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THE OF THE PROTOGYNOUS HERMAPHRODITE PIMELOMETOPONPULCHRUM (PISCES: LABRIDAE)

ROBERT R. W ARNER1

ABSTRACT

Pimelometopon pulchrum, , a labrid of the eastern Pacific Ocean, was collected the year round at Catalina Island, Calif., and comparative material was taken at Guadalupe Island, Mexico. Individuals at Guadalupe were dwarfed relative to those at Catalina. Pimelometopon pulchrum is a protogynous hermaphrodite, the ovarian elements undergoing massive degeneration as sperma• togenic crypts proliferate in the of transitional individuals. Sexual changes occur between breeding seasons. Individuals from both populations mature as at age four; most of those at Catalina function as females for 4 yr and then change , at a length of around 310 mm. Sexual transformation occurs earlier on the average at Guadalupe; most individuals are male by age seven. In both populations, more rapidly growing apparently change sex sooner than other individuals of the same age, and fishes that grow slowly may not change sex at all. Spawning appears to occur in July, August, and September in the Catalina population. Individuals probably several times in a breeding season. The weight of active, prespawning increases at a rate approximately propor• tional to the third power of the length of the fish. weight increases in a linear fashion with age in the Catalina population. The rate of increase with age would be less in the Guadalupe population due to dwarfing. The three coloration phases of P. pulch1-um are described, two of which are found in adult individuals. The uniform coloration is made up mostly of mature and immature fishes. About 5% of the mature uniform individuals were males at Catalina, and about 12%at Guadalupe. The bicolored phase is made up exclusively of males and late transitional individuals. Data from field transects revealed that there were about five uniform individuals to every bicolored male. Based on an estimated yearly survival rate of about 0.7, the mature at Catalina was approximately two females for every male. The ratio at Guadalupe was closer to three females for every two males, due in part to the earlier sex changes seen there.

Sequential hermaphroditism, a phenomenon There are a few protogynous fish for characterized by an individual changing from one which the information is nearly complete. For sex to another at some point in its life history, is example, Moe (1969)provided excellent data on the widespread in fishes (Atz 1964; Reinboth life history pattern, gonadal transformation, and 1970). In some species, individuals change from survival rate of the serranid Epinephelus moria. male to female (protandry) and in others the sit• Natural in the synbranchid uation is the reverse (protogyny). Monopterus albus has been extensively studied Most of the published information on the life both in the field and laboratory (Liem 1963, 1968; histories of sequentially hermaphroditic species Chan 1971), but little is known about its age• has dealt with the distribution of the with specific fecundity and survival pattern. A similar size, sometimes correlated with a histological situation exists for the labrid Caris julis (Reinboth investigation of the gonads (Atz 1964; Reinboth 1957,1962;Roede 1966),where again we lack infor• 1970). However, in order to interpret the full mation on the demography' of the population. implications of the sexual patterns seen in Among the Labridae, perhaps the most complete sequential hermaphrodites, data on the age dis• information exists on the seven Caribbean species tribution, age-specific fecundity, and the sexual of the genera Thalassoma, Halichoeres, and transformation schedule of the population are Hemipteronotus studied by Roede (1972). An un• needed (Warner in press). fortunate limitation was placed on Roede's work by the tropical location, which precluded age de• 'Scripps Institution of Oceanography, University of Califor• nia, San Diego, La Jolla, CA 92037;present address, Smithsonian termination from growth rings on scales or Tropical Research Institute, P.O. Box 2072, Balboa, Canal Zone. otoliths.

ManuscriptFISHERY BULLETIN:accepted JulyVOL.1974.73,NO.2, 1975. 262 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

Pimelometopon pulchrum (Ayres), the Califor• and its coloration noted. Several dorsal spines nia sheephead, is a labrid of the subfamily were removed and frozen, and the gonads were Bodianinae. It is confined to temperate waters, fixed in bouin's fluid. ranging from Monterey Bay, Calif., to Cabo San Lucas at the tip of Baja California, Mexico (Miller Age Determination Methods and Lea 1972).Individuals can reach a large size (over 800 mm standard length [SL]) and are com• Age determination by counting annular marks monly found off southern California along rocky on the otoliths or scales was precluded in P. shores at depths between 5 and 50 m. In this pulchrum. The otoliths are extremely small and report, it is demonstrated that P. pulchrum, like difficult to locate, and the central portions of many other labrids, is a protogynous her• nearly all the scales were either clear or irregularly maphrodite. In addition, data are presented on age banded, indicating regeneration. and growth, on the distribution of the sexes in The bones and spines of P. pulchrum did show relation to color, size, and age, and on the observed regular markings, and younger fish could be suc• patterns of fecundity and survival. The study cessfully aged by counting the marks on either the embraces two widely separated populations, bones (opercula or cranial ridges) or the dorsal chosen to reflect how differences in the spines. However, the proximal portions of the demography of the population might lead to the bones tended to thicken and obscure the earlier observed differences in the schedule of sexual marks on older California sheephead and only . transformation (discussed in Warner in press). dorsal spine annuli could be used for age deter• mination. MATERIALS AND METHODS Dorsal spines were prepared as follows: the flesh was removed by means of a household enzyme Source of Materials and product (Ossian 1970) and the spines were air Times of Sampling dried. The classical methods of decalcification and/or thin sectioning (e.g., Cuerrier 1951) were Pimelometopon pulchrum was taken by means not used. Instead, a high-speed grinding tool with of a hand spear while either skin diving or using a thin abrasive disc was used to cut cleanly scuba. The main collecting area was at Fisher• through the spine at a point just distal to the man's Cove on the northeast shore of Santa Cat• swollen portion of the base. The spinous portion alina Island, Calif., near the University of was then thrust through an opaque light shield so Southern California Marine Station (lat. 33°27'N, that only the cut base protruded. A strong long. 118°29'W). A total of 341 individuals of P. microscope light was directed to the lower portion pulchrum were processed from samples taken the of the shield so that the only light visible on the year round at monthly intervals. Collections began other side then came through the projecting base in December 1969 and continued, with occasional of the spine. The hyaline layers of the spine gaps, until July 1971; monthly samples were transmit much more light and the illuminated between 20 and 30 individuals. pattern, resembling tree rings, is easily seen in a The other area sampled in this study was at dissecting microscope. Guadalupe Island, Mexico, located approximately The second dorsal spine was used for primary 200 km west of Punta Baja, Baja California. counts; the ring patterns on the other spines were Collections were made along the protected east identical, and were used to verify counts for in• side of the island~concentrating on an area 3 km dividuals. Counts on each spine were made by two from the southern tip known as Camp (lat. people and were used in the analysis of growth 29°01'N, long. 118°14'W).Year-round sampling at only when they agreed. False rings, probably Guadalupe Island was not possible, and the 130 caused by abnormal growth conditions, were individuals taken there were from three expedi• identifiable in young individuals by their tions, January 1970(16 specimens), April 1970 (53 proximity to other annuli and their tendency to be specimens), and May 1971(61specimens). incomplete. Supplemental collections were made at La Jolla, Rarely, older fish showed a marked degenera• Calif., including a sample of large individuals from tion of the central portion of the spine, which a spearfishing meet on 19July 1970. became hollow and oil-filled, making age deter• The standard length of each fish was measured, mination from spines impossible. 263 FISHERY BULLETIN: VOL. 73, NO.2

A series of measurements of 100 spines was the same irregularity in mature eggs of other made with an ocular micrometer at a magnifica• labrids, probably correctly attributed this to dis• tion of 30 x. At this magnification, one ocular tortion during fixation and staining. This stage micrometer unit equals 0.033mm. The radius was was seldom seen, but several specimens were seen measured at midspine on a line perpendicular to with eggs in the ovarian lumen and stage 500cytes and beginning at the indentation axis. Distances still within the follicle. from the center of the spine to each annulus were occurs in small crypts, in recorded for back calculation of length, along the radius line. Finally, the distance from the spine which all the cells are at the same stage. The development and appearance of the sperma• margin to the outermost annulus was measured for determination of the time of annulus forma• togonia, primary , secondary sper• tion. matocytes, spermatids, and mature sperm follows very closely the descriptions given by Hyder (1969) for Tilapia and by Moe (1969) for EpinepheZus Methods of Reproductive Biology nwrio, and will not be repeated here .. In the laboratory, each was blotted dry, The gonadal development classes, intended to weighed, and a segment of one lobe was parallel those of Moe (1969)and Smith (1965),were dehydrated in alcohol and embedded in paraffin. designated as follows: Slides were prepared of cross-sections of the lobe, Class 1. Immature female. Stages 1 and 2 cut at thicknesses of 5, 10, and 25p'm; thicker sec• oocytes present, atretic or brown bodies (Chan et tions have less tendency to collapse and were made al. 1967)absent. The ovarian lamellae are pressed to ensure that the overall configuration of the closely together and the lumen is small. cross-section could be observed. Sections were Class 2. Resting mature female. Oocyte stages stained with ehrlich's hematoxylin and eosin. 1, 2, and 3 present, with stage 2 predominating. Each gonad was classified according to sex and Atretic bodies are usually present. state of development. Assignment of a develop• Class 3. Active mature female. Oocyte stages 3 mental class depended on the predominate stage and 4 predominate in the lamellae. In late class 3, of seen in the gonad. The division stage 5 oocytes are also present. of gametogenic stages is as follows: Class 4. Postspawning female. Ovary is was divided into five stages, follow• disrupted, with many empty follicles in the ing criteria detailed for a variety of species by lamellae. Some degenerating stages 4 and 5 Kraft and Peters (1963). Smith (1965), and Moe oocytes are usually found in the lamellae and lumen, (1969). respecti vely. Stage 1. Very small (15-30 p.m in diameter) Class 5. Transitional. Seminiferous crypts oocytes with a large nucleus, single nucleolus, and begin to proliferate in the lamellae, but some stage a relatively small amount of basophilic cytoplasm. 2 oocytes can be seen. These oocytes degenerate and decrease in number as spermatogenic activity Stage 2. (30-50p.m) Previtellogenic oocytes with a strongly basophilic cytoplasm and multiple begins to dominate the gonad. nucleoli around the nucleus margin. Class 6. Inactive male. Crypts containing primary and secondary spermatocytes pre• Stage 3. (150-300 p.m) Vitellogenesis begins dominate; few spermatids and mature sperm are with the deposition of yolk vesicles in the less seen. darkly staining cytoplasm. A thin zona radiata can Class 7. Active male. Spermatids and tailed be seen in late stage 3. sperm increase in abundance until, in the ripe Stage 4. (280-450p.m) Cytoplasm filledwith yolk vesicles and globules; the zona radiata well phase, sperm are densely packed in the collecting ducts and many crypts have coalesced. developed and strongly acidophilic. Class 8. Postspawning male. Ducts are still ex• Stage 5. (450-1,050p.m) Mature or nearly ma• ture oocytes, Uniform in appearance due to the panded, but few sperm can be seen in them. Many new crypts containing spermatogonia are present. coalescence of the yolk glob~.lles.The nucleus is eccentric and the zona radiata is thin and non• This apparently is a short-lived stage that rapidly striated. These oocytes are often extremely gives way to the resting (class 6) testis. irregular in outline and Roede (1972), who noted Fecundity determinations were made by count-

264 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

ing yolky oocytes. A thick cross-section of the to variability in the location of the cut made across ovary was cut from near the middle of the lobe, the tapering spine. weighed, and then ~gitated to dislodge as many (2) The increment of distance from the last an• oocytes as possible from the ovarian lamellae. nulus to the outer edge of the spine should increase Oocytes remaining in the lamellae were teased out with the time since the formation of that mark. If so that a complete count could be made. An es• one mark is formed each year at a particular time, timate of the number of yolky oocytes per gram of the average marginal increment should drop to ovary could then be made directly from the near zero at the time of annulus formation, then sample. The total number of eggs in the ovary was steadily increase for the rest of the year. This then approximated by multiplying by the total pattern is shown (Figure 2) for 77 California weight of the ovary. sheephead from Catalina taken throughout the Relative abundance of coloration types was es• year. Successive age groups did not differ in time timated directly from field observations. To of annulus formation, so the data are combined for eliminate the effects of any differential depth all aged fish. The distinct hyaline bands appeared distribution, visual transects were either run per• to be formed in June and July, at the beginning of pendicular to depth contours or were compiled the period of warming water in the Catalina area from a series of equal length runs parallel to suc• (Quast 1968).Formation of growth marks has been cessive contours. Transects were approximately 50 found to occur in other inshore California fishes . m in length. The number of California sheephead at a similar time (Joseph 1962;Norris 1963;Clarke in each color phase was recorded. It was assumed 1970).Ring formation also overlaps with the ini• that both coloration types are equally visible, and tiation of reproductive activity, although egg this is probably valid. California sheephead are not production and spawning continue well into Sep• secretive when adults; only juveniles tend to tember (see below). remain close to cover. Larger males appear warier (3) Lengths of P. pulchrum at previous ages than other individuals, but still remain in sight. were calculated by a modified direct-propor- The problem in observing California sheephead is not in avoidance, but inquisitiveness. Occasionally 340 transects had to be aborted because of the ten• dency of Pimelometopon to follow the diver. 310 • ._~ •• RESULTS • • .• • 280 • • Age and Growth E Van Oosten (1929)set forth criteria for the ac• .§. 250 ceptance of annuli on scales or bones as yearly l-J: marks. These criteria apply equally well to spines, ze:> ~ 220 and are as follows: (1) The spine must remain con• a 0::: stant in identity and grow proportionally with the a<[ fish. (2) Only one mark must be formed each year. z 190 I-<[ (3) The body lengths calculated by using prior an• en nuli on the spine (back-calculated lengths) should agree with the actual lengths of younger age 160 ... groups. y= 218.38 +7.92(x- 21.61) The criteria will be discussed in order . 130 • (1) Dorsal spines were certainly constantly r = 0.787 identifiable in all individuals of P. pulchrum 100 examined. The relationship of spine radius to standard length (Figure 1) is satisfactorily o 6 12 18 24 30 36 expressed in a linear fashion (r = 0.787)and there SPINE RADIUS (ocular micrometer Units)

_.is no apparent indication of allometric growth of FIGURE I.-The relationship of dorsal spine radius to standard the spine, at least for fishes of lengths greater length for 117 specimens of Pimelometopon pulchrum from Cat• than 130mm. Muchof the scatter in the data is due alina Island. One ocular micrometer unit equals 0.033 mm at 30 x.

265 FISHERY BULLETIN: VOL. 73, NO.2

I~ Table 1 shows the back-calculated lengths for 61- II 12 T w c::: t.)

FIGURE 2.-Mean marginal increments for six bimonthly inter• evidence for a decrease in the rate of growth up to vals from 78 specimens of Pimelometopon pulchrum from Cat• age 13, where the average standard length is 470 alina Island. Sample sizes are shown for each interval, and 95% mm. Pimelometopon pulchrum is quite capable of confidence limits for the mean are drawn on either side of each pain t. growing larger than this, and some individuals

TABLE l.-Back-calculated lengths for age groups 1 through 8 of Pimelometopon pulchrum from Catalina Island.

N Age 220225127547637150184214242308343523478168'185203152178200159212230251320279274295183190261527261391642251912542992471639281622111787 359289100(mm)246231286158198100106130129124145128of971Meansubsample116155197245272238368294(mm)total lengthlengthsampleof 100117 Number 8of individuals7 6 5 4 3 2 group Back-calculated lengths (mm) for ages Overall1 means of calculated lengths

tionality method given by Rounsefell and have very long lifespans. Fitch and Lavenberg Everhart (1953)as follows: (1971)mention a 32-inch (815-mm) male aged at 53 yr, and an 8.3-kg female, no length given, that was L' - C Sf 30 yr old. Although exact age determination L - C =8' becomes difficult for large and old individuals, it is occasionally· possible. The largest California where L = length of the fish at the time the spine sheephead encountered in this study were a 592 was obtained, Lf = length at the time a particular mm SL male, 20 yr of age, and a 538 mm SL male annulus was formed, S = total length of the spine which had lived 18 yr. Size-age distributions can radius, and Sf = length along the spine radius to vary for different locations. In a sample taken by the annulus in question: The term C is a factor the California Department of Fish and Game at a used to correct for the length obtained before the spearfishing meet at San Pedro, Calif., on 28 spine was formed, and is estimated by the inter• March 1971,the mean standard length for males cept of the length axis on a fish length versus spine was 661 mm (range 545-745mm) and for females radius plot (Figure 1). In the case of the Catalina was 450 mm (range 294-656mm). California sheephead population, C was equal to The pattern at Guadalupe Island is different 47.2mm. from that at Catalina (Figure 4). While the sample 266 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

I- __ empirically derived

~ L 4803 E a:::zI-<1w

FIGURE 3.-Mean standard length versus age in the Catalina population of Pimelometopon pulchrum. Sample sizes are shown for each interval, and 95% confidence limits for the mean are drawn on either side of each point. Means for back-calculated lengths are shown for comparison.

is smaller and more variable than that from Cat• alina, a marked tendency towards dwarfing is clear. Judging from the mean lengths of each age class, the Guadalupe California sheephead complete their first year of growth at a standard length about 20 mm shorter than those at Catalina. For each of the next 3 yr they fall behind an addi• tional 10 mm, after which relative growth slows 120 even more. By the eighth year, the mean standard length of Guadalupe California sheephead is a full 80 100mm less than that found at Catalina. In spite of the dwarfing, the Guadalupe popula• 40 tion shows some interesting parallels with Cat• alina. The slowing of the average rate of growth o at the time of maturity (age four) is more striking o I 2 3 4 5 6 7 8 9 10" 12 /3 14 here, and growth appears to pick up again after AGE (YE ARS) the sixth year, by which time at Guadalupe most FIGURE 4.-Mean standard length versus age in the Guadalupe individuals are males (see below). This suggests Island population of Pimelometopon pulchrum. Sample sizes are that an increase in the growth rate is associated shown for each age, and 95% confidence limits are drawn on with sex changes, a topic covered more fully in the either side of each point.

267 FISHERY BULLETIN: VOL. 73, NO.2· alamellar portion in the most ventral section of the During sexual transformation, crypts of gonad, similar to that described by Smith (1965) developing spermatocytes appear, first at the base for some serranids. of the ovarian lamellae, and then throughout the In the female, oogenesis takes place within the gonad (Figure 7). Unshed eggs and nonvi• lamellae. When the egg ripens, it breaks into the tellogenic (stage 2) oocytes are gradually reab• central lumen, which leads to the common oviduct. sorbed and the number of lamellae visible in Some oocytes are interrupted in their normal cross-section are reduced. The basic structure of development and undergo a degeneration into the gonad remains ovarian, with a central lumen various types of corpora atretica (Figure 5). These into which the lamellae protrude. The lumen

FIGURE 5.-Degenerating oocytes (doc) in the lumen of a resting ovary of Pimelometopon pulchrum. Specimen number PP411, 217 mm SL.

have been described briefly for serranids by Smith however no longer functions in transport (1965)and in detail for Morwpterus albus by Chan and sperm are collected in a series of sinuses on the et al. (1967). Chan and his colleagues discuss the periphery of the gonad, reaching the outside by possible endocrine function of atretic structures, means of ducts in the wall of the now unused and state that all types of corpora atretica even• oviduct. This is very similar to the anatomy tually end up as brown or yellowish bodies which described by Reinboth (1962,1970)for other labrid are long lasting in the gonad. In P. pulchrum, secondary (sex-reverned) males. No testes of the brown bodies can usually be found near the gonad primary type were seen. wall and in the central portion of the lamellae. Judging from the number of these terminal phase Transformation Schedule corpora atretica in resting (class 2) females com• pared with the usually greater number of earlier To illuminate the life history patterns of the stage atretics (Chan et al. 1967) in postspawning California sheephead populations, the gonad females, the brown bodies are probably formed development classes were grouped in the following from more than one degenerating oocyte. way: Brown bodies are also found in male gonads; Immature: Class 1 only. some of these are almost certainly the result of Female: Classes 2, 3, and 4. oocyte degeneration in the previous female phase Transitional: Class 5 only. (Figure 6), while others may be the result of Male: Classes 6, 7, and 8. degeneration and coalescence of unshed sperm. The distribution of sexual types by standard

268 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

length for P. pulchrum from Catalina Island (Ta• small size classes. are made up exclusively of im• ble 2) and Guadalupe Island (Table 3), as well as mature females. Mature females are most abun• the relative frequencies for each size grouping dant in the next size classes, and then become less (Figure 8), are similar in both localities in that the numerous as males begin .to predominate in the

750 JI

FIGURE 6.-Degenerating oocytes (doc) in the lumen (I) and lamellae (la) of the gonad of a transitional individual of Pimelometopon pulchrum. Specimen number PP405, 317 mm SL.

FIGURE 7.-Spermatogenic crypts (shown by arrows) developing in a gonadal lamella" of a transforming Pimelometopon pulchrum. Stage 2 oocytes (oe) and a corpus atreticum (ca) can also be seen. Specimen number PP405. 317 mm SL.

269 FISHERY BULLETIN: VOL. 73, NO.2

TABLE 2.-FrequencyImmature2533Transitional39151001854276215332492815194111168101611010146201female438565207161220564 MaleNumberof341130252812183323403415491716141110fishfish75385673291MatureofMaturesexual types in each 20-mm size class for 340-359220-239200-219320-339240-259300-319280-299380-399>360-379160-179340"359260-279120-139100-119180-199140-159180-19.9360-379220-239·260-279400lengthlength (mm) TotalsTotals< 100 thethe CatalinaGuadalupeIslandIslandpopulationpopulationof Pimelometoponof Pimelometoponpulchrumpulchrum.. 100 StandardStandard ••.•.••.•.•...4- ...4-.-A,..,'I i CATAll NA TABLE 3.-Frequency of sexual types in each 20-mm size class for 80 \ t---." \ / ' 60 \ I "'-, % V \ ~ 40 ,. I \ , " , \ 20 '. , \ II 1\.. '. \ o _0 b

GUADALUPE

100 ••.•...4-."'i i 80 i f\ \ : ' i I i I "_.-A immature 60 il il Ij1 % 0--0 f Do--G transitional f. 40 1\ I!1\ _d' , \ 20 I I ,f ~ 0274240333414151310252140<1737334972586132981333351610059230234170253114733341000304142795210145071869 21.Immature22880 MatureMaturefemale maleTransitional population 10+5437986class9 of fish (10 cm groups) TotalsTotalsCatalina STANDARD LENGTH ( 2 Guadalupe pulchrum.standardGuadalupe lengthIsland groupings(bottom)metoponforpopulationspulchrum.the Catalina of IslandPimelometopon(top) and FIGURE S.-Proportions of each AgesexualNumbertypedistributions(Figurein successive9). The2listedcmcurvesin Tableare based4. on the frequency the sexual types in each age class are graphedTABLE 4.-Frequency of sexual types in each year class of Pimelo-

largest sizes. Transitionals were found in inter• mediate sizes, in numbers which varied seasonally (see below). At Catalina, most California sheephead mature at standard lengths between 190 and 230 mm. Sexual transformation occurs over a broader size range beginning at 250 mm, with a peak of ac• tivity apparently occurring at standard lengths between 310and 330 mm. The dwarfing phenomenon found in the Guadalupe population is again evident (Table 3, Figure 8). Maturity begins at a length near 140 mm, and the majority of individuals are male by a length of 210 mm. Peak transformation activity appears to occur in the population in fishes rang• ing from 190to 230mm in standard length. The actual time courses for all these events become evident when the relative frequencies of

270 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

14 FMJ0ADNSA 100 -.-.- ••-.-.-." I CA TALlNA MONTH J 14 80 ! p----<>... \ I " 641002128 \ I " 60 \ / '1>-"'--<>",

40 ~ \ \ , 20 / / \ \ . '0.... __ ...." I I V \.i /'\ " " : i..., o I •

4---4 immature GUADALUPE 0--0 9 0---00 transitional 100 -.-....•-.-.-.'\ :\ . 1\ •..•.•.•.• r:I' \ '\ 80 \\ II \\ I I \ i I \ i I \ 60 il! \b--- 1\ 40 II' \ I \ I \ 20 I \ I \ o I \ I 2 4 5 6 7 8 AGE (YEARS)

FIGURE 9.-Proportions of sexual types in each year class of 12 Pimelometopon pulchrum from Catalina Island (top) and Guadalupe Island (bottom). The last age grouping consists of all fishes 10 or more years old. 10 In both populations, sexual maturity begins in the fourth year of life for virtually all members. 8 By using age groupings, the skewness introduced by the dwarfing at Guadalupe is removed, and differences in the transformation activity time 6 schedule in the two populations are revealed. At Guadalupe, males are present in essentially the 4 same abundance as females in age classes 5 and 6, and strongly predominate at age 7 and thereafter. Therefore the majority of California sheephead at 2 Guadalupe Island spend no more than 2 or 3 yr as functional females. o Transformation generally occurs later in the JFMAMJJ ASOND Catalina population. Most individuals are func• MONTH tional females for at least 4 yr, and males predominate only after age 8. FIGURE 1O.-Number of individuals of Pimelometopon pulchrum in each mature gonadal development class from monthly samples taken at Catalina Island. Distribution of Gonad Development Classeswith Time development classes for 166 California sheephead from Catalina is shown in Figure 10.As expected, The active state of gonads may be determined immature fishes, which are not shown in the directly through histological examination or in• Figure, occur throughout the year. Resting stage ferred from the appearance and the size of gonad females (class 2) were encountered from August (gonad indices). through May, and predominated from October to The seasonal distribution of mature gonad April. Active females (class 3) were present May

271 FISHERY BULLETIN: VOL. 73, NO.2 through September. Late class 3 gonads were seen September. The resting value is then seen again, in July, August, and September, and most spawn• remaining constant through the winter. ing activity probably takes place in these months. The index used was gonad weight scaled to Females with postspawning ovaries (class 4) were compensate for different lengths of individuals. captured in low numbers from August to early When only the mature females less than 310mm in October. Class 4 appears short-lived, quickly standard length are included in the analysis, the receding into a resting class (class 2) or transi• relationship between gonad weight and standard tional (class 5) phase. weight is sufficiently linear (Pearson correlation Transitional individuals were found only from coefficient = 0.845 [P < 0.001] on 24 individuals October to March at Catalina. Those taken in Oc• caught in June) that the use of the following for• tober and November were all in the early stages of mula is justified: transformation, with many stage 2 oocytes and a few scattered spermatogenic crypts in evidence. Gonad index = (gonad weight in grams) (100) (standard length in mm) Transitionals captured in February at Catalina or in May at Guadalupe were more advanced, with The size range used includes the great majority of few stage 2 oocytes and spermatogenic crypts reproductive females at Catalina. dominating the gonad. An analysis of the spawning season of P. Most males at Catalina were inactive (class 6) pulchrum at Guadalupe Island was not possible from October through April, closely paralleling the due to the lack of year-round sampling.· period seen for females. Active gonads predominated in samples from fish taken in May Multiple Spawning and Fecundity through September. Again the pattern suggests that spawning activity takes place from August Two or more distinct groups of ripening oocytes through early October. were usually apparent in the ovaries of P. Further support for designating this period as pulchrum examined in June and July. The size the spawning season comes from the gonad indices distribution of yolky oocytes in an ovarian cross• (Figure 11) of Catalina females caught in section (Figure 12) from a female, 244 mm SL, different months. These reflect a similar pattern captured at Catalina in mid-July, shows that there _. seen in the analysis of gonad development states. is one group of eggs ready to be spawned, and that After a quiescent period from October through two other distinct groups are undergoing vi• April, the ovaries begin to increase in size until a tellogenesis. This type of successive maturation of maximum is reached in June and July. Spawning several groups of oocytes is termed asynchrony, reduces the average index steadily from then until and is characteristic of species that have com• paratively long breeding seasons and multiple spawnings by individuals within each season (Yamamoto and Yamazaki 1961).

24

20

'"(/) t- 16 t) 8 :512 a: '" OJ ~ B z:::> 4

o 2 4 6 B 10 12 14 16 IB 20 OaCYT E DIAMETER (ocular micrometer units)

FIGURE H.-Average gonad indices for monthly samples of ma• FIGURE 12.-Size distribution of yolky oocytes in an ovarian ture female Pimelometopon pulchrum, all of standard lengths cross-section of a 244 mm SL female of Pimelometopon pulchrum less than 300 mm. Sample sizes are shown above the bracketed captured 22 July at Catalina Island. The oocytes are also clas• lines, which are the 95%confidence limits of the mean. sified according to their degree of development.

272 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

Further evidence for multiple spawning is seen Warner in press). As long as the number of eggs in the ovaries from some females captured in per unit weight of ovary does not vary appreciably August and early September. There were a few with size or age, weights of active prespawning mature eggs free in the lumen and numerous ovaries can be used to represent relative fecundi• empty follicles in the lamellae, both indications of ties. The last column of Table 5 shows there is no recent spawning. At the same time, another group apparent effect of fish length on egg density of vitellogenic oocytes were observed developing within the ovary. in the' lamellae and these would presumably have Comparison of ovary weights and standard been spawned at a later time. lengths for mature females captured at Catalina As Yamamoto and Yamazaki (1961) point out, in June and July (Figure 13) shows that fecundity the presence of multiple spawning complicates increases exponentially with the length. The ex- any determination of the number of eggs . ponential equation: produced each year by an individual fish. Es• W = 1.31 X 10-3 L2.95 timates can be made from an analysis over time of frequencies of egg diameters, such as that done by (W = gonad weight, L = standard length) in• Clark (1934) for Sardinops caerula. Such analyses dicates that the increase of gonad weight with require a large sample over the mature size range and this was not available for P. pulchrum. Counts of the yolky oocytes in subsampl~s of 70 • ovaries made for California sheephead females • captured in July (Table 5) are probably overes• timates of the number of eggs spawned during the

TABLE 5.-Estimates of the total number of vitellogenic' oocytes 60 and density of those oocytes in the ovaries of Pimelometopon pulchrum captured at Catalina Island in July 1970. capture7/24Date34.077/1950.027/22yolky41.6319.8028.0017.2316.5316.69ovary6.87pe(9)258,100113,85036,068296,600171,500167,600totalnumber88,30076,87074,270rofgoocytes,ram5,1254,6504,4505,250numberyolkyEstimated4,9205,7506,1256,2005,930Weightofofovaryoocytesofof Estimated Standard330359311314254280238235length(mm) gram 5,377 ± 499. Mean and20995% confidence limits of oocyte density, oocytes=per 50 E 0> Il• <.9 40 3w >• 0:: ••= •• • / ••r w=0.7871.31x10-3 L2.95 ;; 30•• • /'. ./ • • • • o / • •• • season. This is because, as pointed out above, the relationship between the number of these oocytes 20 and the number actually spawned depends on the survival rate of the oocytes to maturity and the proportion that are actually ejected from the body. The smaller numbers of stage 5 oocytes relative to 10 stages 3 and 4 (Figure 12) indicates a loss during development. There are certainly some eggs left in the lumen of posts pawning females. These degenerate and are presumably absorbed during o the resting phase. 20 22 24 26 28 30 32 34 36 38 For an analysis of the functional significance of STANDARD LENGTH (em) sequential hermaphroditism, actual egg numbers fIGURE 13.-0vary weight versus standard length for females of are less important than data on the relative values Pimelometopon pulchrum captured in June and July at Catalina for age- or size-specific fecundities (Williams 1966; Island.

273 FISHERY BULLETIN: VOL. 73, NO.2

length conforms to a simple cube law relationship, which would be expected if gonad weight remains . 70 • some constant proportion of the total weight. The • exponent 2.95 was determined by a least-squares regression fit to a logarithmic transformation of the data. The confidence limits around the regres• sion line become increasingly large with higher 60 values of Wand L, and the curve should not be used for extrapolations beyond the range of the data. Ovary weights in relation to age are shown in • Figure 14. There are few data for the older age 50 ~ classes, but there is a definite positive correlation E of the fecundity and the age of the individual. 0> Il• Coloration, Sex, and Field Distribution ~ 40 • of Coloration Types 3w >- The California sheephead is found in three main cr: color phases (Crozier 1966),all of which are closely :; 30 correlated with sexual state. o • • For the first year, P. pulchrum has juvenile coloration, a gold or salmon body color with black spots on the anal fin, the anterior and posterior 20 • portions of the dorsal fins, and on the caudal • • • peduncle, and with a silver lateral stripe extending • from the eye to the caudal fin. Crozier (1966)stated w= 8.88L -26.25 • that the initial body color was gold, and this was 10 • r = 0.802 gradually replaced by the reddish adult shade. The juvenile coloration was seldom seen in individuals over 100 mm SL, and has never been found in sexually mature individuals. o The most common color pattern of P. pulchrum 4 567 8 9 is a uniform rose or salmon color, covering the AGE (years) entire body with the exception of the chin, which is usually white in mature individuals. The m~dian FIGURE 14.-0vary weight versus age for females of Pimelomet• and pelvic fins are darker than the body, ranging ()]!on pulchrum captured in June and July at Catalina Island. from dusky red to black. The pectoral fins usually match body color. Uniform coloration may be ob• in length from 245 to 315 mm. and were captured scured by a melanistic condition which causes the in June, July, and December. Examination of a entire body to appear brown. This occurs in vary• large series of gonad cross-sections from these in• ing degrees, making the fish appear almost black dividuals revealed a few stage 2 oocytes within the in extreme cases. Eleven percent of the uniformly lamellae from two captured in July. This can be colored fish captured at Catalina were designated taken as evidence for a recent . All the melanistic, as were one-third of all uniform types others had gonads of completely normal male ap• at Guadalupe. pearance. A uniform coloration is characteristic of imma• Field notes revealed that all of these individuals ture fish as well as mature females. Histological were melanistic, and 70%were recorded as having analysis indicated, however, that the relationship some male external characteristics, such as a small was not perfect. At Catalina, 3.5% of the in• nuchal hump or slight differential darkenings of dividuals designated uniform in color were dis• either the head or tail regions (see below). This covered to have male gonads. When only sexually suggests the possibility that some of these in• mature uniformly colored California sheephead dividuals may have been incorrectly typed due to were tallied, 5.1%were male. These males ranged the ground color being obscured by melanin.

274 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

Males in uniform coloration are more frequent TABLE 6.-Numbers of coloration types in two populations of in the Guadalupe population. A total of 6 out of 57 Pimelometopon pulchrum, determined by a series of visual tran• sects. (10.5%) uniformly colored individuals were males. andbicolored343type183uniform33No.640.1570.153Proportiontransectstype95%bicolored9370of±conf.0.0480.035ptypeslimitofNo. of Elimination of Localityimmature No.fishof from the count GuadalupeCatalina Island raises the figure to 12.3%males. Four of the six were melanistic, one of these with slight male char• acteristics. The other two individuals possessed normal uniform coloration with no darkening. In the third color phase the head region, includ• ing the opercle, is dark brown or black. The chin remains white, and the midsection retains the DISCUSSION reddish hue of the uniform type. The caudal por• tion, beginning approximately on a line connect• Anatomical Features of the Gonad ing the initial soft rays of the dorsal fin with the and Sexual Transformation anterior limit of the anal fin, is also dark brown or black. The median fins and pelvics remain The ovary of P. pulchrum is essentially identical generally dark in color, and the pectorals may with that of the labrid Goris julis, which was acquire a dark band at their tips. studied in detail by 'Reinboth (1962). Reinboth, This coloration is found exclusively in males and however, did distinguish between the testes of some transitionals (see below). It is usually ac• those G.julis born as males (primary males) and companied by two other male secondary sexual those that become males through sex reversal features common in the Bodianinae, the nuchal (secondary males). In the former, the testis ap• hump and filamentous extensions of the median pears rather solid and flattened, and sperm are fins. The hump appears to increase in relative size transported by means of a single vas deferens in as the male gets larger, making the head appear each lobe. The secondary male has a testis like that increasingly angular in profile. No individual with described here for P. pulchrum. The two types this bicolored pattern was found to have func• differ in the structure of the vas deferens tional ovaries. During the breeding season, the posterior to the gonadal lobes, which surrounds the pattern serves as an excellent indicator of a func• old oviduct in secondary males, but is a simple tube tional male. in primary males (Reinboth 1970). Individuals classified as transitional varied in When primary and secondary males are present coloration. Of 11 transforming California in a single species, Reinboth (1970) termed the sheephead for which coloration records exist, 3 species diandric. When only secondary males are were scored uniform in color and 2 as bicolored. present, the species is termed monandric. To The remaining 6 were recorded as intermediate in Reinboth's (1970) list of monandric species coloration, usually involving a slight darkening of (Labrus turdus, L. merula, L. bergytta, the head, caudal region, or both. The three uniform Hemipteronotus novacula, and possibly L. individuals were classed as early transitionals bimaculatus) we may add P. pulchrum. Other (large amounts of stage 2 oocytes still in the labrid species have been studied without regard gonad); the two bicolored fishes were classed as for the primary-secondary male phenomenon (Atz late transitionals (only a few degenerating 1964; Reinboth 1970), and cannot be categorized oocytes in the gonad cross~sections). with certainty as monandric or diandric. The distribution of uniform and bicolored types The transition from a functional ovary to a tes• in field populations, determined by visual tran• tis has been described in detail for labrid fishes in sects (Table 6) shows that bicolored males are both naturally occurring situations (Reinboth present in remarkably similar proportions in both 1962; Sordi 1962; Okada 1962; Roede 1972) and localities, occurring in a ratio of about 5.5 uniform under the influence of hormone administration individuals to every bicolored individual. Con• (Reinboth 1962, 1963; Roede 1972). These reports fidence limits for estimating the proportion of are essentially in agreement with the presentob• bicolored individuals were calculated from a servations on P. pulchrum. There is no evidence of binomial distribution, n = 216 and 407 for Cat• synchronous hermaphroditism (Atz 1964:147) in alina Island and Guadalupe Island, respectively the Labridae, but Robertson (1972) found sperma• (Dixon and Massey 1969). togenic crypts in the ovaries of 28 of 29 females of 275 FISHERY BULLETIN: VOL. 73, NO.2

Labroides dimidiatus, and 15 of these had crypts believed that sex reversal is a rare phenomenon ill with sperm or spermatids. Thus, the possibility of this genus. encountering a synchronously hermaphroditic Age determinations allow several more labrid species should not be ruled out. inferences about the sexual life history of a species. When few or no young males can be found, Transformation Schedule there is strong evidence for protogyny since the possibility of differential growth is eliminated. Pimelometopon pulchrum fits the generallabrid The rate of transformation in different age pattern of size and sex distribution. No males were classes can be estimated, and this provides an idea found smaller than 230 mm SL at Catalina Island, of how long the average individual spends in and none smaller than 150 mm at Guadalupe. The different sexual phases. Finally, by comparing the longer size classes (above 350 mm and 230 mm at distribution of sex versus length with sex versus Catalina and Guadalupe, respectively) contain the age of the individual, it may be possible to mostly males. assign a more critical role to one or the other as a Data for labrid sexuality are usually in the form causative factor for sex reversal. of size frequency distributions of males and The age at first maturity (4 yr) does not differ females within a species (Atz 1964; Remacle 1970; for P. pulchrum at Catalina and Guadalupe Roede 1972). Some of these studies have been con• Islands, but the distribution of sexual transfor• founded by the presence of two distinct color pat• mation with age differs markedly. Most in• terns, the investigators wrongly assuming strict dividuals in both populations function at least 1 yr sexual dichromatism (see below). An additional as females. At Guadalupe, many change sex after complication is the possibility of two different 1 yr, and most are males within 3 yr after matur• types of males being present in some species, ing. Most sex reversals occur at Catalina between usually with different life histories and behavior the seventh and eighth year, 4 yr after maturing (Reinboth 1970). Both of these problems are as a female. Some individuals remain female for eliminated by histological examinations of the shorter or longer periods of time. The oldest gonad, which also reveals the presence of inter• female encountered in this study was 17 yr old. sexual or transitional individuals. The dwarfing phenomenon at Guadalupe, which The absence. of males from the smaller size should bring ·about a slower rate of increase of classes at least suggests protogyny. However, fecundity with age, would have enough effect to similar patterns can also result from samples of a decrease the optimum age of transformation in species exhibiting differential growth rates for that population when compared to the Catalina the sexes (e.g., see Strasburg 1970, for weight and population. This will be discussed in detail else• sex distributions of blue marlin, Makaira where (Warner in press). nigricans), and this should be taken into con• Lonnberg and Gustafson (1937) determined the sideration. ages of a series of specimens of Labrus bimacula• Fourteen of the fifteen labrid species either tus (as L. ossifagus) which they correlated with reviewed or dealt with originally by Roede (1972) sexual state. They found that sex reversal occurred had similar patterns of length-sex distribution. in individuals from age seven onward, and was Females predominated in the smaller size classes, associated with a color change from red to blue• males in the larger. The proportion of males in the striped. Females were fou.nd in diminishing smaller sizes (usually associated with a particular numbers up to age 18, mostly confined to the red color pattern; see below) varied from practically phase. Males in the red phase ranged from around none in some species of Halichoeres and 3 to 7 yr old; blue-striped males got as old as 25. Herl'dpteronotus up to nearly 30% for Stethojulis Other protogynous which have been strigiventer (Randall 1955). Males became investigated regarding age of transformation increasingly common as length increased and the show a variety of patterns in the distribution of longest size classes consisted almost exclusively of sex reversal over their life-span.> Liem (1963) males. demonstrated that sex transformation in the Species of the genus Symphodus (Crenilabrus) synbranchid rice eel Monopterus albus occurs appeared to exhibit a different pattern, with mainly when individuals reach about 30 mo of age nearly equal numbers of males and females in the (about 35 cm in length). Few fishes in nature small size classes (S6ljan 1930a, b). Remacle (1970) deviated from this pattern. Liem (1963) was able 276 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

to induce earlier transformations by starving the ed t-test for difference in means) were sig• individuals. Moe (1969) has carefully worked out nificantly different at the 5% level or less, and the the age distribution of sex reversal in the serranid remaining two were significant at the 10% level. Epinephelus morio, and found a rather smooth An assessment of the effect of age on sex period of transition from female to male over at reversal was made in similar fashion, comparing least 5 yr (ages 5 to 10), at a rate of about 15% of the mean ages of males and females in successive the individuals in a year class reversing per year. size groupings (Figure 16). If sex reversal were In a 'less comprehensive survey, McErlean and closely related to the age of an individual, then Smith (1964) estimated that transformation oc• males would tend to be older than females in a curred at age 10 or 11 in Mycteroperca microlepis given length group. The relationship between age (), and speculated that the age of the and sex is less strong (Figure 16). Sample sizes are fish had more effect on sex reversal than the not large, and the range of ages encountered in a length. sample is small relative to measured length values, To determine the effect of individual size on sex so fewer significant results might be expected. transformation in P. pulchrum, mean lengths of Only one size group was found where males were males and females in each age class were com• significantly older than the females. However, the pared (Figure 15). If length is closely related to sex existence of several large negative t values in reversal, one would expect males to be larger than groups where the age of females is greater than females of the same age, and this was found in that of males supports the idea that size is more both the Catalina and Guadalupe populations. In important than age in effecting sex change. every age grouping where sample size permitted The high average age of females in the larger statistical analysis, males tended to be larger than size groupings of both populations (Figure 16) was females. Five of the seven groups tested (one-sid- not expected, and suggests that the individual growth rate may also be involved in sex reversal. The large separation between male and female mean ages begins with the 300-mm size grouping at Catalina, and the 200-mm group at Guadalupe. Inspection of Figure 8 reveals that at abQut these 350 lengths, the proportions of males and females un•

:3 dergo an abrupt shift. A large percentage of the individuals in the populations apparently reverse E sex at these sizes. Furthermore, the difference in E ~300 ages between males and females of lengths above If- these "critical" sizes appears to be significant. The (!) Z mean age of females larger than 300 mm at Cat• W ...J alina is 7.9, a full year older than males in the same a size range (t31 = 1.51, P<0.10). Similarly, females ~ 250 za larger than 200 mm at Guadalupe have a mean age ~ of 9.5 yr, and males at that size range average 7.0 (f) yr (t32 = 2.80, P

277 FISHERY BULLETIN: VOL. 73, NO.2

10 2

9

2 if) ,z 0:: 6 <1:8 1 " I w 1 " >- ~ 1 5 w ~/ GUADALUPE IS. I / 1 " J / (!) / <1: 1 I 7 141 /~c$ / 9 / / c1 / 6 / / FIGURE 16.-Mean ages for suc• cessive 20 mm standard length ~l /' 10 5 groupings of male and female 2 ,{ CATALINA IS. Pimelometopon pulchrum. Sample 6_l;,r 7/ /~ II I /"'4 sizes and standard errors are 5 J r~' shown as in Figure 15. 37 170 190 210 230 250 270 290 310 330 350 370 STANDARD LENGTH (20mm groups)

The best picture, then, that can be drawn from relatively late spawning seasons of these species the present information is that rapidly growing may be caused by upwelling along the southern individuals may transform sooner than other California coast which usually persists well into fishes of the same age. The bulk of the population, June or July, resulting in a delay of inshore water growing at the average rate, eventually reaches a warming until that time (Quast 1968). "critical" size where most of them change sex. Multiple spawning has not often been con• Fishes that grow slowly may not change sex at all. sidered in studies of labrid breeding seasons. Roede (1972)stated that labrids have "continuous, The Breeding Season, Multiple successive spawning cycles," and based this view Spawning, and Fecundity upon the presence of many vitellogenic oocyte stages in mature ovaries of the seven species she Breder and Rosen (1966)have summarized the investigated. She contended there is no resting information available on the spawning seasons of stage of the ovary, but a series of year-round labrids. In temperate species, most activity occurs spawnings. At all times of the year she was able to over a period of approximately 3 mo, most com• find ovaries with several stages of developing monly in April, May, an4 June. The Catalina oocytes as well as the stage 2 recruitment stock. population of P. pulchrum is exceptional in this This clearly is not the case in P. pulchrum, where case, since spawning occurs from August to Oc• the winter-resting ovary contains virtually no tober. The two other commonly found at signs of vitellogenesis. Active ovaries of the Catalina Island also spawn later in the year than California sheephead strongly resemble those pic• other labrids. Oxyjulis californica spawns from tured by Roede (1972, plates II and III) for May until October (Bolin 1930), and Halichoeres Halichoeres and Hemipteronotus. The successive semicinctus probably spawns in late June, July, spawnings within a restricted season indicated for and August (D. R. Diener, pers. commun.). The P. pulchrum may then be a curtailed version of a

278 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

year-round condition in its presumably tropical the Labridae, and extensive sampling is usually ancestor, representing an adaptation to the fluc• needed before the relationship between sex and tuations of food availability characteristic of coloration can be accurately described. temperate regions. Many labrid species exhibit a number of color The size-specific increases in fecundity seen in phases, and these have often been attributed to Catalina P. pulchrum are, of course, common in sexual dimol1Jhism or to differences between im• most long-lived fishes. Many of the Guadalupe matures and adults. Roede (1972) has reviewed a females were not sexually active when the sample number of cases where such an interpretation was was taken and no fecundity data are available. incorrect, being based on casual observation or However, it can be predicted that the average small samples. Apparently there is no strict dis• fecundity of Guadalupe Island individuals will tribution of sex with color in the Labridae and the increase rrmch more slowly with age than that of only generalization possible is that females tend to individuals from Catalina, due to the low growth strongly predominate in the "first adult" (Roede rate of the Guadalupe individuals discussed in an 1972) colors, and the terminal-phase coloration is earlier section. If the active ovary weight made up almost exclusively of males. increases with size in a fashion similar to that seen In most species investigated, males make up 10 at Catalina (Figure 13), the average ovary weight to 35% of the first adult-colored individuals (Roede for a 4-yr-old fish at Guadalupe would be 1972). In Gomphosus varius (Strasburg and Hiatt approximately 8 g. Age class 4 California 1957),Halichoeres maculipinna, H. garnoti, and sheephead at Catalina had ovaries with an average Hemipteronotus martinicensis (Roe de 1972), no weight of 13.13 g. The difference increases with males are found in the initial color phase. In con• age. Six- and eight-year-old individuals at trast, S6ljan (1930a, b) found that 48% of the Guadalupe should have ovaries weighing 9 and 15 Symphodus (Crenilabrus) ocellatus examined in g respectively. Weights for the same ages at Cat• the first adult phase were males. alina were 23.1 g and 53.5 g. The terminal-phase coloration appears to be In the Catalina population, there may be an much more closely restricted as to sex. Of 14labrid abrupt increase in the fecundity of fishes remain• species exhibiting color phases mentioned by ing female after age seven; this is the age where RO€de (1972), the terminal phase consisted most sexual transformations occur (compare exclusively of males in all but two (Halichoeres Figures 9 and 14). If such an increase does exist, it garnoti and H. bivittatus). When other coloration may be an indication of compensation by those classes are described, intermediate between the remaining females for the relative gain in age• initial and terminal phases, the proportions of specific reproductive potential experienced by in• males and females in them are also intermediate. dividuals that do change sex. A more complete Roede (1972) notes that where color changes are discussion of relative male and female age-specific more gradual, as in H. garnoti and H. bivittatus, fecundities can be found elsewhere (Warner in the relationship between size and sex is the least press). exact.

The Relationship of Color and Sex Sex Ratio and an Estimate of Survival

Pimelometopon pulchrum appears to follow the Roede (1972) believed that her collections were general lab rid coloration patter~ quite closely, true random sam.ples of populations and was able with a preponderance of females and immatures to estimate the sex ratio in the seven labrid species in the initial uniform color phase, and the terminal she investigated. There were two to four times as bicolored phase containing only males. Thus the many females as males in all but one species designation of the uniform phase as the "female" (Hemipteronotus splendens), which had an equal coloration and the bicolored phase as the "male" sex ratio. coloration (Jordan and Evermann 1898; Fitch and The samples of P. pulchrum were not considered Lavenberg 1971; Miller and Lea 1972) is more or random and direct sex ratio estimates could not be less correct, especially when immatures are made. Field transects at Catalina and Guadalupe included under the uniform designation (Barnhart islands yielded a ratio of about 5.5 uniformly 1936; Roedel 1948). Dichromatism, however, is not colored individuals to every bicolored male. To es• necessarily an indication of in timate the sex ratios of mature individuals, the

279 FISHERY BULLETIN: VOL. 73, NO.2

proportion of immatures and males in the uniform mature, and approximately 5% of those individuals group must be known, and this requires some would be male. The ratio of mature males to ma• knowledge of mortality rates. ture females from field transects would then be A rough estimate of mortality can be made from derived as: the transect data and the known color composition of each age. The yearly survival rate is calculated _33_+_(1_8_3_X_O_.3_6_X_O._05_)= _36 = 0.57 183 x 0.36 x 0.95 63 using a modification of a simple fisheries estimate (Ricker 1958). The rate is assumed to be constant, or about two females for every mature male. and can be estimated as: For Guadalupe, about a third (34%) of the s=--, Nt + 1 uniform individuals should be mature, and 90% of Nt these would be female. The sex ratio at Guadalupe would then best estimated as: where N is the number of individuals in a par• ticular age class in a sample. Where a large 64 + (343 x 0.34 x 0.1) 76 = 105= 0.72 number of age classes are available, one can weight the classes according to their abundance or approximately three females for every two and separate two or more ages from the numera• males. tor and denominator, giving, for example: An artifact of protogynous hermaphroditism is the concentration of females in the younger ages. 32 = N3 + N4 + + Nr Thus, the observed sex ratio depends on when the 1 + 2 + + r-2 N N N change sex, and upon the mortality oc• For the Catalina population of P. pulchrum, the curring from year to year. Mortality causes sex formula used was: ratios to be biased towards females and these become even more biased the greater the average 36 = Ns + Ng + + N13 age of transformation is in the population. This N2 + N3 + + N7 effect can be seen by comparing the estimated sex In this first approximation we assume that ratio of the Guadalupe population (0.72), where bicolored fishes are all 8 or more years old, and most females change sex within 3 yr after ma• younger fish (ages 2 through 7) are uniform. The turity, with that of Catalina (0.57), where trans• decision to use· age 7 as the dividing point comes formation is relatively delayed. from Figure 9, where between ages 7 and 8 the The deviations of sex ratio from unity seen here proportion of females drops to a low level and the should not be taken as contradictions of the males become predominant. theories put forth on the adaptiveness of the 1:1 From Catalina transect data, 3 is estimated by: ratio (Fisher 1930; Bodmer and Edwards 1960; Kalmus and Smith 1960), as these were developed 36 = 33 and 3 = 0.735. for nonhermaphroditic species, and sought to 183 equalize the lifetime reproductive potentials for The transect ratio can then be adjusted to com• males and females. In sequential hermaphrodites, pensate for bicolored individuals younger than age the same individual functions as both male and 8 and uniform individuals older than age 7 by us• female at sometime in its life, and the question ing proportions derived from Table 4, and each becomes one of changing sex at the proper time to age's contribution to the numerator or denomina• maximize the individual's reproductive potential tor can be weighted according to the first estimate (Warner in press). of survival derived above. The new estimate of survival from the adjusted transect ratio is not SUMMARY very different from the original, 3 = 0.71. A similar estimate for the Guadalupe Island Year-round sampling of a population of the population, assuming in this case that the uniform California sheephead, Pimelometopon pulchrum, individuals are ages 2 through 7 (see Figure 9) and was carried out at Catalina Island, Calif., and adjusting as before, is 3 = 0.69. comparative material was collected from a Mature sex ratios can now be estimated. Using population at Guadalupe Island, Mexico. 0.7 as the yearly survival rate, about 36% of the Age determinations indicate individuals in the uniform individuals seen at Catalina should be Guadalupe population are dwarfed relative to

280. WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

those at Catalina. The growth rate is lower for transitionals and usually have a nuchal hump and Guadalupe fishes and in both populations there filamentous extensions of the median fins. may be a slowing of growth at the onset of ma• Field observations indicate that there are about turity, as well as an increase in the growth rate 5.5 uniformly colored individuals to every after sexual transformation. bicolored male at both Catalina and Guadalupe. Pimelometopon pulchrum is a protogynous her• Individual size appears to have a greater effect maphrodite. During the sex change from female to on the sex change than does age, and rapidly male, the ovary degenerates and spermatogenic growing fishes may change sex sooner than slow crypts dominate the gonad. The basic structure of growing individuals of the same age, which may the gonad remains ovarian however, with lamellae not change sex at all. protruding into a central lumen. Sperm transport With the assumption of constant, age-indepen• is through a series of ducts on the periphery of the . dent mortality, the annual survival rate at both gonad and oviduct. Catalina and Guadalupe was estimated as about Catalina California sheep head attain sexual 0.7, as judged from the field transect data. maturity at age 4, at a standard length of about The mature sex ratio at Catalina was 200 mm. Most function as females for 4 yr and then approximately two females for every male. At change sex, at a length of about 310 mm. Some Guadalupe the ratio was closer to three females for individuals may transform earlier or later, or not every two males, due in part to the earlier sexual at all. The Guadalupe population also matures at transformation seen there. age 4, at a length of about 140 mm. But transfor• mation occurs at an earlier age, with most in• ACKNOWLEDGMENTS dividuals becoming males by age 7. Peak trans• formation activity occurs in fishes between 190 I would like to particularly thank R. H. and 230 mm SL at Guadalupe. Rosenblatt and E. W. Fager for their early and Gonad development states and gonad indices of continued encouragement and advice. lam also Catalina California sheephead suggest that grateful to J. T. Enright, P. K. Dayton, and J. B. . spawning occurs in July, August, and September Graham for their critical comments on an earlier and that sexual transformation occurs in the draft. Special thanks go to Isabel Downs for her winter months between breeding seasons. help in many phases of this project. Finally, I Spawning probably takes place a number of would like to thank D. R. Diener for many times in a. single breeding season, which stimulating discussions on the fascinating field of complicates the determination of the actual hermaphroditism in fishes. number ·of eggs produced by a female each year. Ovary weight, however, can give a good indication of relative age and size-specific fecundities, since LITERATURE CITED egg density does not appear to vary with fish ATZ,J. W. length. The ovary weight of increases P. pulchrum 1964. Intersexuality in fishes. In C. N. Armstrong and A. J. exponentially with length and linearly with the Marshall (editors), Intersexuality in includ• age of the individual in the Catalina population. ing man, p. 145-232. Academic Press., Lond. At Guadalupe, the average fecundity probably BARNHART, P. S. 1936. Marine fishes of southern California. Univ. Calif. increases more slowly with age when compared to Press, Berkeley, 209 p. Catalina, due to the low average rate of growth. BODMER, W. F., ANDA. W. F. EDWARDS. P~melometopon pulchrum has three color 1960. and the sex ratio. Ann. Hum. Genet. phases. Juvenile coloration occurs in individuals 24:239-244. usually less than a year old and smaller than 100 BOLIN, R. L. 1930. Embryonic development of the labrid fish Oxyjulis mm in length, and never in sexually mature in• californicus Gunther. Copeia 1930(4):122-128. dividuals. BREDER, C. M., JR., ANDD. E. ROSEN. The uniform coloration is found in immatures' 1966. Modesofreproductioninfishes. Natural History Press, and mature females. Melanization may obscure Garden City, N.Y., 941 p. CHAN,S.T.H. the ground coloration, but it appears that about 5% 1971. Natural sex reversal in vertebrates. Philos. Trans. R. of the mature uniform individuals were males at Soc. Lond., Ser. B, BioI. Sci. 259:59-71. Catalina, and 12% at Guadalupe. CHAN, S. T. H., A. WRIGHT, ANDJ. G. PHILLIPS. Bicolored fishes are exclusively males or late 1967. The atretic structures in the gonads of the rice-field

281 FISHERY BULLETIN: VOL. 73, NO.2

eel (Monopterus albus) during natural sex-reversal. J. (Valenciennes), from the eastern Gulf of Mexico. Fla. Zool. (Lond.) 153:527-539. Dep. Nat. Resour. Mar. Res. Lab., Prof. Pap. 10,95 p. CLARK,F. N. NORRIS,K. S. 1934. Maturity of the California sardine (Sardina caerulea), 1963. The functions of temperature in the ecology of the determined by ova diameter measurements. Calif. Dep. percoid fish Girella nigricans (Ayres). Ecol. Monogr. Fish Game, Fish Bull. 42, 49 p. 33:23-62. CLARKE,T. A. OKADA,Y. K. 1970. Territorial behavior and population dynamics of a 1962. Sex reversal in the Japanese , Halichoeres pomacentrid fish, the garibaldi, Hypsypops rubicun• poecilopterus. Proc. Jap. Acad. Sci. 38:508-513. da. Ecol. Monogr. 40:189-212. OSSIAN,C. R. CROZIER,G. F., JR. 1970. Preparation of disarticulated skeletons using en• 1966. Features of carotenoid metabolism in growth and zyme-based laundry "pre-soakers." Copeia 1970:199-200. sexual maturation of the labrid fish, Pimelometopon QUAST,J. C. pulchrum (Ayres). Ph.D. Thesis, Univ. California, San 1968. 4. Some physical aspects of the inshore environment, Diego, 93 p. particularly as it affects kelp-bed fishes. In W. J. North CUERRIER,J. P. and C. L. Hubbs (editors), Utilization of kelp-bed 1951. The use of pectoral fin rays for determining age of resources in southern California: Calif. Dep. Fish Game, sturgeon and other species of fish. Can. Fish Cult. Bull. 139:25-34. 11:10-18. RANDALL,J. E. DIXON,W. J., ANDF. J. MASSEY,JR. 1955. Stethojulis renardi, the adult male of the labrid fish 1969. Introduction to statistical analysis. 3rd ed. McGraw• Stethojulis strigiventer. Copeia 1955:237. Hill, N.Y., 638 p. REINBOTH,R. FISHER,R. A. 1957. Sur la sexualite' du teleosteen Coris julis (L.). C. R. 1930. The genetical theory of natural selection. The Acad. Sci. Paris 245:1662-1665. Clarendon Press, Oxford, 272 p. 1962. 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Growth characteristics of two southern California RICKER,W. E. surfishes, the California corbina and spotfin croaker, 1958. Handbook of computations for biological statistics of family Sciaenidae. Calif. Fish Game, Fish Bull. 119, 54 p. fish populations. Fish Res. Board Can., Bull. 119,300 p. KALMUSH., ANDC. A. B. SMITH. ROBERTSON,D. R. 1960. Evolutionary origin of and the 1972. Social control of sex reversal in a -reef sex-ratio. Nature (Lond.) 186:1004-1006. fish. Science (Wash., D.C.) 177:1007-1009. KRAFT,A. N., ANDH. M. PETERS. ROEDE,M. J. 1963. Vergleichende Studien iiber die Oogenese in der 1966. Notes on the labrid fish Coris julis (Linnaeus, 1758) Gattung Tilapia (Cichlidae, Teleostei). Z. Zellforsch. with emphasis on dichromatism and sex. Vie Milieu A Mikrosk. Anat. 61:434-485. 17:1317-1333. LIEM,K. F. 1972. Color as related to size, sex, and behavior in seven 1963. Sex reversal as a natural process in the Caribbean labrid fish species (Genera Thalassoma, synbranchiform fish, Monopterus albus. Copeia Halichoeres, and Hemipterinotus). Studies on the Fauna 1963:303-312. of Cura~ao and other Caribbean Islands 138:1-264. 1968. Geographical and taxonomic variation in the pattern ROEDEL,P. M. of natural sex reversal in the teleost fish order 1948. Common marine fishes of California. Calif. Dep. Fish Synbranchiformes. J. Zool. (Lond.) 156:225-238. Game, Fish Bull. 68, 150 p. LoNNEBERG,E., ANDG. GUSTAFSON. ROUNSEFELL,G. A., ANDW. H. EVERHART. 1937. Contributions to the life history of the striped wrasse, 1953. Fisheries science, its methods and applications. John Labrus ossifagus Lin. Ark. Zool. 29A(7):1-16. Wiley and Sons, N.Y., 444 p. McERLEAN,A. J., ANDC. L. SMITH. SMITH,C. L. 1964. The age of sexual succession in the protogynous her• 1965. The patterns of sexuality and the classification of maphrodite Mycteroperca microlepis. Trans. Am. Fish. serranid fishes. Am. Mus. Novit. 2207, 20 p. Soc. 93:301-302. SOWAN, T. MILLER,D. J., ANDR. N. LEA. 1930a. Nestbau eines adriatischen Lippfisches-Crenilabrus 1972. Guide to the coastal marine fishes of California. Calif. ocellatus Forsk. Z. Morpho!. Oeko!. Tiere 17:145-153. Dep. Fish Game, Bull. 157, 235 p. 1930b. Die Fortpflanzung und das Wachstum von MOE,M. A., JR. Crenilabrus ocellatus Forsk., einem Lippfisch des Mit• 1969. Biology of the red , Epinephelus morio telmeeres. Z. Wiss. Zoo!. 137:150-174.

282 WARNER: REPRODUCTIVE BIOLOGY OF PIMELOMETOPON PULCHRUM

SORD!, M. critique of the scale method. Bull. U.S. Bur. Fish. 1962. Ermafroditismo proteroginoco in Labrus turdus L. e 44:265-428. in L. merula L. Monitore Zoo!. Ita!. 69(3-4):69-89. WARNER, R. R. STRASBURG, D. W. In press. The adaptive significance of sequential her• 1970. A report on the billfishes of the central Pacific maphroditism in animals. Am. Nat. 109(965). Ocean. Bul!. Mar. Sci. 20:575-604. WILLIAMS, G. C. 1966. Adaptation and natural selection: A critique of some STRASBURG, D. W., AND R. W. HIATT. current evolutionary thought. Princeton Univ. Press, 1957. Sexual dimorphism in the lab rid fish genus Princeton, 307 p. Gomphosus. Pac. Sci. 11:133-134. YAMAMOTO, K., AND F. YAMAZAKI. VAN OOSTEN, J. 1961. Rhythm of development in the oocyte of the gold-fish, 1929. Life history of the lake herring (Leucichtys artedi Le Carassius auratus. Bull. Fac. Fish., Hokkaido Univ. Seuer) of Lake Huron as revealed by its scales, with a 12:93-110.

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