Relationships between inner ear and sagitta growth during ontogenesis of three Carapini species, and consequences of life-history events on the otolith microstructure
Parmentier, Eric; Lagardère, Françoise; Vandewalle, Pierre
[en] Three species of Carapidae have in common a tenuis larval stage, during which they settle in the lagoon and take refuge in the same species of holothurold. From the juvenile stage, Carapus homei and C. boraborensis are commensal, whereas Encheliophis gracilis is parasitic. The aims of this study were to analyse to what extent the ontogenctic changes of the otic capsule affected the shape of the inner ear and how environmental cues, due to the above-mentioned life history and the style, could influence the structure of the sagitta. Sagittal sections revealed a three-dimensional asymmetry with a nucleus close to the proximal surface. Observations of the growth axis of the sagitta suggest it has a morphogenetic impact on the otic cavity. Each sagitta contains three main zones related to the life stages of the fish. Bands and checks were observed in the third zone in C. homei and C. boraborensis, but this pattern was less discernible in E. gracilis. These structural differences in zone 3 could be related to the commensal and parasitic life styles of these fishes. Further studies dealing with otosac features and otolith functions are suggested.
Disciplines :
Zoology Aquatic sciences & oceanology
Author, co-author :
Parmentier, Eric ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Morphologie fonctionnelle et évolutive
Vandewalle, Pierre ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Morphologie fonctionnelle et évolutive
Language :
English
Title :
Relationships between inner ear and sagitta growth during ontogenesis of three Carapini species, and consequences of life-history events on the otolith microstructure
Publication date :
September 2002
Journal title :
Marine Biology
ISSN :
0025-3162
eISSN :
1432-1793
Publisher :
Springer-Verlag, New York, United States - New York
Arnold DC (1956) A systematic revision Of the fishes of the teleost family Carapidae (Percomorphi, Blennioidea), with description of two new species. Bull Br Mus (Nat Hist) Zool 4:247-307
Brothers EB, Williams DMcB, Sale PF (1983) Length of larval life in twelve families of fishes at "One Tree Lagoon", Great Barrier Reef, Australia. Mar Biol 76:319-324
Campana SE (1983) Feeding periodicity and the production of daily growth increments in otoliths of steelhead trout (Salmo gairdneri) and starry flounder (Platichthys stellatus). Can J Zool 61:1591-1597
Campana SE (1984) Lunar cycles of otoliths growth in the juvenile starry flounder Platichthys stellatus. Mar Biol 80:239-246
Campana SE (1999) Chemistry and composition of fish otoliths: Pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263-297
Campana SE, Jones CM (1992) Analysis of otolith microstructure data. Can Spec Publ Fish Aquat Sci 117:73-100
Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014-1031
Degens ET, Deuser WG, Haedrich RL (1969) Molecular structure and composition of fish otoliths. Mar Biol 2:105-113
Dufour V, Riclet E, Lo-Yat A (1996) Colonization of reef fishes at Moorea Island, French Polynesia: Temporal and Spatial Variation of the larva flux. NZ J Mar Freshw Res 47:413-422
Dunkelberger DG, Dean JM, Watabe N (1980) The ultrastructure of the otolithic membrane and otolith in the juvenile mummichog, Fundulus heteroclitus. J Morphol 163:367-377
Gauldie RW (1991) The morphology and periodic structures of the otolith of the chinook salmon (Onchorynchus tshawytscha), and temperature-dependent variation in otolith microscopic growth increment width. Acta Zool 72:159-179
Gauldie RW, Nelson GDA (1990) Otolith growth in fishes. Comp Biochem Physiol A 97:119-135
Gauldie RW, Coote G, Mulligan KP, West IF, Merrett NR (1991) Otoliths of deep water fishes: Structure, chemistry and chemically-coded life histories. Comp Biochem Physiol A 100:1-31
Jangoux M (1974) Sur l'association entre certaines astéries (Echinodermata) et des poissons Carapidae. Rev Zool Afr 88:189196
Jones C, Brothers EB (1987) Validation of the otolith increment aging technique for stripped bass, Morone saxatilis, larvae reared under suboptimal feeding conditions. Fish Bull (Wash DC) 85:171-178
Lagardère F, Troadec H (1997) Age estimation in common sole Solea solea larvae: Validation of daily increments and evaluation of a pattern recognition technique. Mar Ecol Prog Ser 155:223-237
Lecomte-Finiger R (1992) Growth history and age at recruitment of European glass eels (Anguilla anguilla) as revealed by otolith microstructure. Mar Biol 144:205-210
Lee TW, Byun JS (1996) Microstructural growth in otolith of conger eel (Conger myriaster) leptocephali during the metamorphic stage. Mar Biol 125:259-268
Lombarte A, Leonart J (1993) Otolith size changes related with body growth, habitat depth and temperature. Environ Biol Fishes 37:297-306
Lombarte A, Popper AN (1994) Quantitative analysis of postembryonic hair cell addition in the otolithic endorgans of the inner ear of the European hake, Merluccius merluccius (Gadiformes, Teleostei). J Comp Neurol 345:419-428
Mayer-Gostan N, Kossmann H, Watrin A, Payan P, Bœuf G (1997) Distribution of ionocytes in the saccular epithelium of the inner ear of two teleosts (Oncorhynchus mykiss and Scophthalmus maximus). Cell Tissue Res 289:53-61
Moksness E, Rukan K, Ystanes L, Folkvord A, Johannessen A (1995) Comparison of somatic and otolith growth in North Sea herring (Clupea harengus L.) larvae: Evaluation of growth dynamics in mecocosms. In: Secor DH, Dean JM, Campana SE (eds) Recent Developments in Fish Otolith Research. University of South Carolina Press, Columbia, pp 119-134
Molony BW (1996) Episodes of starvation are recorded in the otoliths of juvenile Ambassis vachelli (Chandidae), a tropical estuarine fish. Mar Biol 125:439-446
Morales-Nin B (2000) Review of the growth regulation processes of otolith daily increment formation. Fish Res (Amst) 46:53-67
Morales-Nin B, Raltson S (1990) Age and growth Of Lutjanus kasmira (Forskål) in Hawaiian waters, J Fish Biol 36:191-203
Morales-Nin B, Guttierrez E, Massutti S (1995) Patterns of primary growth increments in otoliths of Sparus aurata larvae in relation to water temperature and food consumption. Sci Mar 59:57-64
Mugiya Y (1974) Calcium-45 behavior at the level of the otolithic organs of rainbow trout. Nippon Suisan Gakkaishi 40:457-463
Mugiya Y (1984) Diurnal rhythm in otolith formation in the rainbow trout, Salmo gairdeni: Seasonal reversal of the rhythm in relation to plasma calcium concentrations. Comp Biochem Physiol A 78:289-293
Neilson JD, Geen GH (1985) Effects of feeding and diet temperature cycles on otolith increment formation in juvenile chinook salmon, Onchorynchus tshawytscha. Fish Bull (Wash DC) 83:91-101
Olney JE, Markle DF (1979) Description and occurrence of vexillifer larvae of Echiodon (Pisces: Carapidae) in the western North Atlantic and notes on other carapid vexillifers. Bull Mar Sci 29:365-379
Padoa E (1947) Note di ittologia mediterranea, Nota V. Forme post-larvali e giovanili di Carapus (sin. Fierasfer). Pubb Staz Zool Napoli 20:111-121
Parmentier E, Chardon M, Poulicek M, Bussers JC, Vandewalle P (1998) Morphology of the buccal apparatus and related structures in four Carapidae. Aust J Zool 46:391-404
Parmentier E, Castillo G, Chardon M, Vandewalle P (2000) Phylogenetic analysis of the pearlfish Carapini (Ophidiiformes, Carapidae). Acta Zool 81:293-306
Parmentier E, Lo-Yat A, Vandewalle P (2001a) Identification of tenuis of four French Polynesian Carapini (Carapidae: Teleostei). Mar Biol 140:633-638. DOI 10.1007/s00227-001-0726-0
Parmentier E, Vandewalle P, Lagardère F (2001b) Morpho-anatomy of the otic region in carapid fishes-eco-morphology study of their otoliths. J Fish Biol 58:1046-1061
Payan P, Borelli G, Bœuf G, Mayer-Gostan N (1998) Relationship between otolith and somatic growth: Consequence of starvation on acid-base bahmce in plasma and endolymph in the rainbow trout Onchorynchus mykiss. Fish Physiol Biochem 19:35-41
Payan P, Edeyer A, de Pontual H, Borelli G, Bœuf G, Mayer-Gostan N (1999) Chemical composition of saccular endolymph and otolith in fish based on the chemistry of the endolymph. Am J Physiol 277:123-131
Pisam M, Payan P, LeMoal C, Edeyer A, Boeuf G, Mayer-Gostan N (1998) Ultrastructural study of the saccular epithelium of the inner ear of two teleosts, Oncorhynchus mykiss and Scophthalmus maximus. Cell Tissue Res 294:261-270
Platt C, Popper AN (1981) Fine structure and function of the ear, In: Tavolga WN, Popper AN, Fay RR (eds) Hearing and Sound Communication in Fishes. Springer, New York Berlin Heidelberg, pp 2-37
Popper AN, Lu Z (2000) Structure-function relationships in fish otolith organs. Fish Res (Amst) 46:15-25
Radtke RL (1987) Age and growth information available from the otoliths of the Hawaiian snapper, Pristipomoides filamentosus. Coral Reefs 6:19-25
Smith CL (1964) Some pearlfishes from Guam, with notes on their ecology. Pac Sci 18:34-40
Smith CL, Tyler JC (1969) Observations on the commensal relationship of the western Atlantic pearlfish, Carapus bermudensis, and holothurians. Copeia 1969:206-208
Smith CL, Tyler JC, Feinberg MN (1981) Population ecology and biology of the pearlfish (Carapus bermudensis) in the lagoon at Bimini, Bahamas. Bull Mar Sci 3:876-902
Sogard SM (1992) Interpretation of otolith microstructure in juvenile winter flounder (Pseudopleuronectes americanus): Ontogenetic development, daily increment validation, and somatic growth relationships. Can J Fish Aquat Sci 48:1862-1871
Strasburg DW (1961) Larval carapid fishes from Hawaii, with remarks on the ecology of adults. Copeia 1961:478-480
Takagi Y (1997) Meshwork arrangement of mitochondria-rich, Na+, K+-ATPase-rich cells in the saccular epithelium of rainbow trout (Onchoryhnchus mykiss) inner ear. Anat Rec 248:483-489
Takagi Y (2000a) Cellular contributions to the otolith formation in teleosts: A review. Otsuchi Mar Sci 25:1-6
Takagi Y (2000b) Ultrastructural immunolocalization of the otolith water-soluble-matrix in the inner ear of rainbow trout justhatched fry. Fish Sci (Tokyo) 66:71-77
Takagi Y, Takahashi A (1999) Characterization of otolith soluble-matrix producing cells in the saccular epithelium of rainbow trout (Onchorryhnchus mykiss) inner ear. Anat Rec 254:322-329
Toole CL, Markle DM, Harris PM (1993) Relationships between otolith microstructure, microchemistry, and early life history events in Dover sole, Microstomus pacificus. Fish Bull (Wash DC) 91:732-753
Toshe H, Mugiya Y (2001) Effects of enzyme and anion transport inhibitors on in vitro incorporation of inorganic carbon and calcium into endolymph and otoliths in salmon Oncorhynchus masou. Comp Biochem Physiol A 128:177-184
Trott LB (1970) Contribution of the biology of carapid fishes (Paracanthopterygian: Gadiformes). Univ Calif Publ Zool 89:1-41
Trott LB (1981) A general review of the pearlfishes (Pisces, Carapidae). Bull Mar Sci 31:623-629
Tsukamoto K, Kajihara T (1987) Age determination of ayu with otolith. Nippon Suisan Gakkaishi 53:1985-1997
Van Den Spiegel D, Jangoux M (1989) La symbiose entre poissons Carapidae et Holoturies autour de l'île de Laing (Met de Bismarck, Papouasie Nouvelle Guinée). Indo-Mal Zool 6:223-228
Victor BC (1982) Daily otolith increments and recruitment in two coral-reef wrasses, Thalassoma bifasciatum and Halichores bivitatus. Mar Biol 71:203-208
Victor BC (1986) Delayed metamorphosis with reduced larval growth in a coral reef fish (Thalassoma bifasciatum). Can J Fish Aquat Sci 43:1208-1213
Wang CH, Tzeng WN (2000) The timing of metamorphosis and growth rates of American and European eel leptocephali: A mechanism of larval segregative migration. Fish Res (Amst) 46:191-205
Wilson DT, McCornick MI (1999) Microstructure of settlementmarks in the otoliths of tropical reef fishes. Mar Biol 134:29-41
Zhang Z (1992) Ultrastructure of otolith increments and checks in the teleost fish Oreochromis niloticus. J Morphol 211:213-220
Zhang Z, Runham NW (1992) Otolith microstructure pattern in Oreochromis niloticus (L.). J Fish Biol 40:325-332
