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Early otolith development in the critically endangered tooth-carp, Aphanius farsicus (Teleostei: Cyprinodontidae)

  • Nafiseh Sanjarani Vahed
  • Hamid Reza Esmaeili
  • Mojtaba Masoudi
  • Bettina Reichenbacher
Article

Abstract

Otolith morphology in the tooth-carp/killifish genus Aphanius is a source of informative taxonomic characters at both the species and population level. Most work on otoliths has focused on adult specimens, while evidence of ontogenetic variation is rarely provided. In this study we describe the development of otolith morphology during the early life stages of an endangered and endemic species, the Fars tooth-carp Aphanius farsicus from southern Iran. The study material comprises 34 larvae and early juveniles representing nine different developmental stages (0–120 days post hatching), all reared under the same laboratory conditions. The results reveal (i) a significant correlation between standard length and otolith size (length) in larval and early juvenile stages, (ii) clear differences in otolith morphology between larvae/early juveniles and adults, and (iii) a temporal link between the appearance of the sulcus on the otolith’s inner face and the emergence of the dorsal and anal fins. Our results indicate that otoliths of Aphanius can be recognized as originating from larval or early juvenile fish based on their short rostrum and antirostrum lengths and wide excisura, in addition to their small size. These immature otoliths are, however, not diagnostic at the species level in A. farsicus, nor most probably in other species of tooth-carp. The outcome of our study is also of interest to palaeontologists working with fossil killifish otoliths, as it can help avoid misinterpretation of ancient species diversity.

Keywords

Killifish Cyprinodontiformes Otolith Ontogeny Taxonomy 

Notes

Acknowledgements

The research was funded by Shiraz University and was approved by the Ethics Committee of the Biology Department (SU- 9431436). We are grateful to the editor and reviewers for their constructive comments which improved our manuscript.

References

  1. Aguirre WE (2003) Allometric growth of the sulcus in Cynoscion spp. (Sciaenidae). J Fish Biol 63:1341–1346.  https://doi.org/10.1046/j.1095-8649.2003.00238.x CrossRefGoogle Scholar
  2. Annabi A, Said K, Reichenbacher B (2013) Inter-population differences in otolith morphology are genetically encoded in the killifish Aphanius fasciatus (Cyprinodontiformes). Sci Mar 77:269–279.  https://doi.org/10.3989/scimar.03763.02A CrossRefGoogle Scholar
  3. Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014–1032.  https://doi.org/10.1139/f85-127 CrossRefGoogle Scholar
  4. Capoccioni F, Costa C, Aguzzi J, Menesatti P, Lombarte A, Ciccotti E (2011) Ontogenetic and environmental effects on otolith shape variability in three Mediterranean European eel (Anguilla anguilla, L.) local stocks. J Exp Mar Biol Ecol 397:1–7.  https://doi.org/10.1016/j.jembe.2010.11.011 CrossRefGoogle Scholar
  5. Chancollon O, Pusineri C, Ridoux V (2006) Food and feeding ecology of Northeast Atlantic swordfish (Xiphias gladius) off the Bay of Biscay. ICES J Mar Sci 63:1075–1085.  https://doi.org/10.1016/j.icesjms.2006.03.013 Google Scholar
  6. de Carvalho BM, Vaz-dos-Santos AM, Spach HL, Volpedo AV (2015) Ontogenetic development of the sagittal otolith of the anchovy, Anchoa tricolor, in a subtropical estuary. Sci Mar 79:409–418.  https://doi.org/10.3989/scimar.04218.31A CrossRefGoogle Scholar
  7. Doadrio I, Carmona JA, Fernandez-Delgado C (2002) Morphometric study of the Iberian Aphanius (Actinopterygii, Cyprinodontiformes), with description of a new species. Folia Zool 51:67–79Google Scholar
  8. Esmaeili HR, Teimori A, Gholami Z, Reichenbacher B (2014a) Two new species of the tooth-carp Aphanius (Teleostei: Cyprinodontidae) and the evolutionary history of the Iranian inland and inland-related Aphanius species. Zootaxa 3786:246–268.  https://doi.org/10.11646/zootaxa.3786.3.2 CrossRefPubMedGoogle Scholar
  9. Esmaeili HR, Teimori A, Sayyadzadeh G, Masoudi M, Reichenbacher B (2014b) Phylogenetic relationships of the tooth-carp Aphanius (Teleostei: Cyprinodontidae) in the river systems of southern and south-western Iran based on mtDNA sequences. Zool Middle East 60:29–38.  https://doi.org/10.1080/09397140.2014.892329 CrossRefGoogle Scholar
  10. Ferrito V, Pappalardo AM, Canapa A, Barucca M, Doadrio I, Olmo E, Tigano C (2013) Mitochondrial phylogeography of the killifish Aphanius fasciatus (Teleostei, Cyprinodontidae) reveals highly divergent Mediterranean populations. Mar Biol 160:3193–3208.  https://doi.org/10.1007/s00227-013-2307-4 CrossRefGoogle Scholar
  11. Gholami Z, Esmaeili HR, Erpenbeck D, Reichenbacher B (2015a) Genetic connectivity and phenotypic plasticity in the cyprinodont Aphanius farsicus from the Maharlu Basin, south-western Iran. J Fish Biol.  https://doi.org/10.1111/jfb.12599
  12. Gholami Z, Esmaeili HR, Reichenbacher B (2015b) New data on the zoogeography of Aphanius sophiae (Teleostei: Cyprinodontidae) in the Central Zagros (Southwest Iran). Limnologica 51:70–82.  https://doi.org/10.1016/j.limno.2014.12.002 CrossRefGoogle Scholar
  13. Gierl C, Reichenbacher B, Gaudant J, Erpenbeck D, Pharisat A (2013) An extraordinary gobioid fish fossil from southern France. PLoS One 8:e64117.  https://doi.org/10.1371/journal.pone.0064117 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Green BS et al. (2009) Tropical Fish Otoliths: Information for Assessment, Management and Ecology. In: Tropical Fish Otoliths: Information for Assessment, Management and Ecology, vol 11. Reviews-Methods and Technologies in Fish Biology and FisheriesGoogle Scholar
  15. Hermann TW, Stewart DJ, Limburg KE, Castello L (2016) Unravelling the life history of Amazonian fishes through otolith microchemistry. R Soc Open Sci 3.  https://doi.org/10.1098/rsos.160206
  16. Hrbek T, Keivany Y, Coad BW (2006) New species of Aphanius (Teleostei, Cyprinodontidae) from Isfahan Province of Iran and a reanalysis of other Iranian species. Copeia 2006:244–255CrossRefGoogle Scholar
  17. Hüssy K (2008) Otolith shape in juvenile cod (Gadus morhua): Ontogenetic and environmental effects. J Exp Mar Biol Ecol 364:35–41.  https://doi.org/10.1016/j.jembe.2008.06.026 CrossRefGoogle Scholar
  18. Jaramillo AM, Tombari AD, Dura VB, Rodrigo ME, Volpedo AV (2014) Otolith eco-morphological patterns of benthic fishes from the coast of Valencia (Spain). Thalassas 30:57–66Google Scholar
  19. Kumar P, Chakraborty SK, Jaiswar AK (2012) Comparative otolith morphology of sciaenids occurring along the north-west coast of India. Indian J Fish 59:19–27Google Scholar
  20. Lombarte A, Lleonart J (1993) Otolith size changes related with body growth, habitat depth and temperature. Environ Biol Fish 37:297–306.  https://doi.org/10.1007/bf00004637 CrossRefGoogle Scholar
  21. Lombarte A, Torres GJ, Morales-Nin B (2003) Specific Merluccius otolith growth patterns related to phylogenetics and environmental factors. J Mar Biol Assoc U K 83:277–281.  https://doi.org/10.1017/S0025315403007070h CrossRefGoogle Scholar
  22. Lord C, Morat F, Lecomte-Finiger R, Keith P (2012) Otolith shape analysis for three Sicyopterus (Teleostei: Gobioidei: Sicydiinae) species from New Caledonia and Vanuatu. Environ Biol Fish 93:209–222.  https://doi.org/10.1007/s10641-011-9907-y CrossRefGoogle Scholar
  23. Lychakov DV, Rebane YT (2000) Otolith regularities. Hear Res 143:83–102.  https://doi.org/10.1016/s0378-5955(00)00026-5 CrossRefPubMedGoogle Scholar
  24. Masoudi M et al (2016) Sympatry and possible hybridization among species of the killifish genus Aphanius Nardo, 1827 (Teleostei: Cyprinodontidae) in Southwestern Iran. Limnologica 59:10–20.  https://doi.org/10.1016/j.limno.2016.02.008 CrossRefGoogle Scholar
  25. Monteiro LR, Di Beneditto APM, Guillermo LH, Rivera LA (2005) Allometric changes and shape differentiation of sagitta otoliths in sciaenid fishes. Fish Res 74:288–299.  https://doi.org/10.1016/j.fishres.2005.03.002 CrossRefGoogle Scholar
  26. Morales-Nin B (2000) Review of the growth regulation processes of otolith daily increment formation. Fish Res 46:53–67.  https://doi.org/10.1016/s0165-7836(00)00133-8 CrossRefGoogle Scholar
  27. Nolf D (1985) Handbook of paleoichthyology, Volume 10, Otolithi piscium. vol 10. Handbook of Paleoichthyology, vol 10. Verlag Dr. Friedrich Pfeil, MünchenGoogle Scholar
  28. Nolf D (1993) A survey of perciform otoliths and their interest for phylogenetic analysis, with an iconographic synopsis of the Percoidei. B Mar Sci 52:220–239Google Scholar
  29. Nolf D (2013) The diversity of fish otoliths, past and present. Royal Belgian Institute of Natural Sciences, BrusselsGoogle Scholar
  30. Popper AN, Lu Z (2000) Structure–function relationships in fish otolith organs. Fish Res 46:15–25.  https://doi.org/10.1016/S0165-7836(00)00129-6 CrossRefGoogle Scholar
  31. Rasband WS (1997–2016) ImageJ, 1.49v edn. U.S. National Institutes of Health, Bethesda, Maryland, U.S.A.Google Scholar
  32. Rehberg-Haas S, Hammer C, Hillgruber N, Hussy K, Temming A (2012) Otolith microstructure analysis to resolve seasonal patterns of hatching and settlement in western Baltic cod. ICES J Mar Sci 69:1347–1356.  https://doi.org/10.1093/icesjms/fss112 CrossRefGoogle Scholar
  33. Reichenbacher B, Sienknecht U, Küchenhoff H, Fenske N (2007) Combined otolith morphology and morphometry for assessing taxonomy and diversity in fossil and extant killifish (Aphanius, †Prolebias). J Morphol 268:898–915.  https://doi.org/10.1002/jmor.10561 CrossRefPubMedGoogle Scholar
  34. Reichenbacher B, Kamrani E, Esmaeili HR, Teimori A (2009a) The endangered cyprinodont Aphanius ginaonis (Holly, 1929) from southern Iran is a valid species: evidence from otolith morphology. Environ Biol Fish 86:507–521.  https://doi.org/10.1007/s10641-009-9549-5 CrossRefGoogle Scholar
  35. Reichenbacher B, Feulner GR, Schulz-Mirbach T (2009b) Geographic variation in otolith morphology among freshwater populations of Aphanius dispar (Teleostei, Cyprinodontiformes) from the southeastern Arabian Peninsula. J Morphol 270:469–484.  https://doi.org/10.1002/jmor.10702 CrossRefPubMedGoogle Scholar
  36. Sanjarani Vahed N, Esmaeili HR, Masoudi M, Ebrahimi M (2017) Towards the conservation of a critically endangered species, Aphanius farsicus: embryogenesis and development. Environ Biol Fish online first doi: https://doi.org/10.1007/s10641-017-0691-1
  37. Schulz-Mirbach T, Heß M, Plath M (2011) Inner ear morphology in the Atlantic molly Poecilia mexicana—first detailed microanatomical study of the inner ear of a cyprinodontiform species. PLoS One 6:e27734.  https://doi.org/10.1371/journal.pone.0027734 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Teimori A, Esmaeili HR, Reichenbacher B (2011) Aphanius farsicus, a replacement name for A. persicus (Jenkins, 1910) (Teleostei, Cyprinodontidae). Zootaxa:53–58Google Scholar
  39. Teimori A, Jawad LAJ, Al-Kharusi LH, Al-Mamry JM, Reichenbacher B (2012a) Late Pleistocene to Holocene diversification and historical zoogeography of the Arabian killifish (Aphanius dispar) inferred from otolith morphology. Sci Mar 76:637–645.  https://doi.org/10.3989/scimar.03635.26C Google Scholar
  40. Teimori A, Schulz-Mirbach T, Esmaeili HR, Reichenbacher B (2012b) Geographical differentiation of Aphanius dispar (Teleostei: Cyprinodontidae) from Southern Iran. J Zool Syst Evol Res 50:289–304.  https://doi.org/10.1111/j.1439-0469.2012.00667.x CrossRefGoogle Scholar
  41. Tigano C et al (2006) A study of osteological and molecular differences in populations of Aphanius fasciatus Nardo 1827, from the central Mediterranean (Teleostei, Cyprinodontidae). Mar Biol 149:1539–1550.  https://doi.org/10.1007/s00227-006-0300-x CrossRefGoogle Scholar
  42. Tuset VM, Lombarte A, Assis CA (2008) Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Sci Mar 72:7–198Google Scholar
  43. Tuset VM, Azzurro E, Lombarte A (2012) Identification of Lessepsian fish species using the sagittal otolith. Sci Mar 76:289–299.  https://doi.org/10.3989/scimar.03420.18E CrossRefGoogle Scholar
  44. Volpedo AV, Echeverría DD (1999) Morfología de los otolitos sagittae de juveniles y adultos de Micropogonias furnieri (Demarest, 1823) (Sciaenidae). Thalassas 15:19–24Google Scholar
  45. Volpedo AV, Echeverría 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 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Developmental Biosystematics Research Lab., Zoology Section, Department of Biology, College of SciencesShiraz UniversityShirazIran
  2. 2.Department of Earth and Environmental Sciences, Palaeontology & Geobiology & GeoBio–CenterLudwig-Maximilians-University (LMU)MunichGermany

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