BULLETIN OF MARINE SCIENCE, 47(2): 561-566, 1990

NOTES

SEXUAL DIMORPHISM AND DEMOGRAPHY IN TWO OF OCEANIC MIDW ATER FISHES (: STERNOPTYCHIDAE) FROM THE EASTERN GULF OF MEXICO

Ronald C. Baird, George Y. Jumper and E. E. Gallaher

Marshall (1967) estimates that about 80% of the deep-sea fish fauna living at depths greater than 1,000 m exhibit sexual dimorphism in the olfactory system. The highly developed olfactory organs in males are thought to function in the location of potential mates by olfactory cues (Mead et aI., 1964; Marshall, 1967; 1971). Marshall (1967) also notes that unlike bathypelagic species, fishes living at mesopelagic depths (ca. 200-1,000 m) seldom exhibit dimorphism in olfactory morphology and both sexes usually have well-developed olfactory organs. Me- sopelagic exceptions are the numerically abundant, transparent species of the Cyclothone (Badcock and Merrett, 1976). In this study we describe for the first time sexual dimorphism in the olfactory organs of two species of sternoptychids ( hemigymnus and Valen- ciennellus tripunctulatus) that also inhabit mesopelagic environments. Demo- graphic information is presented from populations of both species resident in the eastern Gulf of Mexico, and we consider the implications of demography for mate location, chemical communication and reproduction.

METHODS

Specimens for analysis were measured to the nearest millimeter (mm) standard length (SL). Indi- viduals were sexed on the basis of the presence of oocytes or significant testicular development. Smaller fish which could not be sexed were classified as sex indeterminate. The nasal rosette on the right side was removed and the lamellae of one row were counted. In a number of large adults (> 23 mm SL) portions of the frontals and occipitals were dissected exposing the telencephalon, olfactory lobes and much of the olfactory tract. The greatest diameter of the olfactory tract was measured at approximately midway between the separation of the tract into a right and left branch and the nasal rosettes (at approximately the points indicated by the label lines in Fig. I). Rosettes are ovoid in shape and were characterized by two length measurements; the major axis (the distance from end to end measured along the rosette midline) and the minor axis (the distance from side to side measured along a 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 the lengths of the major and minor axes by 1r/ 4. Measurements were made to the nearest 0.1 mm by ocular micrometer under a dissecting microscope. Readings ofless than 0.1 mm were not rounded and were categorized as "less than 0.1 mm."

REsULTS AND DISCUSSION Olfaction. - The organization of the olfactory system in both species is similar in general form to the salmonoid bauplan described by Finger (1987) in which there is an olfactory tract connecting each nasal rosette to a prominent olfactory lobe or bulb at the rostral end of the telencephalon. In A. hemigymnus there are large paired olfactory lobes from which an olfactory tract extends to each rosette (Fig. 1). In V. tripunctulatus the olfactory tract at its connection with the closely joined

561 562 BULLETIN OF MARINE SCIENCE, YOLo 47, NO.2. 1990

OLFACTORY LOBE

1---4 lmm Argyropelecus hemigymnus male female 34 mm SL 33 mm SL

Figure I. Morphology of the olfactory organs in A. hemigymnus. olfactory lobes appears as a single bundle that splits into two fibers distally about midway to the nasal rosettes. Both sexes in the two species have paired ovoid nasal rosettes supported by bony olfactory capsules and surrounded by a nasal membrane with two exterior openings. The olfactory epithelium is folded into a number of lamellae arranged in two rows along the major axis which lies at about a 45° angle to the long axis of the body. Lamellar cross sectional area increases posteriorly and in macrosmatic males, distal lamellae are greatly expanded and surround the posterior opening of the nasal membrane, presumably in alignment with water flow along the major rosette axis (Fig. I). The nature and degree of the dimorphic condition is expressed quantitatively in Table I and Figure 2. The number of lamellae in the nasal epithelium, the rosette cross sectional area and olfactory tract diameter are appreciably larger in

Table 1. Ranges of meristic and morphometric measurements of the olfactory organs of adult A. hemigymnus and V. tripunctulatus

Species A. hemigymnus V. tripunctulatus Characteristic Male Female Male Female

Standard length (mm) 28-34 30-34 23-27 25-28 Number lamellae 19-23 1-14 17-20 11-12 Rosette area (mm2) 1.0-1.7 0.~.7 0.5-0.7 0.2-0.4 Olfactory nerve diameter (mm) 0.2-0.3 <0.1 0.1-0.2 <0.1 Numbers examined 7 6 5 6 NOTES 563

15 Indeterminate Q) • 0 0 Female 12 6- 6.6. Q) Male E ~ 6- 6- 6- 0 6- 6- 6- ..J 9 6- 6- 6- '+- 0 6-• 0 0 L Q) 6 «) 0 om 0 CD ..0 •• E • :::::l 3 • Z • 0 ,. . 10 15 20 25 30 35 40 Standard Length (mm)

Figure 2. Number of lamellae on one row of nasal rosette versus standard length for male, female, and sex indeterminate specimens of A. hemigymnus. males than females of both species. Also evident in Figure 1 is a distinct size difference in olfactory lobe dimensions. The cross sectional area of individual lamellae is greater in males. For instance, in A. hemigymnus the length of large distal lamellae in males of 33-34 mm SL often exceeded I mm, while lamellar length never exceeded 0.6 mm in the largest female examined (39 mm SL). The correlation of dimorphism with sexual maturity for A. hemigymnus is evident in Figure 2. Small individuals whose sex could not be determined (filled circles in the figure) have few lamellae. As maturation proceeds more lamellae develop and dimorphism becomes more pronounced. By about 22 mm SL most individuals appear to have functional gonads and dimorphism is clearly evident. The elaboration of the olfactory organs in males is presumed to be indicative of a higher degree of olfactory sensitivity than in females. Significant olfactory development in females of both species suggests a well developed olfactory sense, however, unlike the microsmatic organs in females of bathypelagic species. This is consistent with Marshall's (1967) observation of well developed olfactory organs in both sexes of most mesopelagic fishes. It is known that many fishes possess highly sensitive olfactory systems with detection thresholds of solute concentrations on the of 10-13 M or less (Hara, 1982; Sorensen et al., 1987). Chemical substances are known to alter behavior patterns in fishes and pheromones are involved in sexual behavior and chemical communication in many taxonomically diverse species (Liley, 1982; Stacey, 1983; Hara, 1986). Pheromones are now known to have physiological effects on repro- duction and can serve to synchronize male-female spawning readiness (Sorensen et a1., 1987; Du1ka et a1., 1987). Many of these functions are likely involved in the chemical communication systems presumed present in the two species studied here. It is also not known how males locate mates by chemosensory cues or how far and how quickly pheromones released at a point source by a female diffuse out- ward. Pheromone systems can be expected to significantly expand the "perception 564 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.2, 1990

Table 2, Demographic data for populations of A, hemigymnus and V. tripunctulatus in the eastern GulfofMexico. Data source: (1) Hopkins and Baird, 1985; (2) Hopkins and Lancraft, 1984; (3) Fisher, 1980; (4) Hopkins and Baird, 1981

Demographic parameter A. hemigymnus V. tripuncw/alus

Stock size (m -2) 0.05 (1) -0.Q7 (2) Sex ratio (% female) 63 (3) 58 (3) Length at maturity (mm SL) 22 (3) 23M/25F(3) Percent adults 36 (1) 70 (4) N mature males (x 103 km-2) 7 20 Average male density (x 10-6 m-3) 30 70

envelope" around a female thereby increasing the distance that she can be detected by a searching male. Reproduction. -Several authors have inferred a one year (or less) cycle for both species in subtropical environments. Baird and Hopkins (1981) based their ar- gument on resources and growth efficiency for V. tripunctulatus. Howell and Krueger (1987) and Kawaguchi and Mauchline (1987) based theirs on seasonal length-frequency data. Ridge-Cooney (1987) counted daily increments on otoliths of A, hemigymnus. Fisher (1980) and Howell and Krueger (1987) indicate that A. hemigymnus and V. tripunctulatus are "non-synchronous" spawners and routinely found three to four size classes of eggs in the ovaries of mature females. This suggests egg release in batches over an extended time period. Recent studies by Lisovenko and Prut'ko (1987) on the myctophid Diaphus suborbitalis, a non-synchronous spawner, imply that females of that species de- velop a clutch of eggs as often as every ten days over an extended breeding season. More clutches of eggs are eventually spawned than could be distinguished in the ovary at anyone time. The time window in which a spawning-ready female must find a mate for pelagic spawners may also be very narrow. Eggs are hydrated on the order of 6-12 h before spawning in the anchovy Engraulis mordax (Hunter and Leong, 1981) and apparently in Diaphus suborbitalis as well (Lisovenko and Prut'ko, 1987). Continuous non-synchronous spawning can greatly increase the reproductive potential of a species by allowing more egg production at a small body size. To illustrate, for A. hemigymnus we assume a mean batch fecundity per ovary pair of 200 (Fisher, 1980; Kawaguchi and Mauchline, 1987), sexual maturity at 8 months, 10 days development time per clutch and a 1 year life cycle. This yields an estimate oflifetime fecundity per female of about 2,400, an order of magnitude higher than the batch fecundities reported in the literature. Both species clearly produce multiple clutches and additional study is required to refine this crude estimate oflifetime fecundity. By diverting resources to reproduction at a younger, less resource expensive stage of somatic growth these diminutive species are able to successfully exploit a depauperate (and small sized) resource field that places severe limitations on somatic growth (Hopkins and Baird, 1981). Note that in both species a high percentage of the estimated net caught standing crop consists of adult sized individuals (Table 2). Demography. -Demographic data on both species were obtained from a series of recent studies centered around 27°N and 86°W in the eastern Gulf of Mexico. These data appear in Table 2 and are based on discrete depth sampling with NOTES 565 midwater trawls. From estimates of net caught standing stock, sex ratios, and size distributions, one can calculate the percent adults and number of mature males per unit area in the population (samples were taken from March to October, the warmer months). Hopkins and Baird (1981; 1985) indicate that during the day 95% of the population of A. hemigymnus is found over a 200-m depth range (325- 525 m) while for V. tripunctulatus the range was 300 m (275-575 m). Marked diel migration was not evident, though the distributions were slightly shallower at night. While there was some tendency for larger individuals to be found deeper, adult size classes were found throughout the vertical range of occurrence. Assum- ing that males are randomly scattered over the depth range of occurrence one can derive a first approximation for the average density of males over that depth range (Table 2). (Badcock and Merrett, 1976 noted that the distribution of ripe males to ripe females differed somewhat between different strata and clearly vertical distribution patterns need refinement.) The mate location problem can now be explored in relation to the demography and reproductive strategy in the two species. We estimate that there are about 11,000 females of A. hemigymnus per km2 of ocean in the eastern Gulf. If each female spawns a clutch of eggs over a 24-h period, there are 10 days between spawning bouts and reproduction is randomly distributed throughout the year, then on the average one in ten females enters spawning readiness on any given day (or about 1,100 fish). The critical dimension then is mean male-female dis- tance. Assuming random dispersal over the depth range of abundance for A. hemigymnus the average distance between individuals would be on the order of 22-25 m (18-20 for V. tripunctulatus). For humans, at body length 2 m, this distance on a relative scale would be on the order of 1.7 km or about a mile. Note, however, that spawning-ready females are quite sparse (50-60 m apart). Both species studied here have large pan-oceanic distributions, are common inhabitants of large subtropical gyre systems (Baird, 1971; Clarke, 1974; Boro- dulina, 1978; Howell and Krueger, 1987) and the demographic patterns of these populations undoubtedly differ in various degrees from the first order approxi- mations made here. Nonetheless, over a broad geographic range reproductive mode (non-synchrony, long breeding season, limited spawning time window), population structure (low density, high percent adults in standing crop) and habitat (low light intensities, sparse resources) interact to place a selective premium on an effective, energy efficient system of mate location. Chemical communication, one such option, is apparently an essential element in the reproductive repertoire of both A. hemigymnus and V. tripunctulatus.

ACKNOWLEDGMENTS

Thanks to K. Hartell (MCZ) and J. E. Craddock (WHOn for providing material for this study and J. Haley (WPI) for graphics and illustration. We acknowledge T. L. Hopkins and the students of the midwater ecology program at the University of South Florida for their helpful suggestions. This work was partially supported by a grant from Rodney Hunt Corporation and contracts DES 75-03845 and OCE 75-03845 from the National Science Foundation.

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DATEACCEPTED: January 25, 1990.

ADDRESSES: (ReB) Department of Biology and Biotechnology, Worcester Polytechnic Institute, Worcester, Massachusetts 01609; (GYJ) Department of Mechanical Engineering, Worcester Polytechnic Institute, Worcester, Massachusetts 01609; (EEG) RMS Technologies. Marlton, New Jersey 08053.