish 89:607-618 https://doi.org/10.1007/s10641-010-9673-2
  31. Lundberg YW, Xu Y, Thiessen KD, Kramer KL (2015) Mechanisms of otoconia and otolith development. Dev Dynam 244(3):239-253 https://doi.org/10.1002/dvdy.24195
  32. Mac Arthur RH (1972) Geographcal ecology: patterns in the distribution of species. Harper and Row, New York, 269 p
  33. Mendoza RPR (2006) Otoliths snd their applicationsin fishery science. Croat J Fish 64(3):89-102
  34. Meyer-Rochow VB (1999) Comming to grips with a slippery issue: human waste disposal in cold climates. Int J Circumpol Heal 58:57-62
  35. Meyer-Rochow VB, Cook I, Hendy CH (1992) How to obtain clues from the otoliths of an adult fish about the aquatic environment it has been in as a larva. Comp Biochem Phys A 103:333-335 https://doi.org/10.1016/0300-9629(92)90590-M
  36. Militelli MI, Macchi GJ, Rodrigues KA (2015) Maturity and fecundity of Champsocephalus gunnari, Chaenocephalus aceratus and Pseudochaenichthys georgianus in South Georgia and Shag Rocks Islands. Polar Sci 9:258-266 https://doi.org/10.1016/j.polar.2015.03.004
  37. Miller JA, Hurst TP (2020) Growth rate, ration, and temperatur effects on otolith elemental incorporation. Front Mar Sci 7:320. doi:10.3389/fmars.2020.00320
  38. Miyazaki T, Iwami T, Meyer-Rochow VB (2011) The position of the retinal area centralis changes with age in Champsocephalus gunnari (Channichthyidae), a predatory fish from coastal Antarctic waters. Polar Biol 34:1117-1123 https://doi.org/10.1007/s00300-011-0969-2
  39. Montgomery JC, Coombs S, Janssen J (1994) Form and function relationships in lateral line systems: comparative data from six species of Antarctic notothenioid fish. Brain Behav Evol 44:299-306 https://doi.org/10.1159/000113591
  40. Montgomery JC, Macdonald JA (1987) Sensory tuning of lateral line receptors in Antarctic fish to the movements of planktonic prey. Science 235:195-196 https://doi.org/10.1126/science.235.4785.195
  41. Montgomery JC, Macdonald JA, Housley GD (1988) Lateral line function in an Antarctic fish related to the signals produced by planktonic prey. J Comp Physiol A 163:827-833 https://doi.org/10.1007/BF00604059
  42. Morris RW, Kittleman LR (1967) Piezoelectric property of otoliths. Science 158(3799):368-370. doi:10.1126/science.158.3799.368
  43. Motta CM, Bice A, Balassone G, Balsamo G, Fascio U, Simoniello P, Tammaro S, Marmo F (2009) Morphological and biochemical analyses of otoliths of the ice-fish Chionodraco hamatus confirm a common origin with redblooded species. J Anat 214(1):153-162. doi:10.1111/j.1469-7580.2008.01003.x
  44. Mucha M (1980) Characteristics of South Georgia icefish (Pseudochaenichthys georgianus, Norman) from the region of South Georgia Island (Antarctic) in the years 1977-1979. Pol Polar Res 1(4):163-172
  45. North AW (1988) Distribution of fish larvae at South Georgia: horizontal, vertical and temporal distribution and early life history relevant to monitoring year-class strength and recruitment. Commission for the Conservation of Antarctic Marine Living Resources, Hobart, pp 105-142
  46. North AW (1990) Ecological studies of Antarctic fish with emphasis on early development of inshore stages at South Georgia. University of Hull, Ph.D. Thesis, pp 1-319
  47. North AW, White MG (1987) Reproductive strategies of Antarctic fish. In: Kullander SO, Fernholm B (eds), Proc Vth Congress of European Ichthyology. Swedish Museum of Natural History, Stockholm, pp 381-390
  48. Parmentier E, Cloots R, Warin R, Henrist C (2007) Otolith crystals (in Carapidae): Growth and habit. J Struct Biol 159:462-473 https://doi.org/10.1016/j.jsb.2007.05.006
  49. Permitin JE (1973) Plodovitost i biologija rozmnozenija belokrovych (sem. Chaenichthyidae), ugretreskovych (sem. Muraenolepidae) i antarkticeskich ploskonosov (sem. Bathydraconidae) moria Skorza (Antarktika). Voprosy Ichtiologii, 13:245-258
  50. Popper AN, Hawkins AD, Sand O, Sisneros JA (2019) Examining the hearing abilities of fishes. J Acoust Soc Am 146(2):948-955 https://doi.org/10.1121/1.5120185
  51. Radtke RL, Hourigan TF (1990) Age and Growth of the Antarctic fish Nototheniops nudifrons. Fish B-NOAA 88(3):557-571
  52. Reid K (2017) Peer-review of fisheries management in the commission for the Conservation of Marine Living Resources (CCAMLR). In: American Fisheries Society 147 Annual Meeting, Tampa, 20-24 Aug 2017, 110 p
  53. Reimer T, Dempster T, Warren-Myers F, Jensen A, Swearer S (2016) High prevalence of vaterite in sagittal otoliths causes hearing impairment in farmed fish. Sci Rep 6:25249. doi:10.1038/srep25249
  54. Salim SA, Thekra LI (2009) Solving linear programming problems by using Exscel's solver. Tikrit J Pure Sci 14:1-12
  55. Schulz-Mirbach T, Ladich F, Plath M, Hess M (2019) Enigmatic ear stones: what we know about the functional role and evolution of fish otoliths. Biol Rev 94:457-482 https://doi.org/10.1111/brv.12463
  56. Sheykholeslami K, Kaga K (2002) The otolithic organ as a receptor of vestibular hearing revealed by vestibular-evoked myogenic potentials in patients with inner ear anomalies. Hearing Res 165(1-2):62-67 https://doi.org/10.1016/S0378-5955(02)00278-2
  57. Sobczak R, Nitkiewicz Z, Koszkul J (2003) Supermolecular structure and thermal properties of polypropylene composites reinforced glass fibre (Struktura nadczasteczkowa i wlasnosci termiczne kompozytow na osnowie polipro pylenu wzmacnianych wloknem szklanym). Kompozyty, 3(8):343-348
  58. Sosinski J, Paciorkowski A (1993) State of mackerel icefish (Champsocephalus gunnari Lonnberg, 1905) stock from South Georgia area based on Polish biological investigationsin 1975-1992. Pol Polar Res, 14:407-431
  59. Thomas ORB, Swearer SE, Kapp EA, Peng P, Tonkin-Hill GQ, Papenfuss A, Roberts A, Bernard P, Roberts BR (2019) The inner ear proteome of fish. FEBS J 286(1):66-81 https://doi.org/10.1111/febs.14715
  60. Tomchik SM, Lu Z (2005) Octavolateral projections andorganization in the medulla of a teleost fish, the sleeper goby (Dormitator latifrons). J Comp Neurol 481(1):96-117. doi: 10.1002/cne.20363
  61. Traczyk R (2015) Age, growth and distribution of thr Antarctic fish Pseudochaenichthys georgianus based on otolith morphometry. Journal of Environmental Science and Engineering B4:53-102
  62. Traczyk R, Meyer-Rochow VB (2019) Age structure and biomass of the icefish Pseudochaenichthys georgianus Norman (Channichthyidae) between 1976 and 2009: a possible link to climate change. Ocean Polar Res 41(4):233-250 https://doi.org/10.4217/OPR.2019.41.4.233
  63. Traczyk R, Meyer-Rochow VB, Hughes RM (2020) Icefish Adaptations to climate change on the South Georgia Island Shelf (Sub-Antarctic). Ocean Sci J 55(2):303-319. doi:10.1007/s12601-019
  64. Traczyk R, Meyer-Rochow VB, Hughes RM (2021) Age determination in the icefish Pseudochaenichthys georgianus (Channichthyidae) based on multiple methods usig otoliths. Aquat Biol 30:1-18 https://doi.org/10.3354/ab00736
  65. Vanella FA, Calvo J, Morriconi E, Aureliano D (2005) Somatic energy content and histological analysis of the gonads in Antarctic fish from the Scotia Arc. Sci Mar 69:305-316 https://doi.org/10.3989/scimar.2005.69s2305
  66. Volpedo AV, Echevarria DD (2003) Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fish Res 60:551-560 https://doi.org/10.1016/S0165-7836(02)00170-4
  67. Volpedo AV, Tombari AD, Echeverria DD (2008) Eco-morphological patterns of the sagitta of Antarctic fish. Polar Biol 31:635-640 https://doi.org/10.1007/s00300-007-0400-1
  68. Whitehouse MJ, Meredith MP, Rothery P, Atkinson A, WardP, Korb RE (2008) Rapid warming of the ocean around South Georgia, Southern Ocean, during the 20th centuary: forcing, characteristics and implications for lower trophic levels. Deep-Sea Res 55(1):1218-1228 https://doi.org/10.1016/j.dsr.2008.06.002
  69. Wroblewski AK (1983) Encyklopedia fizyki wspolczesnej. Published by Panstwowe Wydawnictwo Naukowe. Panstwowe Wydawnictwo Naukowe, Wars zawa, 1007 p
  70. Yang T, Hu L, Xiong X, Petru M, Noman MT, Mishra R, Militky J (2020) Sound absorption properties of natural fibers: a review. Sustainabil 12:8477. doi:10.3390/su12208477
  71. Zabrowski M (2000) The osteology and ossification variability of the skull of antarctic white-blooded fish Chaenodraco wilsoni Regan, 1914 (Channichthyidae, Notothenioidei). Acta Ichthyol Piscat 30(2):111-126 https://doi.org/10.3750/AIP2000.30.2.11
  72. Zhou G-T, Yao Q-Z, Fu SQ, Guan Y-B (2010) Controlled crystallization of unstable vaterite with distinct morphologies and their polymorphic transition to stable calcite. Eur J Mineral 22(2):259-269. doi:10.1127/0935-1221/2009/0022-2008
  73. Zhou Q, Lam KH, Zheng H, Qiu W, Shung KK (2014) Piezoelectric single crystalsfor ultrasonic transducers in biomedical applications. Progress in Materials Science 66:87-111 https://doi.org/10.1016/j.pmatsci.2014.06.001