Otoliths: Morphology, Hearing, and Growth:
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The fish inner ear consists of a membranous labyrinth made up of a series of sacs and canals, filled with a liquid similar to the interstitial fluid, the endolymph (Platt and Popper, 1981). The labyrinth is divided into a pars superior composed of three major canals and one sac-like structure, the utriculus, and the pars inferior composed of two additional sac-like structures, the sacculus and the lagena (Popper and Coombs, 1980; Platt and Popper, 1981) (Figure 1). The three major canals protruding from the labyrinth in the pars superior are known collectively as semicircular canals, and each connects at both ends with the utriculus. The semicircular canals are oriented at right angles from each other in three different planes. Each semicircular canal has a spherical expansion known as the ampulla at one end (Platt and Popper, 1981). Within the ampulla there is a sensory structure known as the crista (Platt and Popper, 1981). Above the crista there is a gelatinous cupula which is deformed by fluid movements within the canal (Platt and Popper, 1981). The semicircular canals serve to detect turning movements (Romer and Parsons, 1977). All fishes have three semicircular canals with the exception of hag fishes, which have one and lampreys which have two (Romer and Parsons, 1977). The utriculus is believed to be the main gravistatic organ in fishes, although it may also participate in sound reception in certain taxa (Popper, 1983). The two sac-like structures in the pars inferior, the sacculus and the lagena, function primarily in sound reception (Popper and Coombs, 1980, 1982; Platt and Popper, 1981; Popper, 1983).
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| Figure 1. Inner Ear of Fishes, Lateral View. SC= Semicircular Canals, U= Utriculus, UO=Utricular Otolith or Lapillus, M=Macula, SU=Sulcus, S=Sacculus, SO=Saccular Otolith or Sagitta, L=Lagena, LO=Lagenar Otolith or Asteriscus. Modified from Popper and Coombs (1982). |
All three sac-like structures of the inner ear have large areas of sensory epithelium, known as maculae. The macula contains sensory hair cells, each of which is surrounded by a number of microvilli-covered supporting cells, and is associated with branches of the eighth auditory nerve (Popper and Coombs, 1980; Platt and Popper, 1981; Popper, 1983). An apical bundle or tuft of cilia typically projects from the sensory hair cell into the otolithic chamber, and contains a single eccentrically placed cilium, the kinocilium, and numerous shorter, often graded sterocilia (Popper, 1983). As in the ampulla of the semicircular canals, there is a gelatinous membrane or cupula over the combined tips of the macula. In fishes this membrane becomes thickened by mineral depositions, forming a single solid compact structure, the otolith (Popper and Coombs, 1980; Platt and Popper, 1981; Popper, 1983).
Otoliths are composed primarily of aragonite, which is a form of calcium carbonate (Degens et al., 1969). They also contain from 0.2 to 10% organic matter in the form of a protein known as otolin. Otolin has a molecular weight of over 150,000 and is characterized by a high abundance of aspartic and glutamic acids, the presence of cystine and hydroxyproline, and a low content of aromatic and basic amino acids (Degans et al., 1969). Otoliths are supported on the macula by a thin otolithic membrane which connects to the microvilli on the supporting cells of the sensory epithelium and to the surface of the otolith (Popper and Coombs, 1982; Popper, 1983). The otolithic membrane maintains the position of the otolith with respect to the sensory epithelium, while allowing the two structures to move independently of one another (Popper and Coombs, 1980). Each sac-like structure has its own otolith, the otolith of the utriculus is known as the lapillus, the otolith of the sacculus is known as the sagitta, and the otolith of the lagena is known as the asteriscus. The lapillus is typically the least variable morphologically. The sagitta and asteriscus are both highly variable morphologically, with the asteriscus presenting its greatest variability and development in ostariophysine teleosts, and the sagitta presenting the greatest variability and development in nonostariophysine teleosts (Platt and Popper, 1981).
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Sagittae are typically oval and laterally flattened in shape with smooth or crenulated rims. Many sagittae have long, well developed processes or highly irregular rims. The lateral face of the sagitta is usually irregular, occasionally possessing large processes. The medial face is usually smooth and possesses well defined, regular features. Nolf (1985) presented a summary of terms that have been used to describe the medial face, however, no terminology has been developed to describe the lateral face of the sagitta. The impression formed where the macula comes into contact with the medial face of the sagitta is known as the sulcus (Figure 2). It is typically the same shape as the macula (Gauldie, 1988) and differs morphologically from one group to the next. The sulcus can be divided into two regions, the anterior region is called the ostium and the posterior region is called the cauda. In acanthopterygians the ostium is usually enlarged and oval in shape, and the cauda is more elongate, somewhat resembling a tail (Nolf, 1985).
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| Figure 2. Medial View of Left Sagitta of Cynoscion arenarius Indicating the Location of the Sulcus, Ostium, and Cauda. |
Sagittae vary tremendously in shape and size in different groups of fishes. Many different factors have been reported to influence sagitta morphology, however, two factors have been especially prominent in the literature. These are the selective pressures acting on sagittae so their morphology meets specific auditory needs (Platt and Popper, 1981; Popper and Coombs, 1982; Gauldie, 1988) and the effects of differences in growth rate caused by environmental factors such as water temperature, depth, and mineral and food availability (Wilson, 1985; Lombarte, 1992; Lombarte and Lleonart, 1993; Arellano et al., 1995; Aguirre and Lombarte, 1999). Constraints in terms of physical packing of sagittae within the skull have also been cited in several papers, especially those treating closely related species with large sagittae (Gaemers, 1984; Smith, 1992; Arellano et al., 1995). However, this latter factor has only been mentioned in the literature, it has not been thoroughly studied.
Sagittae are the major receptors of sound in fish. As such, they may be subject to strong selective pressures related to the specific auditory needs of different taxa. Fishes hear when sound waves cause the sensory epithelium and the sagittae to vibrate. Because of their different densities these structures vibrate at different rates, producing a shearing action which bends the sensory cells and is translated into a sound signal by the auditory nerves (Platt and Popper, 1981; Popper, 1983; Gauldie, 1988). Morphological differences in sagitta shape and sculpturing may affect the patterns through which sagittae move on the sensory epithelium resulting in the macula being stimulated differentially under distinct acoustic conditions (Popper and Coombs, 1980, 1982; Platt and Popper, 1981; Popper, 1983; Gauldie, 1988).
Gauldie (1988) proposed a model in which sagittae shape is controlled by functional aspects related to hearing. Since action potentials of sensory cells are produced by shearing in the horizontal plane of the macula, stimulation of sagitta from sources perfectly orthogonal to the plane of the macula would not stimulate the sensory cells. This limitation is overcome in Gauldie’s model by the fact that the region of the sagitta extending beyond the sensory cell pad of the macula acts as a lever pivoted on another fixed lever composed of the protein matrix uniting the sagitta with the sensory cells. This lever system would allow for shearing between the sensory cells and the sagitta even when the sound source is orthogonal to the plain of the macula. Gaudie further hypothesized the frequency response and the auditory threshold of the fish ear would be directly related to the ratio of macula area to otolith area with species that have a higher macula area to sagitta area ratio, possessing a higher sensitivity to particular frequencies. Gauldie’s model has important implications for the relationship between the area of the sagitta and the area of the macula (or sulcus), and has been cited in several later papers (Lombarte, 1992; Arellano et al., 1995; Aguirre and Lombarte, 1999).
Intraspecific and interspecific differences in sagitta morphology have been attributed in many cases to differences in growth rate. In many studies, the presence of larger sagittae in specimens, populations or species with lower somatic growth rates has been attributed to a process known as “uncoupling”, in which sagittae grow independently of somatic growth rate. Although there are studies in which uncoupling was tested and did not occur (i.e. Dickey et al., 1997), cases in which slower growing individuals had larger sagittae than fast growing individuals have been documented for wild specimens (Templeman and Squires, 1956; Smith, 1992; Francis et al., 1993) as well as for specimens under experimental conditions (i.e. Mosegaard et al., 1988; Reznick et al., 1989; Secor and Dean, 1989; Wright et al., 1990). Wilson (1985) also discussed the potential importance of growth rate on sagitta morphology. However, this author speculated higher growth rates, not lower growth rates, could be partly responsible for the occurrence of larger sagittae in some macrourids. Similar results have been documented for other deepwater fishes (Botha, 1971; Lombarte, 1992; Lombarte and Lleonart, 1993). Campana and Casselman (1993) summarized a series of stock discrimination studies using otolith shape analysis and found different growth rates were by far the most important factor contributing to differences in sagitta size as well as shape. Several cases of sexual dimorphism of sagittae have also been attributed to differences in growth rate between males and females (Templeman and Squires, 1956; Gaemers and Crapon de Crapona, 1986; Echeverria, 1987; Campana and Casselman, 1993).
Sciaenids are characterized, among other things, by having extremely large sagittae that vary greatly in morphology among genera and even among species of the same genus. In addition, sciaenid sagittae have a unique tadpole shaped sulcus with a massively enlarged ostium and a cauda curved downward and frequently extending anteriorly (Trewavas, 1977; Chao, 1978) (Figure 2). Most species of Cynoscion have large sagittae, even relative to those of other sciaenids. They also tend to be more elongate than those of other sciaenids, this is especially noticeable in large adults. The posterior portion of the sagitta is typically thicker than the anterior portion (Chao, 1978). The sulcus is relatively elongate and the ostium is oval or frequently pear-shaped (Chao, 1978).
Sagittae of Cynoscion have been put to multiple uses. They are most commonly used for ageing fish in stock assessment studies (Lowerre-Barbieri et al., 1994; Murphy and Taylor, 1994; Lowerre-Barbieri et al., 1995; Warren, 1995). They have also been used for identifying species from stomach contents (Laerm et al., 1997), from die-offs (Martini and Reichenbacher, 1997), and from the fossil record. Mendo (1986) used sagitta morphology to distinguish between the morphologically similar species C. analis and I. remifer in Peru. Colura and King (1989) attempted to use sagitta morphology for identifying stocks of Cynoscion nebulosus in the Gulf of Mexico.
Sagittae have also been popular in phylogenetic studies of the genus. Moshin (1981) speculated on the phylogenetic relationships of the four species occurring in the north west Atlantic based on the morphology of their sagittae. Later, Schwarzhans (1993) divided Cynoscion into four subgenera based on sagitta morphology. He placed the species C. arenarius, C. jamaicensis, C. nebulosus, C. nothus, C. phoxocephalus, C. regalis, C. similis, and C. thalassinus in the subgenus Cynoscion. He defined this subgenus as having the most pleisomorphic sagittae, with a relatively small ostium, and a gently curving postdorsal rim. He placed the species C. acoupa, C. albus, C. elongatus, C. leiarchus, C. microlepidotus, C. parvipinnis, C. reticulatus, C. steindachneri, C. stolzmanni, and C. xanthulus in the subgenus Apseudobranchus, defining this subgenus as having a relatively large ostium, having the sagitta wider anteriorly and narrowing posteriorly, and typically having a distinct concave area at the postventral rim. He placed the species C. squamipinnis, C. praedatorius, and C. virescens in the subgenus Buccone, and defined this subgenus as having a straight, oblique posterior rim, a strongly widened parallelogram shaped ostium, and a concave postventral rim. Finally, Schwarzhans placed the species C. analis and C. othonopterus in the subgenus defining this subgenus as intermediate between Cynoscion and the closely related genus . The sagittae are thin, flat, elongate, and parallelogram-shaped.
Aguirre, H., and A. Lombarte. 1999. Ecomorphological comparisons of sagittae in Mulus barbatus and M. surmuletus. Journal of Fish Biology 55:105-114.
Arellano, R.V., O. Hamerlynck, M. Vinex, J. Mees, K. Hostens, and W. Gijselinck. 1995. Changes in the ratio of the sulcus acusticus area to the sagitta area of Pomatoschistus minutus and P. lozanoi (Pisces, Gobiidae). Marine Biology 122:355-360.
Botha, L. 1971. Growth and otolith morphology of the Cape hakes Merluccius capensis Cast. and M. paradoxus Franca. Investigational Report Division of Sea Fisheries of South Africa No. 97. Capetown. 32 pp.
Campana S.E., and J.M. Casselman. 1993. Stock discrimination using otolith shape analysis. Canadian Journal of Fisheries and Aquatic Sciences 50:1062-1083.
Chao, L.N. 1978. A basis for classifying western Atlantic Sciaenidae (Teleostei: Perciformes). NOAA Technical Report Circular- 415. 64 pp.
Colura, R.L., and T.L. King. 1989. Preliminary evaluation of the use of calcified structures for separating spotted seatrout stocks. Texas Management Data Series No. 3. Austin. 7 pp.
Degens, E.T., W.G. Deuser, and R.L. Haedrich. 1969. Molecular structure and composition of fish otoliths. Marine Biology 2:105-113.
Dickey, C.L., J.J. Isely, and J.R. Tomasso. 1997. Slow growth did not decouple the otolith size-fish size relationship in striped bass. Transactions of the American Fisheries Society 126:1027-1029.
Echeverria, T.W. 1987. Relationship of otolith length to total length in rockfishes from northern and central California. Fishery Bulletin 85(2):383-387.
Francis, M.P., M.W. Williams, A.C. Pryce, S. Pollard, S.G. Scott. 1993. Uncoupling of otolith and somatic growth in Pargus auratus (Sparidae). Fishery Bulletin 91:159-164.
Gaemers, P.A.M. 1984. Taxonomic position of the Cichlidae (Pisces, Perciformes) as demonstrated by the morphology of their otoliths. Netherlands Journal of Zoology 34(4):566-595.
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Lombarte, A. 1992. Changes in otolith area: sensory area ratio with body size and depth. Environmental Biology of Fishes 33:405-410.
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with a discussion of historical changes in maximum size. Fishery Bulletin 93:643-656.
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Moshin, A.K.M. 1981. Comparative account of the otoliths of the weakfishes (Cynoscion) of the Atlantic and Gulf coasts of the United States. Pertanika 4(2):109-111.
Mossegaard, H., H. Svedang, and K. Taberman. 1988. Uncoupling of somatic and otolith growth rate in Arctic char (Salvelinus alpinus) as an effect of differences in temperature response. Canadian Journal of Fisheries and Aquatic Sciences 45:1514-1524.
Murphy, M.D., and R.G. Taylor. 1994. Age growth and mortality of spotted seatrout in Florida waters. Transactions of the American Fisheries Society 123:482-497.
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Reznick, D., E. Lindbeck, and H. Bryga. 1989. Slower growth results in larger otoliths: An experimental test with guppies (Poecilia reticulata). Canadian Journal of Fisheries and Aquatic Sciences 46:108-112.
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Smith, M.K. 1992. Regional differences in otolith morphology of the deep slope red snapper Etelis carbunculus. Canadian Journal of Fisheries and Aquatic Sciences 49:795-804.
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Last Updated: 18 February 2001
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