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Olfactory Organs in the Deep Sea Hatchetfish <I>Sternoptyx

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Olfactory Organs in the Deep Sea Hatchetfish <I>Sternoptyx NOTES BULLETIN OF MARINE SCIENCE, 53(3): 1163-1167, 1993 OLFACTORY ORGANS IN THE DEEP SEA HATCHETFISH STERNOPTYX DIAPHANA (STOMIIFORMES, STERNOPTYCHIDAE) Ronald C. Baird and George Y. Jumper It has been estimated that more than 80% of the deep sea fish fauna living at depths greater than 1,000 m exhibit sexual dimorphism in the olfactory system (Marshall, 1967). The most common form of dimorphism involves development oflarge, complex olfactory receptors in males while in females the olfactory system is regressed or microsmatic. Marshall also notes that in contrast, mesopelagic fishes living at depths less than 1,000 m generally have well-developed olfactory systems in both sexes and sexual dimorphism is uncommon. Recently, sexual dimorphism was reported in the olfactory organs of two me- sopelagic sternoptychids Argyropelecus hemigymnus and Valenciennellus tri- punctulatus by Baird et aI., 1990. Unlike many of the deeper living fishesdescribed by Marshall (op. cit.) the olfactory systems in females of these species are relatively well developed. The potential advantages of chemical communication to mate location in deep- sea fishes have been explored by Jumper and Baird (1991) and the use of odor cues appears to greatly enhance mate location in A. hemigymnus. The nasal rosettes of the hatchetfish Sternoptyx diaphana do not exhibit di- morphism. More importantly, the nasal rosettes of both sexes in S. diaphana are much smaller in size, and considerably less complex in structure than in A. hemi- gymnus. In this article, we describe the external morphology of the olfactory organs in sexually mature individuals of S. diaphana, compare them to that found in A. hemigymnus and briefly consider the implications of the microsmatic condition in relation to demography and reproduction of populations inhabiting the eastern Gulf of Mexico. METHODS Specimens of S. diaphana used for analysis were measured to the nearest millimeter (mm) standard length (SL). Individuals were considered sexually mature if the testes were enlarged and whitish in coloration for males or the ovary contained significant numbers of yolked eggs of about 0.4 mm or greater in diameter. Anum ber of mature individuals of both sexes were dissected by removing portions of the frontals and occipitals, exposing the telencephalon, olfactory lobes and much of the olfactory nerve. The diameter of the nerve was measured at a point prior to its separation into a right and left branch. The nasal rosettes were ovoid in shape and were characterized by two length measurements; the major axis (distance from end to end along the rosette midline) and minor axis (distance side to side measured along line normal to and bisecting the major axis). The cross sectional area listed in Table I is an elliptical approximation obtained by multiplying the product of both axes by ?T/4. Measurements were made to the nearest 0.1 mm by ocular micrometer. Readings less than 0.1 mm were not rounded and categorized as "less than 0.1 mm." In addition, individuals of both sexes of the species Sternoptyx obscura, S. pseudobscura, and S. pseudodiaphana were partially dissected in the same manner and were examined for the presence of microsmatism and sexual dimorphism. Museum of Comparative Zoology (MCZ) catalog numbers, geographic location and number of specimens examined are as follows: S. diaphana, MCZ 66686, 110-37'N, 6so-32'W (8); S. pseudodiaphana, MCZ 66685, 2°-38'S, 28°-47'W (3); S. obscura, MCZ 77436, 4°-12'N, 60°-08'E, (8); S. pseudobscura, MCZ 66688, 2°-44'S, 29°-05'W (5). 1163 1164 BULLETIN OF MARINE SCIENCE, VOL. 53, NO.3, 1993 Table 1. Comparison of ranges of morphometric and meristic characteristics of the olfactory organs in A. hemigymnus and S. diaphana A. hemigymnus S. diaphana Male Female (both sexes) Standard length (mm) 28-34 30-34 29-35 Number lamellae 19-23 11-14 o Rosette area (mm2) 1.0-1.7 0.6-0.7 0.2-0.4 Olfactory nerve diameter (mm2) 0.2-0.3 <0.1 <0.1 Number examined 7 6 (5F,3M) RESULTS AND DISCUSSION Olfaction. - The olfactory system of S. diaphana is depicted in Figure I. Nomen- clature follows Finger (1988). Microscopic examination of several individuals of both sexes of the three other known species in Sternoptyx (Badcock and Baird, 1980) confirmed that the olfactory organs in these species are microsmatic and similar morphologically to S. diaphana. The olfactory system of S. diaphana shares many similarities with A. hemigymnus, as described by Baird et at. (1990). As in most salmonoids there is an olfactory nerve which connects each nasal rosette to an olfactory bulb that lies near the rostral end of the telencephalon. The paired ovoid nasal rosettes are supported by bony olfactory capsules. Unlike A. hemigymnus, however, S. diaphana has an unpaired and, by com- parison, quite small olfactory bulb. The olfactory nerve is minute, the rosettes are small and lie exposed to the exterior (i.e., are not encased as in A. hemigymnus, by a nasal membrane). No sexual dimorphism is evident and the nasal epithelium in both sexes of S. diaphana is unfolded, lacking the lamellar structure which greatly increases the epithelial surface area in A. hemigymnus, particularly in sexually dimorphic macrosmatic males (Fig. 1). The nature and degree of some of these differences are expressed in Table 1. Note the lack oflamellar structure, small rosette cross sectional area and absence of dimorphism in S. diaphana. The olfactory organs in S. diaphana are clearly microsmatic, a characteristic of females of many bathypelagic fishes (Marshall, 1967). The nasal rosette cross sectional area in adult S. diaphana is about five times smaller than in males of A. hemigymnus of comparable length and there is an even larger difference in olfactory nerve cross-sectional area. There are order of magnitude differences in surface area (and presumably the number of chemoreceptors) of the nasal epi- thelium between the two species. Further, S. diaphana lacks the nasal membrane and naris system typical of A. hemigymnus, an adaptation in fishes to increase water flow across the receptor cells of the nasal epithelium. There are a number of important conclusions that follow from these observa- tions. Fishes known to rely heavily on olfactory cues have elongated nasal rosettes, much lamellar development in the nasal epithelium and significant signal pro- cessing capability as evidenced by considerable olfactory nerve, bulb and forebrain development (Moyle and Cech, 1982). The olfactory system of S. diaphana simply lacks the structural features indicative of high chemo-sensitivity and signal pro- cessing capability. The dimorphic condition is also absent. For these reasons we believe the olfactory sense in S. diaphana is unlikely to be sufficiently sensitive for effective long range chemical communication. By extension the olfactory sense is unlikely to playa major role in such activities as prey location or predator avoidance. There may, however, be some sensitivity to odors. Ifso, olfactory cues are likely sensed only in the near field. NOTES 1165 Olfactory Bulb Olfactory Nerve Nasal Rosette Nasal Rosettes Sternoptyx diaphana b male Stemoptyx ArgyropeIecus d\apllana hemlgymnus 30mmSL male •male 30mmSL 34mmSL Figure I. Schematic diagram of the morphology of the olfactory organs in S. diaphana. Note: Ol- factory tract not to scale. Insert: Nasal rosettes of male A. hemigymnus and S. diaphana at same scale. Demography and Reproduction. - The morphological evidence strongly suggests that the olfactory sense in Sternoptyx plays a less significant role biologically than in the two related genera described in Baird et al. (1990). Sexual dimorphism appears most prevalent in deeper living members of many deep sea groups (Mar- shall, 1967). This may not be the case in hatchetfishes where species of Sternoptyx are generally found at greater depths than species in related genera (Hopkins and Baird, 1985; Howell and Kruegar, 1987). The genus has evolved a number of morphological features unique within the family Sternoptychidae (Weitzman, 1974) and microsmatism appears to be another case in point. The lack ofa long range olfactory communication system in Sternoptyx suggests that male/female recognition occurs at considerably shorter ranges than expected in A. hemigymnus. For example, Jumper and Baird (1991) predict that phero- mones in A. hemigymnus could reach ranges of 30-80 m from an emitting female. Other mechanisms for extending mate recognition distance may exist however in Sternoptyx. For instance, while there are no sexually dimorphic photophores, both sexes possess oral light organs that appear to illuminate the mouth interior when open (Herring, 1977). Perception distances could theoretically be enhanced by "advertising" individuals coding bioluminescent signals. The question arises as to the severity of the mate location problem in the absence oflong range (> 3 m) communication in Sternoptyx. Hopkins and Baird (1985) found S. diaphana and A. hemigymnus to have net caught standing stocks of about equal magnitude and the former species to be found primarily between 600 and 800 m in the eastern Gulf of Mexico. There were no diel differences in depth evident in S. diaphana. However, the proportion of the population taken in trawls at size classes larger than 20 mm SL was much higher in A. hemigymnus, yet population mean densities over the depth range of maximum abundance were of 1166 BULLETIN OF MARINE SCIENCE, VOL. 53, NO.3, 1993 similar magnitude for both species. The important points are that adults of S. diaphana appear to occur deeper and at lower densities on average than A. hem i- gymnus in the Gulf and both species are sparsely distributed. This would mean that adult individuals of S. diaphana on average are 20-30 m apart if horizontal distributions are randomly dispersed over the 200 m depth range of maximum abundance. Jumper and Baird (1991) explore the consequences oflow population densities to mate location in the absence of long range communication.
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