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Saccular Otolith Mass Asymmetry in Adult Flatfishes 2581

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Saccular Otolith Mass Asymmetry in Adult Flatfishes 2581 Journal of Fish Biology (2008) 72, 2579–2594 doi:10.1111/j.1095-8649.2008.01869.x, available online at http://www.blackwell-synergy.com Saccular otolith mass asymmetry in adult flatfishes D. V. LYCHAKOV*†,Y.T.REBANE‡, A. LOMBARTE§, M. DEMESTRE§ AND L. A. FUIMANk *Sechenov Institute of Evolutionary Physiology and Biochemistry of Russian Academy of Sciences, St Petersburg, Thorez pr., 44, 194223, Russia, ‡Ioffe Physical Technical Institute of Russian Academy of Sciences, Politekhnicheskaya 26, St Petersburg 194021, Russia, §Departament de Recursos Marins Renovables, Institut de Cie`ncies del Mar-CMIMA (CSIC), Passeig Marıtim´ 37-49, 08003 Barcelona, Catalonia, Spain and kDepartment of Marine Science, University of Texas at Austin, Marine Science Institute, 750 Channel View Drive, Port Aransas, TX 78373-1267, U.S.A. (Received 29 June 2007, Accepted 20 February 2008) A dimensionless measure of otolith mass asymmetry, w, was calculated as the difference between the masses of the right and left paired otoliths divided by average otolith mass. Saccular otolith mass asymmetry was studied in eight flatfish species (110 otolith pairs) and compared with data from a previously published study on roundfishes. As in the case of symmetrical fishes, the absolute value of w in flatfishes does not depend on fish length and otolith growth rate, although otolith mass and the absolute value of otolith mass difference are correlated with fish length. The values of w were between À0Á2 and þ0Á2in96Á4% of flatfishes studied. The mean Æ S.E. value of w in flatfishes was significantly larger than in standard bilaterally symmetrical marine fishes (‘roundfishes’), respectively 0Á070 Æ 0Á006 and 0Á040 Æ 0Á006. The most prominent distinction is the existence of downside prevalence of saccular otolith mass in flatfishes, which contrasts with no right–left prevalence in roundfishes found in a previous study. In the right- eyed flatfishes (Soleidae), the left saccular otoliths are heavier than the right otoliths. In the left- eyed flatfishes (Bothidae and Citharidae), the right saccular otoliths are heavier than the left otoliths. Not all flatfishes, however, fit in this design: 11Á8% of flatfishes studied had the heavier saccular otoliths in the upside labyrinth and 5Á4% of flatfishes had no otolith mass asymmetry (within the accuracy of the analysis). At the same time, the more mobile flatfishes (bothids and citharids) have more symmetrical and, hence, more precisely organized saccular otolith organs than the bottom-associated flatfishes (soleids). It is possible to assume that the value of the otolith asymmetry is not only correlated with flatfish placement in a particular family, or position of eyes, but also may correlate with general aspects of their ecology. Mathematical modelling indicated that for most flatfishes one-side saccular prevalence had no substantial significance for sound processing. On the other hand, calculations showed that 49% of flatfishes (but only 14Á5% of roundfishes) have jwj which exceed the critical level and, in principle, could sense the difference between the static displacement of the large and small paired otoliths. At that, the number of the soleids that could sense this difference is greater than the number of the bothids and citharids, 84 and 27%, respectively. # 2008 The Authors Journal compilation # 2008 The Fisheries Society of the British Isles Key words: flatfishes; mathematical modelling; morphometry; saccular otolith. †Author to whom correspondence should be addressed. Tel.: þ7 812 5504989; fax: þ7 812 5523012; email: [email protected] 2579 # 2008 The Authors Journal compilation # 2008 The Fisheries Society of the British Isles 2580 D. V. LYCHAKOV ET AL. INTRODUCTION Otolith mass asymmetry may be responsible at least partly for both space illu- sionary sensations and space motion sickness in human subjects and abnormal behaviour when fishes are subjected to weightlessness during parabolic or space flight (Egorov & Samarin, 1970; Hoffman et al., 1977; Von Baumgarten et al., 1982). Mathematical modelling has shown that acoustic functionality (sensitiv- ity, temporal processing and sound localization) of a fish can be altered by oto- lith mass asymmetry due to incompatibility and incongruity of the right and left otolith movements (Lychakov & Rebane, 2005). There are some extreme values of otolith asymmetry in fishes (Lychakov, 1996; Lychakov et al., 2006). Obviously, to avoid the detrimental effects due to mass discrepancy, a large otolith asymmetry must be accommodated by the central nervous sys- tem or at the macular level. The questions arise: what degree of otolith asym- metry does have an affect on the functioning of otolith organs? Does the natural otolith asymmetry have substantial implication for sound and vestibu- lar processing for most fishes? Teleosts are well-suited biological models for assessing the physiological role of otolith mass asymmetry because the compact otoliths can easily be quanti- tatively assessed. Otolith mass asymmetry was studied in 811 otolith pairs of 77 bilaterally symmetric teleost species (roundfishes) (Lychakov et al., 2006). Mathematical modelling has indicated that for most roundfishes, otolith mass asymmetry is well below critical values, so that most roundfishes do not experi- ence functional impairment as a result of otolith mass asymmetry (Lychakov & Rebane, 2005; Lychakov et al., 2006). In contrast to roundfishes, otolith asym- metries have been reported in flatfishes (Nolf, 1985; Campana, 2004; Helling et al., 2005). These asymmetries seem at first glance quite natural because flat- fishes (Order Pleuronectiformes) have the most asymmetric shape and lateralized behaviour of any fishes. During their metamorphosis, flatfishes undergo a 90° tilt to the right or left side to become bottom-adapted animals (Platt, 1973; Graf & Baker, 1990; Schreiber, 2006). At the same time, the otolith organs do not rotate within the skull, as the eyes do, and retain their individual structural orientation relative to the dorsal fin (Fig. 1) (Platt, 1973; Sogard, 1991). It is possible to assume that the otolith asymmetries revealed in adult flatfishes, may have as yet unknown adaptive significance. The aims of the present study were to quantify otolith mass asymmetry in a large number of flatfishes and to model its influence on auditory and vestib- ular functions. Because the flatfish sacculi are involved in both hearing and gravity (vestibular) perception (Chapman & Sand, 1974; Graf & Baker, 1990) only this organ was chosen for investigation. MATERIALS AND METHODS Data used in the analysis were collected from eight species of adult Pleuronectiformes from the Catalan coast (north-western Mediterranean) caught with an epibenthic dredge (Table I). All fishes were obtained in experimental trawl cruises; all fishes were dead when they arrived on board. Experimental procedures for extracting and prepar- ing otoliths for the study were published previously (Lombarte & Morales-Nin, 1995; Lombarte et al., 2006) and are briefly described here. Standard lengths (LS) were # 2008 The Authors Journal compilation # 2008 The Fisheries Society of the British Isles, Journal of Fish Biology 2008, 72, 2579–2594 SACCULAR OTOLITH MASS ASYMMETRY IN ADULT FLATFISHES 2581 FIG. 1. Schematic drawings of (a) the premetamorph flatfish larva from a top view and (b) adult right- eyed flatfish from a side view (not to scale). The premetamorph flatfish larva is pelagic with dorsal fin upright, and with lateralized eyes. The adult flatfish lies on the left side (blind-side) with dorsal fin horizontal, and both eyes are on the right side (eyed-side). The saccular otoliths are in the conventional morphological position relative to the dorsal fin in premetamorph and adult flatfishes. Right and left saccular otoliths are represented as short black strips. They deviate from the mid- sagittal plane of the fish by an angle 45°. b is an angle between the longitudinal axis of the fish and the axis of stimulation. I and II correspond to the situation such that the sound direction (arrow) is coincident or not with the longitudinal axis of the fish. measured from the tip of the snout to the base of the tail prior to removal of otoliths. After dissection of the auditory capsules, saccular otoliths were removed from each side, rinsed in distilled water, air-dried at room temperature for several days and then weighed on an OHAUS (Pine Brook, NJ, U.S.A.) analytical plus balance with a preci- sion of 0Á0001 g. For comparison, previously collected data from marine fishes (74 spe- cies, 608 saccular paired otolith) were used (Lychakov et al., 2006). # 2008 The Authors Journal compilation # 2008 The Fisheries Society of the British Isles, Journal of Fish Biology 2008, 72, 2579–2594 2582 Journal compilation TABLE I. Species used in this study, number of fishes (n), standard length (LS) range, saccular otolith mass (M) range, heavier saccular otolith location, mean absolute otolith asymmetry jwj, relation between LS and otolith asymmetry and number of fishes with otolith asymmetry exceeding the value of the critical level (jwjcrit) Side of heavier otolith Regression # location (number of fishes) jwj LS and jwj Number of 2008 The Fisheries Society of the British Isles, Species and fishes with 2 Position of eyes Family common name nLS (mm) M (mg) Left Right Equal Mean Æ S.E. Prjwj > jwjcrit Right-eyed Soleidae Microchirus variegatus 12 85–145 3Á35–10Á30 12 — — 0Á119 Æ 0Á021 0Á338 0Á092 11 (left side (Donovan, 1808) blind fishes) Thickback sole D. V. LYCHAKOV Soleidae Monochirus hispidus 7 55–110 1Á27–7Á38 6 1 — 0Á075 Æ 0Á021 0Á681 0Á036
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