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.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
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
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
Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014–1032. https://doi.org/10.1139/f85-127
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
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
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
Doadrio I, Carmona JA, Fernandez-Delgado C (2002) Morphometric study of the Iberian Aphanius (Actinopterygii, Cyprinodontiformes), with description of a new species. Folia Zool 51:67–79
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
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
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
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
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
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
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 Fisheries
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
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 2006:244–255
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
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 30:57–66
Kumar P, Chakraborty SK, Jaiswar AK (2012) Comparative otolith morphology of sciaenids occurring along the north-west coast of India. Indian J Fish 59:19–27
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
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
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
Lychakov DV, Rebane YT (2000) Otolith regularities. Hear Res 143:83–102. https://doi.org/10.1016/s0378-5955(00)00026-5
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
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
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
Nolf D (1985) Handbook of paleoichthyology, Volume 10, Otolithi piscium. vol 10. Handbook of Paleoichthyology, vol 10. Verlag Dr. Friedrich Pfeil, München
Nolf D (1993) A survey of perciform otoliths and their interest for phylogenetic analysis, with an iconographic synopsis of the Percoidei. B Mar Sci 52:220–239
Nolf D (2013) The diversity of fish otoliths, past and present. Royal Belgian Institute of Natural Sciences, Brussels
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
Rasband WS (1997–2016) ImageJ, 1.49v edn. U.S. National Institutes of Health, Bethesda, Maryland, U.S.A.
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
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
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
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
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
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
Teimori A, Esmaeili HR, Reichenbacher B (2011) Aphanius farsicus, a replacement name for A. persicus (Jenkins, 1910) (Teleostei, Cyprinodontidae). Zootaxa:53–58
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
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
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
Tuset VM, Lombarte A, Assis CA (2008) Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Sci Mar 72:7–198
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
Volpedo AV, Echeverría DD (1999) Morfología de los otolitos sagittae de juveniles y adultos de Micropogonias furnieri (Demarest, 1823) (Sciaenidae). Thalassas 15:19–24
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
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.
About this article
Cite this article
Vahed, N.S., Esmaeili, H.R., Masoudi, M. et al. Early otolith development in the critically endangered tooth-carp, Aphanius farsicus (Teleostei: Cyprinodontidae). Environ Biol Fish 101, 1309–1317 (2018). https://doi.org/10.1007/s10641-018-0778-3