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From Southern California BACA HOVEY ET AL., REPRODUCTION IN PARALABRAX NEBULIFER CalCOFI Rep., Vol. 43, 2002 THE REPRODUCTIVE PATTERN OF BARRED SAND BASS (PARALABRAX NEBULIFER) FROM SOUTHERN CALIFORNIA CHERYL BACA HOVEY LARRY G. ALLEN TIMOTHY E. HOVEY Department of Biology Department of Biology California Department of Fish and Game California State University, Northridge California State University, Northridge 4949 Viewridge Avenue Northridge, California 91330-8303 Northridge, California 91330-8303 San Diego, California 92123 [email protected] ABSTRACT m during their spawning season. Their eggs and larvae Sea basses of the genus Paralabrax are either gono- are pelagic, drifting in open water, and juveniles appear chores or protogynous hermaphrodites. This study sought in shallow water from late summer to early winter (Love to determine which, if either, reproductive strategy pre- 1991). In this species, 50% of males matured at 219 mm, vails in barred sand bass (Paralabrax nebulifer). A total of and 50% of females matured at 239 mm. Males mature 436 specimens were collected from June 1996 through between the ages of 2 and 4 years and females between April 1997 from seven different locations along the south- the ages of 2 and 5 years (Love et al. 1996). ern California coast. Of these, only two (< 0.1%) tran- The barred sand bass is a warm temperate member sitional individuals were found. All males examined of the family Serranidae (sea basses) and one of the three exhibited testes with a membrane-lined central cavity species of Paralabrax that occur along the southern and a sperm sinus in the gonadal wall; our findings sug- California coast. Many species of the family Serranidae gest that these individuals may have passed through a have specialized reproductive strategies. Some species are female-like juvenile stage prior to maturation. In addi- protogynous hermaphrodites and hence spend the early tion, 52% of the males examined had atretic bodies. part of their lives as females and later change sex to con- However, males and females were equally distributed clude their lives as males. Oda et al. (1993) suggested throughout the age classes collected. Based on all evi- that barred sand bass might be protogynous hermaph- dence, we conclude that barred sand bass in southern rodites based on a relatively small number of specimens California are functional gonochores that possess a latent, (N = 81). They found six specimens that had gonads perhaps ancestral, ability to change sex. containing both ovarian and testicular tissue. Four of these were believed to be active males with primary INTRODUCTION oocytes in the testes. Proliferating testicular tissue was The barred sand bass (Paralabrax nebulifer) is a common found in the remaining two specimens, one of which species in the nearshore marine environment and an im- was an immature individual. This finding led Oda portant part of the marine recreational fishery of south- et al. (1993) to conclude that barred sand bass may be ern California. It ranked second in the number of fish capable of both pre- and post-maturational sex change. taken by sport-fishers in the state in 1989 and remains However, based on the criteria for hermaphroditism es- one of the most frequently caught species (Oliphant 1990). tablished by Sadovy and Shapiro (1987), Oda et al. con- The barred sand bass together with the kelp bass (Paralabrax cluded that there was insufficient evidence to identify clathratus) comprised more than 90% of the general “rock barred sand bass as a protogynous hermaphrodite. Their bass” recreational catch in the first half of the twentieth histological evidence was certainly suggestive of that century (Frey 1971). Barred sand bass range from Santa conclusion. The major weakness of this study was born Cruz, California, south to Magdalena Bay, Baja California out of the relatively small sample size, which made it Sur, including Guadalupe Island (Miller and Lea 1972), impossible to examine sex ratios over size classes and, and occupy a variety of different habitats, including kelp particularly, age classes. We sought to address these short- beds and sand flats on the open coast to inland harbors comings by using a much larger sample and determin- and bays. They are benthic, relatively sedentary fish and ing the age of each specimen. are rarely found more than 3 m above the substrate, Studies on the other two temperate Paralabrax species closely associated with bottom structure and sand (Turner have shown varying results (DeMartini 1987). Kelp bass et al. 1969; Feder et al. 1974; Larson and DeMartini (P. c lathratus) are found in nearshore coastal waters usu- 1984). Barred sand bass are oviparous broadcast batch ally associated with hard substrate and kelp. They have spawners that breed from April to August, with a peak been termed “secondary gonochores,” believed to have in July (Love et al. 1996). They tend to form large breed- evolved from protogynous ancestors and do not change ing aggregations over soft bottom areas at depths of 15–30 sex (Smith and Young 1966). Spotted sand bass (P. mac- 174 BACA HOVEY ET AL., REPRODUCTION IN PARALABRAX NEBULIFER CalCOFI Rep., Vol. 43, 2002 Figure 1. Sampling locations along the southern California coast for barred sand bass (Paralabrax nebulifer) reproductive study. ulatofasciatus) found in harbors and bays (Allen et al. 1995) Huntington Flats, Santa Catalina Island, San Onofre, have specific populations that are protogynous her- Cardiff, and San Diego Bay (fig. 1). Each specimen was maphrodites and others that appear to be gonochoric weighed to the nearest gram, measured to the nearest (Hastings 1989; Hovey and Allen 2000). The presence millimeter standard length, and preliminarily sexed. of protogynous hermaphrodites in P. maculatofasciatus was Gonads were removed, weighed, and preserved in 10% hypothesized to be related to population structure and formalin for later histological examination. mating system at various locations. Gonads were fixed by immersion in Davidson’s solu- Our main objective in this study was to determine tion (20% formaldehyde, 10% glycerin, 30% EtOH, 10% whether protogynous hermaphroditism occurs in barred glacial acetic acid, and 30% deionized water) for two sand bass and, if so, to what extent. To that end, we will weeks then transferred to 70% ethyl alcohol. Cross- present both histological evidence and age structure data sectional tissue samples (4 mm thick) were removed from from a large sample of barred sand bass collected pri- the mid area of each gonad and placed in Tissue Tek tis- marily from breeding aggregations off the coast of south- sue cassettes. Using the Tissue Tek tissue-fixing unit, ern California. cassettes were emersed in a series of increasing concen- Knowledge of the reproductive strategy used by a trations (70%, 80%, 95%, and 100%) of ethyl alcohol species is important for proper management of the fish- with a final emmersion in xylene. The processed tissue ery. Fisheries are managed to protect the species and to was embedded with paraffin (at 56˚C) and placed in a provide sustainable yields. Management strategies as- vacuum infiltrate for 1 h. The surface of the tissue block suming gonochorism may not be appropriate for fish was then exposed and samples were soaked in a deter- populations with protogynous hermaphroditism. Species gent bath for 10–14 days. Samples were sectioned at with the latter may have numerous small females and 6–12µm using an 820 Spencer microtome and mounted fewer larger males rather than equal ratios of males and on slides. The slides were placed in an oven and allowed females by length and age. Such species may require spe- to dry for 7 days at 35˚C. They were then stained using cial protective measures to ensure sufficient numbers of Mayer’s alum hematoxylin and eosin, allowed to dry, and both genders. sealed with cytosol and a cover slip. Gonad morphol- ogy was examined using a compound microscope under METHODS 100–400× power. Initial sex determination was con- A total of 436 specimens were collected by hook and firmed based on the finding of ovarian tissue (females), line from June 1996 through April 1997 along the coast testicular tissue (males), and indeterminate tissue (im- of southern California at Redondo Beach, Long Beach, mature individuals). 175 BACA HOVEY ET AL., REPRODUCTION IN PARALABRAX NEBULIFER CalCOFI Rep., Vol. 43, 2002 TABLE 1 Number, Size, and Sex of Barred Sand Bass (Paralabrax nebulifer) Collected in Reproductive Biology Study, June 1996–April 1997 Size Size Size Size Size Total no. range No. of range No. of range No. of range No. of range Location specimens (mm) males (mm) Females (mm) Immatures (mm) transitionals (mm) Cardiff 80 170–310 46 200–290 33 170–310 1 183 0 Catalina 18 158–395 11 158–395 6 171–300 1 178 0 Huntington Flats 233 191–362 106 191–322 127 198–362 0 1 273 Long Beach 4 202–328 3 202–297 1 328 0 0 Redondo 6 250–405 5 250–405 1 285 0 0 San Diego 51 78–335 17 121–308 12 169–335 22 78–201 1 306 San Onofre 44 155–460 20 230–460 19 230–375 5 155–190 0 Total 436 78–460 208 121–460 199 169–375 29 78–201 2 273–306 Potential hermaphroditism was diagnosed following the criteria outlined in Sadovy and Shapiro (1997). The following features were considered strongly indicative of protogynous hermaphroditism: (1) transitional individ- uals; (2) atretic bodies in stages 1, 2, or 3 of oocytic atre- sia within the testes; (3) a membrane line central cavity in the testes; and (4) sperm sinuses in the gonadal wall. A fifth feature, population structure, can also add sup- port to a diagnosis of hermaphroditism, if indicated. We examined all samples to determine the presence of any of these features.
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