Northeast Gulf Science Volume 12 Article 3 Number 2 Number 2

10-1992 An Investigation of the Reproductive Mode of the Pinfish, Lagodon rhomboides Linnaeus (Osteichthyes: ) Richard P. Cody Louisiana State University

Stephen A. Bortone University of West Florida

DOI: 10.18785/negs.1202.03 Follow this and additional works at: https://aquila.usm.edu/goms

Recommended Citation Cody, R. P. and S. A. Bortone. 1992. An Investigation of the Reproductive Mode of the Pinfish, Lagodon rhomboides Linnaeus (Osteichthyes: Sparidae). Northeast Gulf Science 12 (2). Retrieved from https://aquila.usm.edu/goms/vol12/iss2/3

This Article is brought to you for free and open access by The Aquila Digital Community. It has been accepted for inclusion in Gulf of Mexico Science by an authorized editor of The Aquila Digital Community. For more information, please contact [email protected]. Cody and Bortone: An Investigation of the Reproductive Mode of the Pinfish, Lagodon Northeast Gulf Science Vol. 12, No. 2 October 1992 p. 99·110 AN INVESTIGATION OF THE REPRODUCTIVE MODE OF THE PINFISH, Lagodon rhomboides Linnaeus (Osteichthys: Sparidae)

Richard P. Cody Museum of Natural Science Louisiana State University Baton Rouge, LA 70803 and Stephen A. Bortone Dep

ABSTRACT: The majority of spa rids studied have shown evidence of hermaphroditism. The reproductive mode of the pinfish was investigated using museum and field collections of pinfish (n =974) distributed in size from 13 to 276 mm SL. The observed female to male sex ratio of 1.3:1.0 was not ~niflcantly different from uniformity. Males were distributee! in size from 63 to 252 mm SL (x = 127 mm); females were distributed from 57 to 276 mm (x = 119 mm). Individuals of undetermined sex occurred to 178 mm SL. Although the mean lengths of the sexes differed significantly, overlapping length·frequency distributions suggested gonochoristic development. Gonadosomatic indices (GSI) indicated spawning occurs between October and March in pinfish. Contrary to the predominance of hermaphroditism in sparids, histological investigation of the gonads of 106 specimens supported gonochorism as the reproductive mode in pinfish.

The diversity of reproductive Mehl, 1973; Malo-Michelle, 1977; Coetzee, "strategies" among sparids (Table 1) is 1982; Waltz et al., 1982; Garratt, 1986). In unrivalled by any other perciform family general, testicular and ovarian portions with the possible exception of the are completely separated by connective serranids (Smith, 1975). Types of sparid tissue. This germinal configuration has reproductive modes include protandry, been referred to by Sadovy and Shapiro protogyny, non-functional herma­ (1987) as a "delimited" type. In phroditism, and gonochorism. Evidence protogynous individuals, testicul~r tissue of simultaneous hermaphroditism is becomes enlarged and envelops limited to a few isolated cases within degenerating ovarian tissue which populations (Waltz et al., 1982; Cody, remains as a narrow strip on the medial 1989). Of 43 species examined to date, surface of the gonad. Remnants of over 80% show evidence of sex change. testicular tissue in protandrous Although the pinfish has been shown to individuals may be detected as be an important component species of longitudinal flaps positioned laterally on estuarine communities of the eastern the ovary (D' Ancona, 1949a). The United States and the Gulf of Mexico "delimited" type configuration ·of the (Stoner, 1980) information on its reproduc­ sparid ovotestis has allowed sex­ tive mode is sparse (Muncy, 1984). changers to be detected in many cases Morphological descriptions of the by gross visual inspection of the gonad sparid ovotestis indicate consistency in rather than histological examination of form (Kinoshita, 1936, 1939; D'Ancona, gonadal structure (Penrith, 1972). 1941, 1949a; Pasquali, 1941; Lissia-Frau It has been established that most 1966, 1968; Lissia-Frau and Casu, 1973; sparids are hermaphroditic and as such, 99 Published by The Aquila Digital Community, 1991 1 Gulf of Mexico Science, Vol. 12 [1991], No. 2, Art. 3 100 Cody, R. P. and S. A. Bartone the failure to uncover evidence of hook-and-line and beach seine specimens hermaphroditism in a population should were collected from the Northwest not be confused with the failure to accept of Florida. Larger pinfish were acquired hermaphroditism (or gonochorism) as a from day-cruise headboats and longliners valid reproductive "strategy". Care should operating 17-25 km offshore from Panama be taken with methodology so that if sex­ City and Destin, Florida. These changers are present in a population in specimens were fixed in 10% Formalin low frequencies, they are likely to be for up to 72 hours and subsequently detected. Caldwell (1957) believed that a transferred to 40% Isopropanol for size or sex-associated change in body storage. shape may occur in pinfish but did not Standard length (SL) and body depth demonstrate such a relationship. Such a (BD) were measured to the nearest mm. change in body shape may be associated Body weight was measured in grams and with sex-change. Winstead (1977) examin­ gonad weight was measured to the ed the possible homology between cyst nearest mg. Sex was determined by gross epithelial cells in pinfish testes and inspection of the gonad. Gonads were mammalian Sertoli cells. Although not classified according to the criteria of alluded to in the study, isolated early Orange (1961): stage 1S- gonads elongate stage oocyte-like cells were found in pin­ and ribbonlike in appearance, sex, not fish testes (Winstead, pers. comm.). discernible by gross inspection; stage 1 Winstead's and Caldwell's observations -elongate, sex recognizable by color and in addition to the predominance of textural differences; stage 2 - slightly hermaphroditism as a reproductive mode enlarged, ova not visible to the naked eye in sparids were considered sufficient correspohding to an early maturation criteria to warrant examination of sex­ phase; stage 3 - late maturation phase, change as a possible reproductive mode individual ova distinguishable; stage 4 - in pinfish. The hypothesis of ripe ova loose from follicles; stage 5 - hermaphroditism in the pinfish was undergoing atresia, resorption evident. tested using size distribution of the sexes Entire gonads were extracted from and sex ratio data in addition to 537 individuals and stored in 40% macrocscopic and histological examina­ isopropanol. Subsamples of the extracted tion of gonadal structure and maturation. gonads for each month were examined The establishment of standardized histologically. A base sample of 72 criteria to detect hermaphroditism was gonads consisting of three ovaries and also an objective of this study. three testes representing small (mean SL = 87 mm), medium (mean SL = 115 mm), MATERIALS AND METHODS and large (mean SL = 145 mm) individuals from each month was Specimens were obtained from supplemented with additional tissue, catalogued collections of the University comprised of 34 gonads from months of South Alabama, Mobile, Alabama; the preceding and following the peak Florida State Museum, University of spawning period. An estimate of Florida, Gainesville, Florida; University of spawning period was made from calcula­ West Florida Ichthyology Collection, tion of gonadal index (GSI), where GSI = Pensacola, Florida; and from uncataloged (wet gonadal weight I wet body weight) X 2 collections of the Department of 10 • Descriptive terminology for oogonial Biological Sciences, Florida State Univer­ and spermatogonial development sity, Tallahassee, Florida. In addition, followed Hayashi (1972), Coetzee (1983), https://aquila.usm.edu/goms/vol12/iss2/3 2 DOI: 10.18785/negs.1202.03 Cody and Bortone: An Investigation of the Reproductive Mode of the Pinfish, Lagodon

Reproductive mode of pinfish 101 and Selman and Wallace (1986). no significant difference was found Transverse sections 6J.im • 1OJ.im were between females (SUBD = 2.44) and taken from anterior, medial, and posterior males (SLIBD = 2.47), immature portions of the gonad. Entire gonads from specimens (SL BD = 2.37) were found 10 specimens were serially sectioned. In to differ significantly from both males and larger individuals where serial sectioning females using a Student-Newman-Keuls of the gonad was not practical, 5 mm · 7 test (a = 0.05). mm cubes were removed and embedded Poor fixation and preservation of for sectioning. Dehydration and infiltra­ some of the specimens made thorough tion followed criteria described by analysis of gross gonadal morphology Humason (1972) for paraffin embedding. and development difficult. For this Sections were progressively stained in reason, descriptions of gonadal hematoxylin (gills formulation 2) and morphology and development 't:'er13 only counterstained in eosin-y. Statistical briefly summarized. In appearance, the analysis was performed using SAS pinfish gonad was elongate and bilobed, (Helwig and Council, 1979). positioned dorsal to the intestine, with each lobe attached anteriorly to the body RESULTS wall. The lobes united posteriorly, anterior to the genital opening. In immature A total of 974 specimens were specimens, the gonad was thread-like. In distributed from 13 mm to 276 mm SL. developing females it was larger and Females comprised 31% (n = 304) and thicker than in similar-sized males, in males 24% (n = 233) whereas immatures which the testes were thin and ribbon­ accounted for almost 45% (n = 437) of like. Vascularization was also more evi­ the total sample. Females and males dent in the ovary. Spent ovaries were were distributed from 57 mm to 276 mm sack-like and grey in preserved and 63 mm to 252 mm SL respectively specimens. Immature (stage 1S) gonads (Figure 1). Although the size distributions were encountered up to a size of 178 mm of the sexes overlapped considerably SL in 44.9% of the sample. Most (with the exception of immature specimens attaining a size of 100 mm SL specimens), a one-way ANOVA revealed showed macroscopic evidence of a significant difference in means (F gonadal maturation (stage 1). Females =303.7, df = 2, p <0.0001). A Student· sampled from March to September Newman-Keuls test grouped immatures, generally had stage 1 and stage 2 gonads. females and males separately (a = 0.05). Stage 3 gonads were present only in The mean SL of females was 119 mm small numbers in females from late July compared to a mean SL of 127 mm for through February. Individuals having males. A female to male sex ratio of 1.3:1 stage 3 and stage 4 gonads were com­ was not significantly different from mon in collections from October to uniformity (Chi Sq. = 4.69, df = 1, NS). March. Females with stage 4 gonads A comparison of SUBD ratios was were collected from December through made to look for sex-related "shape" April, but were uncommon. differences. A one-way ANOVA also Gonadosomatic index (GSI) data tested differences in the mean ratio of SL were summarized for the sexes in Figure to BD between males, females, and 2. Noticeable peaks in GSI occurred for immatures. Significant differences both males and females in the months of between the three "classes" were found February. Variance was relatively high for (F = 21.03, df = 2, p =0.0001). Although the months of October, December,

Published by The Aquila Digital Community, 1991 3 Gulf of Mexico Science, Vol. 12 [1991], No. 2, Art. 3 102 Cody, R. P. and S. A. Bartone

60,_-~~_L_L_i~ __L_L__L_~~_L~_j __L_L_L_i_j__L_L_i~~L_L_~j_~-~

40

20

20

40

SL (mm) Figure 1. Length frequency distribution of male and female pinfish, measured as standard length (SL).

Female 2.5 February and March in females while in (81) males the months with the highest degree

(22) of variance were December, March, and 1.5 iii (]5) (12) May. Low variability in GSI values obtained for the months: April-september

(J) suggested spawning occurred from October through March in pinfish -. 5 sampled. J A s 0 D J F M A M J " Histological examination of pinfish Male 2.5 gonads supported macroscopic descrip­ tions and GSI results. The pinfish testis (18) (7}) was comprised of a complex network of :21.5 seminiferous tubules which emptied into (4) vasa efferentia (Figure 3). Developing males from all months showed a limited degree of spermatogenesis (Figure 4). Ripe testis determined by gross examina­ AS ONDJFMAMJ Month tion displayed little spermatogenic Figure 2. Monthly progression of pin fish ovarian activity; the crypts being either full of and testicular condition based on mean spematozoa, or partially evacuated gonadosomatic index (GSI). Error bars represent (Figure 5). The pinfish ovary was found to 1 standard deviation, number of specimens are shown in parenthesis. consist of numerous ovigerous lamellae https://aquila.usm.edu/goms/vol12/iss2/3 4 DOI: 10.18785/negs.1202.03 Cody and Bortone: An Investigation of the Reproductive Mode of the Pinfish, Lagodon Reproductive mode of pinfish 103

Figures 3·6. 3. Lobular conformation of testis, showing seminiferous tubules leading to sperm duct via the vasa efferentia, scale = 1 mm. 4. Cyst configuration of developing testis showing spermatozoa in lumina of tubules, scale = 0.05 mm. 5. Reduction of spermatogenic activity in ripe testis, scale = 0.05 mm. 6. Early phase oocytes in developing ovary, scale = 0.5 mm. B = blood vessel, G1 = gonial cell, L = ovarian cavity, V = ovigerous lamellae, S = spermatozoa, VE = vasa efferentia, W = ovarian wall.

Published by The Aquila Digital Community, 1991 5 104 Cody, R. P. and S. A. BertoneGulf of Mexico Science, Vol. 12 [1991], No. 2, Art. 3 projecting inward to the ovarian lumen with neither sex dominating the larger or from the tunica albuginea (Figure 6). The smaller size classes. A slightly skewed ovarian lumen continued posteriorly as sex ratio of 1.3 females to each male did the oviduct which was also recognizable not represent a significant departure from in individuals determined to be immature the hypothesized uniformity. Sex ratios as by gross examination of the gonad. low as 2:1 have been encountered for Developing ovaries contained mostly hermaphroditic species (Penrith, 1972) early phase oocytes in which the nucleoli and as high as 6:1 for gonochoristic lined the periphery of the nucleus (Figure species (Dooley, 1978). The unreliability of 7). Primary yolk-vesicle oocytes were of sex ratios as indicators of noticeably larger than perinuclear stage hermaphroditism was shown by Erickson oocytes. There was, however, a wide and Grossman (1986) for the range in cell diameter depending on the gonochoristic Atlantic tilefish, degree of yolk-vesicle formation (Figure Lopholatilis chamaeleonticeps despite 8). In early yolk-vesicle formation, two the dominance of smaller size classes by distinct bands of yolk-vesicles were females. Sex ratio may also vary visible; a circum-nuclear band of large considerably from year to year. Manooch vesicles and a row at the cell periphery. (1976) found that ratio of female to male Secondary yolk-vesicle oocytes were red porgies varied from 1.9:1 to 3.3:1 characterized by a loss of the banding within a three year period for fish caught pattern found in primary yolk-vesicles and in North Carolina. Inaccurate sex ratio also by the thickening of the zona radiata data from population samples may be (Figure 8). Tertiary yolk-vesicle oocytes produced as a result of segregation of the were recognizable by the peripheral posi­ size classes and sexes due to respective tion of the nucleus, consolidation of habitat preferences. Larger pinfish in­ secondary yolk globules, and a large lipid habit deeper water (Hastings et al., 1976) droplet replacing the migratory nucleus. and in colder months there is a general The large central primary yolk was offshore migration as inferred from the obscured. Secondary yolk-vesicle absence of larger size classes from coalescence was clear (Figure 9). shallow water (Orth and Heck, 1980; Although maturing oocytes were Nelson, 1979; Stoner and Livingston, observed, histological sections were '1984). As pinfish sampled were collected generally of poor quality. Of 52 ovaries by a variety of methods over a number of examined, atretic oocytes were limited to years, and from a variety of habitats the ripe and maturing individuals (stage 4 and effects of size-related (and sex-related, if stage 5 ovaries) occurring from December present) habitat preferences should have through February (Figure 10). been reduced. The sex ratio may be closer to uniformity as immature ovaries were DISCUSSION easier to recognize than immature testes. It is possible that discrete Features of population structure morphological differences may arise in such as sex ratios and size differences of fish undergoing sex change (or fish that males and females have been widely used have already changed sex) due to to detect hermaphroditism in teleost physiological adjustments associated (Sadovy and Shapiro, '1 987). Female with gonadal (ovotesticular) development and male pinfish differed significantly in similar to changes which occur in some mean size, but, their respective size developing or maturing individuals of a distributions overlapped considerably gonochoristic species. It was https://aquila.usm.edu/goms/vol12/iss2/3 6 DOI: 10.18785/negs.1202.03 Cody and Bortone: An Investigation of the Reproductive Mode of the Pinfish, Lagodon Reproductive rnode of pinfish 105

Figures 7·10. 7. Ovigerous lamellae of developing ovary, perinuclear oocytes with migrating nucleolus at periphery of nucleus, scale = 0.05 mm. 8. Primary and secondary yolk vesicles (note double band of yolk globules in primary vesicle stage which is lost in secondary yolk vesicles), scale = 0.2 mm. 9. Late maturation phase containing predominantly tertiary yolk vesicles (nucleus has migrated to periphery of cell, scale = 0.2 mm. 10. Atretic oocytes (type-c) in ripe ovary, scale = 0.2 mm. L = ovarian lumen, E = germinal epithelium, G = zona granulosa, N = nucleus, 02 = secondary oocyte, 03 = late perinuclear oocyte, PV = primary yolk vesicle, R = zona radiata, SV = secondary yolk vesicle, TV = tertiary yolk vesicle, Y = secondary yolk globules,.

Published by The Aquila Digital Community, 1991 7 Gulf of Mexico Science, Vol. 12 [1991], No. 2, Art. 3 106 Cody, R. P. and S. A. Bortone hypothesized here that individuals taken to avoid "unnecessary" or undergoing sex-change could account for redundant histology. The technique of us­ suspected differences in pinfish shape. In ing GSI data to identify the times of the general, teleost growth is allometric so year when sex change (if present) was SUBD would not be expected to remain most likely to occur we believe is sound. constant (Bookstein, et al. 1985). As The months just prior to spawning, and SUBD was significiantly smaller for im­ directly after spawning (when the gonad matures than males and/or females, this undergoes the most amount of physical suggests that variation in pinfish shape and physiological change) were more is growth-related rather than sex-related. heavily sampled. Large cells resembling Measurement error must also be early stage oocytes were observed occa­ acknowledged as a potential influence. sionally in testes but these may have As a "ratio" was used to examine body been undifferentiated gonia. shape, one may expect greater error In conclusion, pinfish gonadal struc­ among the smaller size classes. The ture was consistent with primary mean size of the immature pinfish was 67 gonochorism being the dominant or ex­ mm. We would have less confidence in pressed reproductive mode. It should be results if smaller specimens were used to noted that this mode of reproduction measure SUBD. It is also possible that represented an exception to the differences in "body shape" were not predominance of hermaphroditism within reflected in the the use of SUBD. Results the family. Atz (1964) indicated that the of a discriminant function analysis have sexual history of a single sparid had yet shown that at least 14 morphometric to be described adequately, and this is variables were required before separation reflected in more recent conflicting of the sexes was achieved with 95% con­ evidence on sparid reproductive modes fidence and no other class representing (Table 1). The lack of consistency in sex changers was detected (Cody, 1989). cri~eria used to determine the reproduc­ GSI results supported the tive modes of species (added to confu­ "suspected" winter-spawning of pinfish. sion existing in sparid nomenclature) has A reduction in the number of larger pin­ made assessment of the diversity of fish observed in shallow waters during sparid reproductive modes difficult. winter months (Nelson, 1979; Orth and However, an increasing body of Heck, 1980; Stoner and Livingston, 1984) knowledge of reproductive strategies is has been attributed to prespawning becoming available so that interspecific migration and avoidance of temperature comparisons may provide some explana­ fluctuations associated with shallow tion for the apparant preponderance of water (Gunter, 1945; Joseph and Yerger, hermaphroditism relative to gonochorism 1956; Moe and Martin, 1965; Hansen, in sparids. It will be interesting to see if 1970). Largest GSI values were found in future studies can relate differences in October, December, February and March reproductive mode to ecology, behavior, in females and December and February and phylogeny. for males suggesting a protracted ­ ing period. However, as samples con­ ACKNOWLEDGMENTS sisted of fish from a number of years and from a number of localities results may This study was completed in partial reflect year to year variation. fulfillment of the degree of M.S. at the A major concern of this study was University of West Florida. I thank C. L. effective histological sampling. Care was Gilbert, A. L. Shipp, W. P. Davis, C. N. https://aquila.usm.edu/goms/vol12/iss2/3 8 DOI: 10.18785/negs.1202.03 Cody and Bortone: An Investigation of the Reproductive Mode of the Pinfish, Lagodon Reproductive mode of pinfish 107

Table 1. Summary of sparid reproductive modes: + refers to conflicting evidence on reproductive mode, and * refers to incomplete or inconclusive evidence.

Species Reprod. Mode Reference Acanthopagrus australis Protandry Pollock, 1985 Acanthopagrus bifasciatus Gonochorism Druzhenin, 1975 Acanthopagrus cuvieri Rudimentary Hussain et at., 1981 Archosargus probatocephalus Rudimentary Render & Wilson, In press Boops boops Protogyny+ Lissia·Frau, 1968 Boops sa/pa (Box salpa) Protandry+ Lissia·Frau, 1966; Joubert, 1981 Boopsoidea inornata Gonochorism Penrith, 1972 Calamus leucosteus Protogyny Waltz et al., 1982 Calamus proridens Protogyny* Cody, 1989 Cheimerius nufar Rudimentary Coetzee, 1982 Chrysoblephus cristiceps Protogyny Robinson, 1976 Gonochorism Penrith, 1972 Protogyny Penrith, 1972 Chrysoblephus punic/us Protandry Garratt, 1986 Chrysophrys major Protogyny+ Huang et al., 1974 Dentex dentex Gonochorism D'Ancona, 1949b Dentex gibbosus Protandry Bonnet, 1969 Diplodus annularis (Sargus annularis) Protandry* + D'Ancona, 1949a; Salekhova, 1961 Diplodus puntazzo (Puntazzo puntazzo) Rudimentary+ D'Ancona, 1949b; Faranda et al., 1985 Diplodus vulgaris (Sargus vulgaris) Rudimentary+ D'Ancona, 1949b Lagodon rhomboides Gonochorism Cody, Present study Lithognathus lithognathus Rudimentary Mehl, 1973 Oblada me/anura Rudimentary+ D'Ancona, 1949b Pachymetopon grande Gonochorism Penrith, 1972 Page/Ius acarne Protandry* Reinboth, 1962 Page/Ius centrodontus Functional Williamson, 1911 Page/Ius erythrinus Protogyny D'Ancona, 1949b Page/Ius mormyrus (Lithognathus mormyrus) Protandry+ D'Ancona, 1949b Pagrus auriga Protogyny Alekseev, 1982 Pagrus ehrenberg/ Protogyny Alekseev, 1982 Pagrus orpheus Protogyny Alekseev, 1982 Petrus rupestris Gonochorism Penrith, 1972 Pterogymnus /aniarius Conochorism + Penrith, 1972 Rhabdosarqus g/obiceps Gonochorism Penrith, 1972 Sargus sargus (Dip/odus sargus) Protandry+ Reinboth, 1962 Sparus aries (Acanthopagrus aries) Protandry* Kinoshita, 1939 Sparus auratus (Chrysophrys aurata) Protandry Pasquali, 1941; D'Ancona, 1949b Sparus caeru/ostictus Protogyny Bonnet, 1969 Sparus latus (Acanthopagrus latus) Protandry* Kinoshita, 1939 Sparus longispinis (My/io macrocephalis) Protandry* Kinoshita, 1936; Okada, 1965 a,b,c, Spondy/iosoma cantharus (Cantharus cantharus) Protogyny Bonnet, 1969 Spondyl/osoma emarginatum Gonochorism Penrith, 1972 Talus tum/frons Protogyny Aoyama, 1955 D'Asaro, and J. J. Luczkovich who provid­ Pagrus orpneus, Pagrus ehrenoergi ed specimens and helpful discussion. A and Pagrus auriga, from West Africa. special thanks is due also, to C. K. Swing J. lchthyol. 22, 85-94. and J. M. Fitzsimons for reviewing early Atz, J. W. 1964. Intersexuality in fishes. In versions of the manuscript. Intersexuality in Vertebrates Including Man. (C. N. Armstrong & A. J. Marshall, LITERATURE CITED eds.), P. 145.-232. New York: Academic Press. Alekseev, F. E. 1982. Hermaphroditism in Aoyama, T.1955. On the hermaphroditism sparid fishes (, Sparidae) 1. of the yellow sea bream, Taius Protogyny in porgies, Pagrus pagrus, tumifrons. Jap. J. lchthyol 4, 119-129.

Published by The Aquila Digital Community, 1991 9 Gulf of Mexico Science, Vol. 12 [1991], No. 2, Art. 3 108 Cody, R. P. and S. A. Bartone Bonnet, M. 1969. Les sparides des cotes Puntazzo puntazzo (Gmelin, 1789) Nord-OuestAfricanes. Revue Trav. lnst. (Pisces, Sparidae) under controlled Pech. marit. 33, 97-116. conditions. Aquaculture 49, 111-123. Bookstein, F. L., Chernoff, B., Elder, R. L., Garratt, P. A. 1986. Protogynous Humphries, Jr., J. M., Smith, G. R., and hermaphroditism in the slinger, R. E. Strauss. 1985. Morphometries in Chrysoblephus punicius (Gilchrist & Evolutionary Biology. Acad. Nat. Sci. Thompson, 1908) (Teleostei: Sparidae). Phila., Special Publ. 15, 277 pp. J. Fish Bioi. 28, 297-306. Caldwell, D. K. 1957. The biology and Gunter, G. 1945. Studies on marine fishes systematics of the pinfish Lagodon of Texas: Publ. lnst. Mar. Sci. Univ. Tex. rhomboides (Linnaeus). Bull. Fla. State 1, 189-307. Mus. Bioi. Sci. 2, 77-173. Hansen, D. 1970. Food, growth, migration, Cody, R. P. 1989. An evaluation of the reproduction, and abundance of pin­ reproductive mode of the pinfish, fish, Lagodon rhomboides, and Lagodon rhomboides (Pisces; Atlantic croaker, Micropogon Sparidae). M. S. Thesis, University of undulatus, near Pensacola, Florida, West Florida, (unpubl.). 53 pp. 1963-1965. Fish. Bull. 68, 135-146. Coetzee, P. S. 1983. Seasonal histological Hastings, R. W., Ogren, L. H., and M. T. and macroscopic changes in the Mabry. 1976. Observations on the fish gonads of Cheimerius nufar fauna associated with offshore (Ehrenberg, 1820) (Sparidae: Pisces). S. platforms in the Northeastern Gulf of Afr. J. Zool. 18, 76-89. Mexico. Fish. Bull. 74, 389-401. D'Ancona, U. 1949a. Ermafroditismo ed Hayashi, I. 1972. On the.ovarian matura­ intersessualita nei Teleostei. Experien­ tion of the Japanese sea bass, tia 5, 381-391. Lateolabrax japonicus. Jap. J. lchthyol. _____.1949b. II differenziamento 19, 243-254. della gonade e l'inversione sessuale Helwig, J. T., & Council, K. A. (eds.). 1979. degla Sparidi. Arch, Oceanogr. Limnol. SAS user's guide. SAS lnst., Inc., North 6, 97-163. Carolina. 494 pp. Dooley, J. K. 1978. Systematics and Huang, C.-C., Lo, C.-F., and f5.·H. Chang. biology of the tilefishes (Perciformes: 1974. Sex reversal in one sparid fish, Branchiostegidae and Malacanthidae) Chrysophrys major (Perciformes, with descriptions of two new species. Sparidae). Bull. lnst. Zool., Academia NOAA Technical Report NMFS, Sinica 13, 55-60. Circular 441. Humason, G. L. (1972). Tissue Druzhenin, A. D. 1975. Some data on Techniques. W. H. Freeman and Co., sparid fishes, family Sparidae of the San Fransisco. 641 pp. Gulf of Aden region. J. lchthyol. 15, Hussain, N., Akatsu, S. and C. EI-Zahr. 531-541. 1981. Spawning, egg, and early larval Erickson, L. E., and G. D. Grossman. 1986. development, and growth of Reproductive demography of tilefish Acanthopagrus cuvieri (Sparidae). from the South Atlantic Bight with a Aquaculture 22, 125-136. test for the presence of protogynous Joseph, E. B., and R. W. Yerger 1956. The hermaphroditism Trans. Amer. Fish. fishes of Alligator Harbor, Florida, with Soc. 115, 279-285. notes on th~ir natural history. Fla. Sta. Faranda, F., Cavaliere, A., Lo Paro, G., Univ. Stud. 22, 111-156. Manganaro, A., and A. Mazzola. 1985. Joubert, C. S. W. 1981. Aspects of the Preliminary studies on reproduction of biology of species of inshore reef https://aquila.usm.edu/goms/vol12/iss2/3 10 DOI: 10.18785/negs.1202.03 Cody and Bortone: An Investigation of the Reproductive Mode of the Pinfish, Lagodon Reproductive mode of pinfish 109

fishes on the Natal coast, South Africa. pinfish. U. S. Fish Wildl. Serv. Invest. Rep. Oceanogr. Res. lnst. 51, FWS/OBS-82/11.26. U.S. Army Corps of 1-16. Engineers, TR EL-82-4. 18 pp. Kinoshita, Y. 1936. On the conversion of Nelson, W. G. 1979. An analysis of sex in Sparus /ongispinus (Temminck structural pattern in an eelgrass and Schlegel), (Teleostei). J. Sci. (Zostera marina) amphipod communi­ Hiroshima Univ., B1, 4(5/7). 69-79. ty. J. Exp. Mar. Bioi. Ecol. 39, 231-264. Kinoshita, Y. 1939. Studies on the Okada, Y. K. 1965a. Bisexuality in sparid sexuality of genus Sparus (Teleostei). fishes. I. Origin of bisexual gonads in J. Sci. Hiroshima Univ., B1, 7(2), 25-37. Mylio macrocephalus. Proc. Jap. Acad. Lissia-Frau, A. M. 1966. Recerche sur 41' 294-299. differenziamento sessuale di Boops _____.1965b. Bisexuality in sparid salpa (L.) (Teleostei, Sparidae). Atti fishes. II. Sex segregation in Mylio Accad. Gioenia Sci. Nat. 18, 165-174. macrocephalus. Proc. Jap. Acad. 41, _____.1968. Recerche sui differen 300-304. ziamento sessuale di Boops boops (L.) _____.1965c. Bisexuality in sparid (Teleostei, Sparidae). Boll. Pesca. fishes. Ill. Sporadic cases of bisexual Piscic. ldrobiol. 21, 9-21. gonads in Chrysophrys majorTemm. et _____,., & Casu, S. 1973. II Differen­ Schl. Proc. Jap. Acad. 41, 471-476. ziamento di Lithognathus mormyrus Orth, R. J., and K. L. Heck, Jr. 1980. (L.) e di Oblada me/anura (L.). Studi Structural components of eelgrass Sassa., 202-220. (Zostera marina) meadows in the lower Malo-Michelle, M. 1977. Contribution a Chesapeake Bay - fishes. Estuaries 3, l'etude histologique de Ia gonade, en 278-288. particulier de l'ovaire, chez Ia saupe, Pasquali, A.1941. Contribute allo studio Boops salpa (D.) (telosteen, Sparidae). dell'ermafroditismo e del differen­ Donnees nouvelles sur son type d'her­ ziamento della gonade nell'orata maphroditisme. lnv. Pesq. 41, 165-183. (Sparus auratus L.). Pubbl. Stn. Zool. Manooch, C. S. 1976. Reproductive cycle, Napoli 18, 282-312. fecundity, and sex ratios of the red Penrith, M. J. 1972. Sex reversal in the porgy, Pagrus pagrus (Pisces: sparid fish Chrysoblephus laticeps. Sparidae) in North Carolina. U. S. Fish. Koedoe 15, 135-139. Bull. 74, 775-781. Pollock, B. R. 1985. The reproductive Mehl, J. A. P. 19873. Ecology, osmoregula­ cycle of the yellowfin bream, Acan­ tion and reproductive biology of the thopgrus australis (Gunther), with par­ white steenbras, Lithognathus ticular reference to protandrous sex in­ lithognathus (Teleostei: Sparidae). version. J. Fish Bioi. 26, 301-311. Zool. Africana 8(2), 157-230. Reinboth, R. 1962. Morphologische und Moe, Jr., M. A. , and G. T. Martin. 1965. Funktionelle Zweigeschlechlichkeit bei Fishes taken in monthly trawl samples Marinen Teleostiern (Serranidae, offshore in Pinellas County, Florida, Sparidae, Centracanthidae, Labridae). with new additions to the fish fauna of Allg. Zool., Jahrb. Physiol. Tiere 69, the Tampa Bay area. Tulane Stud. Zool. 405-480. 12, 129-151. Render, J. H., and C. A. Wilson. rn press. Muncy, R. J. 1984. Species profiles: life Sexuality of the sheepshead histories and environmental Archosargus probatocephalus requirements of coastal fishes and (Teleostei: Sparidae) from the Northern invertebrates (Gulf of Mexico) - Gulf of Mexico.

Published by The Aquila Digital Community, 1991 11 Gulf of Mexico Science, Vol. 12 [1991], No. 2, Art. 3 110 Cody, R. P. and S. A. Bartone Robinson, G. A. 1976. Sex reversal in the dageraad Chyrsoblephus cristiceps (Pisces Sparidae). Koedoe 19, 43-48. Sadovy, Y. and D. Y. Shapiro. 1987. Criteria for the diagnosis of her­ maphroditism in fishes. Copeia, 1987. 135-156. Salekhova, L. P. 1961. Hermaphroditism of annular bream Diplodus annularis (L.). Trudy Sevastopol Bioi. Sta. 14, 257-268. Selman, K., and R. A. Wallace. 1986. Gametogenesis in Fundulus heteroclitus, Amer. Zool. 26, 173-192. Smith, C. L. 1975. The evolution of hermaphroditism in fishes. In Intersex­ uality in the Animal Kingdom (R. Rein­ both, ed.). Heidelberg: Springer-Verlag, pp. 295-310. Stoner, A. W., and R. J. Livingston. 1984. Ontogenetic patterns in diet and feeding morphology in sympatric sparid fishes from meadows. Copeia 1984, 174-187. Waltz, C. W., Roumillat, W. A., and C. A. Wenner. 1982. Biology of the whitebone porgy, Calamus leucosteus, in the South Atlantic Bight. Fish. Bull, 80, 863-87 4. Williamson, H. C. 1911. Report on the reproductive organs of Sparus centrodontus (De Ia Roche); Sparus cantharus (L); Sebastes marinus. Scient. Invest. Fish. Bd. Scotl. 1, 1-35. Winstead, J. T. 1977. Ultrastructure of the Testis of the Pinfish Lagodon rhom­ boides (Sparidae) with emphasis on the Possible Homology between cyst epithelial (CE) cells and mammalian sertoli cells. M. S. Thesis, University of West Florida, (unpubl.). 105 pp. Winstead, J. T. 1987. Department of Biology, University of West Florida, Pensacola, FL 32514.

https://aquila.usm.edu/goms/vol12/iss2/3 12 DOI: 10.18785/negs.1202.03