Sexual Patterns in the Labroid

Fishes of the Western Caribbean, II:

The Parrotfishes (Scaridae)

D. ROSS ROBERTSON

and

ROBERT R. WARNER

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 255
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SMITHSONIA N CONTRIBUTION S T O Z O O L O G Y • N U M B E R 25 5

Sexual Patterns in the Labroid

Fishes of the Western Caribbean, II:

The Parrotfishes (Scaridae)

D. Ross Robertson

and Robert R. Warner

SMITHSONIAN INSTITUTION PRESS

City of Washington

1978
ABSTRACT

Robertson, D. Ross, and Robert R. Warner. Sexual Patterns in the Labroid

Fishes of the Western Caribbean, II: The Parrotfishes (Scaridae). Smithsonian

Contributions to Zoology, number 255, 26 pages, 12 figures, 6 tables, 1978.—

The interactions of protogynous sex change, coloration, and mating behavior

in ten species of Caribbean parrotfishes are outlined. The species considered are

Cryptotomus roseus, Sparisoma rubripinne, S. chrysoplerum, S. viride, S. aurofrenatum, S. radians, S. atomarium, Scarus vetula, S. croicensis, and S. laeniopterus. For each, we outline (1) the distribution of sexual types according to size

and coloration, (2) the testis weight of different types of males, (3) characteristic

habitat and relative abundance, (4) the social and mating system, and (5) breeding seasonality. Non-sex-changing (primary) males are absent in the sparisomatines but present in the scarinines and prematurational sex change is much more

common among the sparisomatine species. There are also very large overlaps in

size and coloration among the various sexual types of the sparisomatines. Large

testes are present in small males of some species, and this is related to their

interference spawning strategy. In species that do not occur at high density but

do have haremic mating systems, small males are rare or absent. This is probably

due to an increased ability of large males to control spawning in females.

Haremic species are much more common in the parrotfishes than in the wrasses,

perhaps because of basic differences in the distribution of food resources in

time and space.

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recorded in the Institution's annual report, Smithsonian Year. SERIES COVER DESIGN: The coral

Montastrea cavernosa (Linnaeus).

Library of Congress Cataloging in Publication Data

Robertson, D. R.

Sexual patterns in the labroid fishes of the Western Caribbean, II, the parrotfishes (Scaridae).

(Smithsonian contributions to zoology ; no. 255)

Companion volume to Sexual patterns in the labroid fishes of the Western Caribbean, I, the

wrasses (Labridae) by R. R. Warner and D. R. Robertson.

Bibliography: p.

1. Scaridae—Behavior. 2. Sexual behavior in animals. 3. Fishes—Behavior. 4. Fishes—Caribbean Sea. I. Warner, Robert R., joint author. II. Title. III. Series: Smithsonian Institution. Smithsonian contributions to zoology ; no. 255.

QL1.S54 no. 255 [QL638.S3] 591'.08s [59V.58J 77-608162
Contents

Page

Introduction 1

Acknowledgments 1

Materials and Methods 2

Species Studied 2

Study Area 2

Collecting 2

Terminology and Population Parameters 2

Results 2

Cryptotomus roseus 2

Sparisoma rubripinne 3

Sparisoma chrysopterum 5

Sparisoma viride 7

Sparisoma aurofrenatum 8

Sparisoma radians 9

Sparisoma atotnarium • 11

Scarus vetula 13

Scarus croicensis 14

Scarus taeniopterus 16

Discussion 16

General Life History Patterns 16

Testis Size in Relation to Spawning Strategies 17

Social Systems, Mating Systems, and the Success of Different Mating

Strategies 18

Perspective 18

Haremic Species 18

Nonharemic Species 20

Additional Factors 20

Appendix: Tables 23

Literature Cited 26

in

Sexual Patterns in the Labroid

Fishes of the Western Caribbean, II:

The Parrotfishes (Scaridae)

D. Ross Robertson

and Robert R. Warner

Introduction

Reinboth (1968) established the occurrence of

protogyny in certain scarids. Since that time, the

only work on patterns of sexuality in this group

has been Choat's (1969) comprehensive treatment

of sixteen Pacific (Great Barrier Reef) species (published in part in Choat and Robertson, 1975).

Although the basic similarity in the patterns of

sex change exhibited by both wrasses and parrotfishes was discovered by Reinboth (1962, 1968) in

Caribbean scarids, there has been no systematic

and comprehensive examination of sexuality in the

fishes of that area. Whereas Choat's (1969) Pacific

study dealt with scarinine species only, parrotfishes in the Caribbean are all the more interesting

since they have a strong representation from both

scarid subfamilies, the Scarinae and the Sparisomatinae.

This paper comprises the second part of a study

of the patterns of sexuality in Caribbean labroids

(see Warner and Robertson, 1978). In these two

works, we draw together what we have been able

to learn of the patterns of protogyny at the population level, the relationship of permanent color

pattern changes to age, sex, and sex change, and

D. Ross Robertson, Smithsonian Tropical Research Institute,

P.O. Box 2072, Balboa, Canal Zone. Robert R. Warner, Department of Biological Sciences and Marine Science Institute,

University of California, Santa Barbara, California 93106.

the structure of social and mating systems. From

this information, we have attempted a synthetic

treatment of the evolution of protogynous sex

change in these fishes (see also Warner, 1975a;

Warner, Robertson, and Leigh, 1975).

ACKNOWEDGMENTS.—We would like to thank the

government of the Republic of Panama and the

Cuna Indians of the Comarca de San Bias for permitting us to live and work in the San Bias Islands.

Funds and facilities generously supplied by Smithsonian Tropical Research Institute (STRI) and the

Australian Commonwealth Scientific and Industrial

Research Organization (CSIRO) enabled us to do

this work: Robert R. Warner during his tenure as

a STRI postdoctoral fellow and D. Ross Robertson

as a CSIRO postdoctoral student visiting STRI.

Additional funds were provided by the National

Geographic Society and a general research grant

from the University of California, Santa Barbara

(UCSB); the Marine Science Institute at UCSB

aided us with clerical help and computer funds.

The assistance of Isabel Downs and Elizabeth

Fletcher in the field and laboratory was invaluable.

Isabel Downs also drew the figures and provided

technical aid and advice. We were also assisted in

the field by S. Hoffman, D. Diener, N. Davis, G.

Irvine, J. Bryan, and S. Cruz. A. W. Ebeling

and R. H. Rosenblatt read the manuscripts and

provided helpful comments.
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Materials and Methods

SPECIES STUDIED.—We obtained sufficient numbers of the following nine species to enable us to

examine population structures: Cryptotomus roseus,

Sparisoma rubripinne, S. chrysopterum, S. viride,

S. aurofrenatum, S. radians, S. atomariurn, Scarus

vetula, and 5. croicensis. A smaller number of

Scarus taeniopterus were also collected, together

with a very few S. guacamaia, S. coeruleus, and

S. coelestinus. We never saw the one remaining

Caribbean scarid listed by Randall (1968), Nicholsina usta.

STUDY AREA.—Collections and observations were

made in the San Bias islands of Panama, the same

area as referred to in Warner and Robertson

(1978). An additional sample of Sparisoma radians

was collected farther westward at Galeta Point, in

the Canal Zone.

COLLECTING.—Collections and observations were

made throughout the period March 1974-May

1975. As with the labrids (see Warner and Robertson, 1978), we attempted not to take specimens

during periods of sexual activity, in order to reduce

bias in the population samples. Apart from some

trawl collections of small species (principally Sparisoma radians) living in turtle grass beds, specimens

were speared as described in Warner and Robertson

(1978).

TERMINOLOGY AND POPULATION PARAMETERS.—In

this study we follow the same scheme as used for

the labrids (Warner and Robertson, 1978, Appendix 1). When there is more than one distinct adult

color phase, initial phase individuals have that

pattern shown by smaller adults and terminal

phase fish that of the largest males. In fully sexually dichromatic species the terminal phase pattern

contains color elements that are not present in the

initial phase pattern. In partially dichromatic species the patterns of both phases have the same elements but some of them are more strongly developed in the terminal pattern than in the initial

pattern.

For each species, data are presented on: (1) the

degree of sexual dichromatism; (2) the ratio of the

number of initial phase to terminal phase fish in

populations of dichromatic species; (3) the withinpopulation overlap in the size ranges of the two

color phases, based on data obtained from collections and field observations; (4) the presence or

absence of males that are born as such (primary

males) as opposed to males that are sex-changed

females (secondary males) (see Reinboth, 1962, for

criteria for distinguishing these two types histologically; when both types of males are present,

the population is termed diandric, with only one

type, it is monandric, see Reinboth, 1967); and

distributions of the two types of males in the different size classes and color phases; (5) the distribution of recently sex-changed males (i.e., those containing previtellogenic oocytes in their testes) in

the different size classes and color phases; (6) the

absolute and relative (to body weight) weights of

the testes of different classes of males; (7) the overall sex ratio, as determined from a combination

of the color phase ratio and the within-color-phase

sex ratio; (8) the characteristic habitat(s) of the

species; (9) relative abundance, calculated from a

series of counts of all species in a number of habitats, including (a) shallow (<5 m depth of water)

stands of Sargassum, (b) large, shallow (<5 m)

beds of turtle grass (Thalassia and other spermatophytes), and (c) coral reef substrates (coral, coralline rock, and sand patches dotted with coral

growths), this last habitat surveyed on a series of

depth profiles (<3 m, 3-6 m, 6-9 m, 9-12 m,

12-25 m, 15-18 m); (10) observations on the structure of social and mating systems; (11) breeding

seasonality, as determined from observations on

spawning and the collection of ripe females at

various times of the year.

Results

Cryptotomus roseus.—This species is fully dichromatic (see Randall, 1968; and Chaplin and

Scott, 1972, for pattern descriptions). While terminal phase males may rapidly and temporarily

lose virtually all of their characteristic colors, sufficient differences remain to permit their field identification on very close inspection. Terminal phase

males also have distinctly larger heads than initial

phase fish. The color phase ratio was strongly

biased towards the initial phase (Table 1). There

was a moderate degree of within-site overlap in the

size ranges of the two color phases. In six separate

collections (totalling 15 terminal and 63 initial

phase fish), there were two overlaps, each of 1.5 cm

SL. One of those cases, however, involved two
NUMBER 255

50-

40

N 30

20-

10-

CRYPT0T0MUS

Terminal

phase

n = 20

n

rd1 o

2»<JI

n

l

Ph

1

0 0

3 4

n

0

2

i

i1

0

4

ROSEUS

0

9

0

1

n „

0 0

5 1

Initial phase

n = 108

n<f= 12

l°(f

2-(f

-10

0 10 20 30 40 50 60 70 80 90 100

Standard length (K)mm size classes)

FIGURE 1.—Pattern of sexuality in Cryptotomns roseus: size/

frequency bar graph of our sample, with indication of

sexual origin of a number of the males in each size class

(n = total sample size in specified color phase; \° $ —

primary males; 2° $ = secondary males; stippled bars—

females, white bars = males; due to subsampling of more

numerous size groups and losses during processing, the number of males histologically analyzed for sexual origin often

falls short of the total number of males in the sample;

placement of individuals in size classes follows the pattern

of all fishes 20-29 mm SL belonging in the 20 mm size

class).

small transitionally colored terminal phase individuals.

Since all the males we examined were secondary

(Figure 1), C. roseus is evidently monandric. Secondary males were detected in all size classes of

mature initial phase fish, including those well below the size of the smallest terminal phase individuals. The only males with transitional gonads

that we found were two small (61 and 64 mm SL)

terminal phase fish that had not yet fully taken

on terminal coloration. The gonads of initial and

terminal phase males weighed the same absolutely,

but those of the initial pliase males formed a much

higher percentage of body weight (Table 2). The

three smallest terminal phase fish had the relatively

heaviest gonads of any fishes in that color phase.

The sex ratio (Table 1) was moderately biased

towards females, primarily as a result of the scarcity

of initial phase males. We were unable to determine size at maturity because the smallest fish we

collected were sexually active.

Cryptotomus roseus was restricted to shallow

dense turtle grass beds and the broad interfaces of

grass beds and coral reefs. It was one of the least

abundant species, both overall and in the habitats

to which it was restricted (Table 3).

We saw no good evidence of strong permanent

territoriality by members of either color phase.

Initial phase fish moved about in pairs and occasionally in small schools of up to a dozen individuals. Some of those groups also contained a terminal phase male, and we occasionally saw several

such males moving quietly about near each other.

Sexual activity was observed in the early afternoons, when intensely colored terminal phase males

became aggressive to each other. They coursed actively about over areas of up to several hundred

square meters, apparently defending territories.

Fifteen pair spawnings involving such males were

observed, each with a smaller female. There were

no signs of attempted interference by initial phase

males or any indications that group spawning

might occur. The terminal phase male courted

either a single female or an entire small school.

Sexual activity was observed only on the outer

edges of reefs and banks in the habitats normally

favored by the species.

Breeding occurred in all months of the year

(Table 4). Not all females were continuously producing eggs, since we found some large individuals

with inactive ovaries.

Sparisoma rubripinne.—The two color phases of

this species are figured in Randall (1968), Bohlke

and Chaplin (1968), and Chaplin and Scott (1972).

It is fully sexually dichromatic (see Figure 2) and

terminal phase fish appear to be unable to revert

to the initial pattern. The color phase ratio was

moderately biased towards females (Table 1). Direct

observations and a few small collections indicated

that the intrapopulational overlap of the size

ranges of the two phases was exceptionally high.

Three overlaps occurred in seven collections (16

terminal and 43 initial phase fish in total). The

largest overlap was 11.5 cm. Also, as is shown in
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

20-

N 10-

SPARISOMA RUBRIPINNE

Terminal

phase

n=43

.nn ~ n n fi „ 11

P<J 0 0 0 0 000000000 0

1 2 3 I 3 3 I 7 4 2 I I I

Bll H

00000000000 0

14642 2 14 1 12 2

O

I 2°<JI

-10

100 110 120 130 140 150 160 170 180 190 200 210 220 230 240250 260 270 280 290 300 310

Standard length (10mm size classes)

FIGURE 2.—Pattern of sexuality in Sparisoma rubripinne (for explanation of format, see Figure 1).

Figure 2, the largest females and initial phase males

closely approached the largest terminal phase fish

in size.

All males of both color phases proved to be secondary, establishing the monandric status of this

species. Secondary males were also distributed

throughout the entire size range of mature initial

phase fish (Figure 2). Six males with transitional

gonads were collected, four among the smallest size

classes of initial phase males (145-169 mm SL) and

two moderately large fish (235-260 mm SL) in the

terminal phase. The smallest transitional individuals had changed sex prior to maturing as females.

Our samples showed that females are mature beginning at about 160 mm SL. Initial phase males

fell into two distinct classes: males smaller than

200 mm SL had very much smaller testes both absolutely (Figure 3) and relative to body weight,

than did larger males. The gonads of the larger initial phase males weighed much more, both absolutely and relatively, than did those of terminal

phase males (Table 2). In the largest initial phase

males, relative testes weights equaled 6 percent of

body weight, two orders of magnitude greater than

that for terminal phase males.

Due to the strong representation of males in the

initial phase (Figure 2), the sex ratio is not heavily

biased towards females (Table 1).

This species, one of the less abundant scarids,

was distributed throughout the habitats sampled

with the exception of turtle grass (Table 3). Other

observations indicated that it was most commonly

associated with Sargassum beds in areas subject to

heavy wave action, and on turtle grass beds close

to the edges of reefs.

Feeding schools were often encountered. They

consisted of up to 40 fishes of both color phases

and a variety of sizes. This and the overlapping

movement of individual fish strongly suggest that

this species shows no permanent territoriality.

Intensely colored terminal phase males set up

temporary territories and engaged in sexual activity on the peripheries of reefs facing deep water.

The 27 pair spawnings that we observed involved

such males, and occurred at one site in late afternoon. Sexually active males were observed by us
NUMBER 255

4 5 -

4 0 -

3 5 -

3 0 -

-

2 5 -

2 0 -

-

15-

_

, 0 -

5 -

-

SPARISOMA RUBRIPINNE

o Initial phase

• Terminal phase °

o

0

o o

o

o

o

° o

o

©

° o

o

• o

15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31

Standard length (cm)

FIGURE 3.—Gonad weights for various sizes of initial phase and terminal phase males of

Sparisoma rubripinne.

in the mornings in other areas. We observed no

group spawning in this species or any participation

by satellite initial phase males in the pair spawnings of territorial males. However, Randall and

Randall (1963) describe group spawning in aggregations of hundreds of initial phase fish. Initial

phase males were certainly present in the same

areas as sexually active terminal phase fish; we

speared two that were being persistently and vigorously harrassed by territorial males.

Sparisoma rubripinne probably breeds throughout the year, although our data are not quite

complete enough to show it (Table 4). Females

with inactive gonads were also regularly collected.

Sparisoma chrysopterum.—Although Sparisoma

chrysopterum is fully sexually dichromatic (see
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Randall, 1968, for illustrations of the two color

phases), we experience some terminological difficulty in describing the bright all-male phase as a

terminal coloration. Females grow to the same size

as terminal phase males, perhaps even slightly

larger (Figure 4). However, since juveniles bear

the same coloration as initial phase adults, terminal phase individuals, at one time in their lives,

have been in the initial phase. For this reason we

continue to call the bright pattern of large males

the terminal coloration. Terminal phase males did

not appear capable of temporarily regaining the

initial color pattern. The color phase ratio was

quite equable (Table 1). Direct observations and

a series of small collections indicated that the degree of color phase size overlap within a population was high. Overlaps of up to 6.3 cm SL were

found in six of eight collections, comprising 21

terminal and 45 initial phase fish.

Sparisoma chrysopterum is evidently monandric,

since all the males of both color phases that we

examined were secondary (Figure 4). The few initial phase males were restricted to the lower end

of the initial phase size range. Most of those males

also had transitional gonads, as did seven of the

terminal phase males. These terminal phase males

were also quite small individuals (145-194 SL). For

females, the onset of maturity appears to occur

at about 140 mm SL. Secondary males smaller than

the smallest mature females were collected. The

testes of males of both color phases were small,

with no significant size differences between the two

phases (Table 2). Our initial phase male sample,

however, is small and thus does not rule out the

possibility that some such males have large testes.

Although there were few initial males, the sex

ratio was not strongly biased towards females due

to the low color phase ratio (Table 2).

This species was most commonly encountered in

turtle grass beds, typically close by reefs, to which

it retreated when threatened. It was moderately

common overall (Table 3).

Feeding schools of Sparisoma chrysopterum containing up to about a hundred adults of various

sizes and both color phases were commonly seen

in turtle grass areas. We saw no indications of permanent territoriality by members of this species.

In midafternoon, we regularly observed strongly

2 0 -

N 10

SPARISOMA CHRYSOPTERUM

Terminal

phase

n=27

-10

n

I°<J 0 0 0 00000 0 0

2°d* 4 4 2 33211 2 3

Initial phase

n = U8

1 1 1 § 1 1 - "

0 0

I I

0 0

2 I 2°d*

' 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 i r70 80 90 100 110 120 130 140 150 160 170 180 190 200210 220230240 250 260270 280290300

Standard length (10mm size classes)

FIGURE 4.—Pattern of sexuality in Sparisoma chrysopterum •(for explanation of format, see

Figure 1).
NUMBER 255

colored terminal phase males defending temporary

territories scattered along the shallow rims of reefs

in areas of good coralline rock cover. Small groups

of females moved about through the territories of

these males. The males courted them and, on two

occasions that we observed, pair spawned with

them. We never saw anything to suggest that males

of either color phase might interfere in pair spawnings or participate in group spawning.

The species bred during both main seasons

(Table 4), probably throughout the year. Inactive

as well as active females were collected at all times

of the year, indicating a lack of continuous egg

production by females.

Sparisoma viride.—Full sexual dichromatism is

shown by Sparisoma viride (see Randall, 1968, for

color illustrations). Our observations have shown

the terminal coloration is permanent. The color

phase ratio was moderately biased towards the

initial phase (Table 1). There was a high degree

of intrapopulational overlap in the size ranges of

the two phases. We observed this directly and it

is shown by some of our collections: overlaps of

up to 11.2 cm SL occurred in five of seven collections comprising 14 terminal and 73 initial phase

fish.

Reinboth (1968) found that this species is protogynous. Our large sample of males of both color

phases shows that S. viride is monandric (Figure

5). Although males comprised a high proportion

of the smaller initial phase fish, they were absent

from the larger initial phase size classes. Only two

of the males examined had transitional gonads;

one was the smallest terminal phase male obtained

(110 mm SL) and the other a moderate sized terminal phase male (199 mm SL). Females mature

at sizes greater than 160 mm SL. Secondary males

smaller than the smallest mature females were also

obtained. Six males whose terminal coloration had

not yet fully developed were collected; none of

these six had transitional gonads. The size range

of the transitionally colored individuals in our

collection was 130-200 mm SL, on the lowest end

of the terminal phase size range. Larger, similarly

colored fish, however, were seen. Terminal phase

males had testes that weighed much less than those

3 0 -

2 0 -

10-

SPARISOMA VIRIDE

Terminal

phase

n=34

10

n n <-. n n n

pd1 o

2°d* I

0 o

1 i

0 0 0 0 0

2 3 3 3 4

0 0 0

4 2 2

0 0

2 I

., PI 13 i n i-ilLlLlT n hir in..

Initial phase

n * 228

00000000 0

2 1 1 3 3 4 4 3 1

ft

80 90 KX) 110 120 130 140 150 160 170 180 190 200 210 220230240250260270280 290300 310 320330

Standard length (10mm size dosses)

FIGURE 5.—Pattern of sexuality in Sparisoma viride (for explanation of format, see Figure 1).
8

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

of initial phase males, both absolutely and relatively (Table 2). The sex ratio was moderately

biased towards females in this species (Table 1).

Sparisoma viride was largely restricted to coral

reef habitats where it occurred at a variety of

depths (Table 3). It was one of the more abundant

scarids in its main habitat.

Typically we found this species feeding in loosely

knit aggregations of up to twelve fish of both color

phases and a range of sizes, and occasionally in

well-defined schools of up to several hundred

adults. We saw no behavior that would have indicated permanent territoriality by members of this

species.

We frequently observed sexually active terminal

phase males, however, temporarily defending territories on the shallow parts of the outer rims of

reefs. In some instances, there appeared to be more

males than available territories, and the "excess"

formed loose inactive groups a little away from

the territory holders. This territoriality was temporary and restricted to that part of the day when

sexual activity occurred. The timing of sexual

activity varied from site to site, being consistently

in mid to late afternoon at one regularly visited

place, while early morning activity was observed

elsewhere. The earliest spawning seen was at 0745

and the latest at 1700. Twenty-one pair spawnings

involving territorial terminal phase males and

smaller females were noted. Although we saw no

indications of successful sneaking or streaking by

initial phase males, or any group spawning, I.

Downs (pers. comm.) on one occasion saw several

pair spawnings that each involved a {presumed)

initial phase male. Sexually active terminal phase

males often chased initial phase males.

Spawning occurred in both major seasons and

probably throughout the year (Table 4). All females

were not constantly producing eggs, since we collected both active and inactive females in the same

sample on numerous occasions.

Sparisoma aurofrenatum.—Randall {1968),

Bohlke and Chaplin (1968), and Chaplin and Scott

(1972) each provide color illustrations of the two

adult color phases of this species which shows full,

strong sexual dichromatism (Figure 6). We found

no indications that terminal phase males could

temporarily lose their color elements and revert to

the initial pattern. The color phase ratio was one

of the least strongly biased towards initial phase

(Table 1). There was very little within-population

overlap in the size ranges of the two color phases, as

indicated by our field observations and collections.

Only one instance of overlap, of 2 mm SL, occurred

in eight samples totalling 25 terminal and 56 initial

phase fishes.

Sparisoma aurofrenatum is another of the scarids

that Reinboth (1968) found to be protogynous. Our

data show that it is monandric (Figure 6). Males

were too rare in the initial phase to allow us to determine accurately whether they were restricted to

any particular size classes. Four secondary males

with transitional gonads were found, all terminal

phase individuals (119-169 mm SL). The testes of

initial phase males were much heavier, both absolutely and relatively, than those of terminal phase

fish (Table 2). Although the color phase ratio was

one of the more equable among the scarids, the

rarity of males in the initial phase resulted in the

sex ratio being moderately biased towards females

(Table 1). We were unable to determine exact size

at female maturity. It occurs at lengths less than

90 mm SL.

Sparisoma aurofrenatum was restricted to coral

reef areas and their immediate surroundings and

occurred throughout the depth range of that

habitat. It was one of the more abundant species

that we studied (Table 3).

There were strong indications that almost all

terminal phase males of this species were permanently territorial. We never observed these males in

aggregations or schools, and whenever we saw two

together they were almost invariably interacting

agonistically. At common borders, fights between

terminal phase males were regularly seen and these

males appeared to be distributed evenly throughout

their habitat. With initial phase fish, the situation

was less clear, but it appeared that a harem of a few

females of varying sizes lived within the permanent

territory of a larger terminal phase male. This system is similar to that described by Buckman and

Ogden (1973) for Scarus croicensis. We certainly

never saw schools of initial phase fish or more than

about six individuals together in a small area.

Spawning apparently took place within the permanent territories of the terminal phase males.

Sexually active terminal phase males were observed

coursing actively about their territories on the edges

of reefs from midmorning until early afternoon.

We noted 26 pair spawnings involving such males
NUMBER 255

50-

40-

N 30-

20-

10-

i i—

Terminal

phase

n = 53

l°ct

2°ct

J

SPARISOMA AUROFRENATUM

_ _ n

0 0 0

1 5

•

7

0 0

3 1

n

0

3

0

1

1

0

1

c

7

) 0

' 6

•3

n

0

1

1

i°

2

Initial

r

r

cf

0

2

phase

i = 24l

irf=5

0

1

-20

-10

50 60 70 80 90 100 110 120 130 140 150 160 170 180 190200 210 220230240

Standard length (10 mm size classes)

FIGURE 6.—Pattern of sexuality in Sf>arisoina aurofrenatum {for explanation of format, see

Figure 1).

and smaller females, with no indications of attempted participation in them by any other males.

This species was found to be breeding in most

months of the year (Table 4) and probably does so

throughout both main seasons. Females with ovaries

in various states of activity were taken in each of

our collections.

Sparisoma radians.—Randall (1968) provides

color illustrations of the two color phases of this

species. Although it is fully sexually dichromatic,

we encounter the same terminological problem as

experienced with Sparisoma chrysopterum: initial

phase fishes grow to the same size as terminal phase

males, perhaps even larger than them (see Figures

7, 8; in the two samples collected at Galeta Point

and San Bias the size range of terminal phase individuals is completely contained in the size range of

the initial phase). For the same reasons as given for

Sparisoma chrysopterum, however, we retain the

color pattern classification. Although terminal

phase males evidence temporary fading of their

brighter color elements, thus strongly resembling

initial phase fish, the two can be distinguished on

close inspection. Terminal phase males also have

more heavily built heads than most initial phase

fish. The color phase ratio, based on two large trawl

collections, and supported by field observations, was

quite equable (Table 1). These two collections also

showed a very high degree of intrapopulational

overlap in the size ranges of the color phases (Figure 8).

Since, in our large sample covering both color

phases, all the males that we examined proved to

be secondary, Sparisoma radians is monadric. The

few initial phase males encountered were all among

the smaller size classes of that phase (20-60 mm SL).

Only two males with transitional gonads were obtained, both in the largest size class of initial phase

males (both 63 mm SL). Four small males without

fully developed terminal colors were also taken.

Although the gonads of terminal phase males were

slightly heavier than those of initial phase males,
10

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

50-

4 0 -

N 30 -

2 0 -

10-

Terminal

phase

n= 157

i i i i _n i

i°S o o 0 (

n

3 0

2°6* 9 23 20 12

—i

0 0 0

1 5

rr

0

3

J

D

3

SPARISOMA RADIANS

0

2

JL

2«<J

n

0

i

i

i i n „ i i

0

3

i a i a i i i i

0

1

iTil

i

Initial phase

n = 238

ni = 16

50

40

30 N

20

10

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190

Standard length (K)mm size classes)

FIGURE 7.—Pattern of sexuality in Sparisoma radians (for explanation of format, see Figure 1).

they comprised much less of the total body weight

(Table 2). They did weigh more, relative to the

fish's body weight, however, than the gonads of

terminal phase males of any other scarids we examined. Because of the very low color phase ratio,

the sex ratio was less strongly biased towards

females than in any of the other scarid species

(Table 1). Mature females were found among the

smallest individuals collected.

Sparisoma radians was essentially restricted to

shallow beds of dense turtle grass and Sargassum,

although it also extended into the interfaces between these and hard reef areas. Overall, it was one

of the most abundant species (Table 3). Although

we have no specific data, it is our impression that

this species tended to form permanent aggregations,

even within large areas of apparently uniform

habitat.

There were strong indications that some, at least,

of the terminal phase males were permanently territorial, since we repeatedly observed defense of

small (x = 7 m2, n = 13) areas in the same sites

throughout the day. In the same localities, initial

phase fish and less brightly colored nonterritorial

terminal phase fish moved about singly or in small

schools of up to twenty individuals, and were harrassed by the territorial males. It also appeared that

some of the initial phase individuals remained for

a long time in small groups within the territories

of larger terminal phase males.

Sexual activity was observed in midafternoons,

most frequently along the sloping outer edges of
NUMBER 255 11

SPARISOMA RADIANS

40-

20-

20-

10

GALETA POINT

Terminal

n n

n = 103 1~1 I 11 I n Q ^^

nnn n

Initial phase

n = l28

SAN BLAS

Terminal

phas pnasee r-i

n - 2 5 -ni l

Initial phase

n = 39

, n n 1 1 PI n r-i •-. ^-

-40

- 2 0

-20

-10

20 30 40 50 60 70 80 90 100 110 120

Standard length (lOrnm size classes)

FIGURE 8.—Size range overlap between initial and terminal

phase Sparisoma radians within two local populations; initial phase individuals include both males and females.

grass beds, where the species was found at other

times. At such times, territorial terminal phase

males became brighter colored and more strongly

territorial. There was a general influx into the

spawning ground by females, which were often followed by small groups of initial phase males and

nonterritorial terminal phase males. Territorial

males pair spawned with these females. The other

two classes of males group spawned with the

females. Often, males of both color phases were in

one spawning aggregation. Pair spawnings of territorial males were commonly participated in by one

or more other males of either or both color phases.

This occurred in 35 of 62 spawnings observed. Territorial males also commonly interfered in the pair

spawnings of neighboring territory holders. They

would occasionally join in group spawnings, although they often tried initially to disrupt them.

For example, we watched the spawning activity of

three territorial males over three days on one

spawning ground. The three males pair spawned a

total of 29 times, and in 16 of these spawnings suffered interference by other males. These same three

males group spawned 'three times, and six times

they interfered in neighbor's pair spawnings.

Sparisoma atomarium.—Superficially, this species

strongly resembles its congener Sparisoma radians:

both are small, cryptically colored fish of similar

shape that live in association with turtle grass beds.

None of the three recent works that describe and

figure parrotfishes (Randall, 1968; Bohlke andChaplin, 1968; Chaplin and Scott, 1972) illustrate

or even adequately describe the color patterns of

S. atomarium. For this reason, we show the main

characteristics by which these two sibling species

can be distinguished in the field (see Figure 9).

Close observation is often needed before decisions

can be made.

Sparisoma atomarium is fully sexually dichromatic. Terminal phase males can evidence alteration of the intensity of their colors, but evidently

do not revert even temporarily to the initial color

pattern. The color phase ratio was the second most

strongly biased toward the initial phase when compared to that of all other species we examined

(Table 1). There was also very little overlap in the

size ranges of the two color phases within any population. In eight separate population collections,

totalling 27 terminal phase and 78 initial phase

fishes, there were only three instances of overlap,

none of more than 4 mm SL.

Sparisoma atomarium is monandric, since no

primary males were found in the moderate sample

of males examined (Figure 10). Males were also rare

in the initial phase, and apparently restricted to the

upper end of the size range of that phase. No males

with transitional gonads were collected. The sample

size of initial phase males was too small to allow

determination of whether the size of the gonads of

such males differed significantly from those of terminal phase males (Table 2). The sex ratio was

more strongly biased towards females than in any

other species (Table 1), because both terminal

phase and initial phase males were scarce. Mature

females occurred in the smallest size classes that we

collected.
12

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

INITIAL COLOR PHASE

SPARISOMA

RADIANS

TERMINAL COLOR PHASE

opalescent

spot

green area including

fin base

genital papilla pink

body and median fins grey-green

black fin base

body and median fins grey-green;

all shaded areas are black

SPARISOMA

ATOMARIUM

opalescent

spot

yellow fin base genital papilla black dull yellow

fin base

light yellow area

body pink-brown, median fins red; all

shaded areas are black

body and median fins pink-brown, with

three rows of pale opalescent spots

on belly

FIGURE 9.—Distinguishing coloration of Sparisoma radians and S. atomarium.

Although Sparisoma atomarium was found in

dense turtle grass beds, where it mingled with

S. radians, we more often encountered it in the

interfaces between grass and coral reef substrates,

where S. radians was much less common. Overall it

was one of the least abundant species (Table 3).

The social system of this species in many respects

closely resembles that of Sparisoma aurofrenatum.

The site attachment and numerous agonistic interactions of the solitary terminal phase males suggested permanent territoriality. Small groups of

females appeared to restrict their movement to

within the territories of these larger males. In areas

of dense turtle grass stands, where the species

reached its highest densities, we also saw small feeding schools of up to twenty subadult and small

adult intial phase fish. Our collections showed that

these were all females.

The mating system of S. atomarium resembles

that of S. aurofrenatum: terminal phase males

spawn with the females resident in their permanent

territories. Sixty-eight pair spawnings by such territorial males and "their" females were noted, all in

midafternoons. We also observed one pair spawning

by a known initial phase male with a female that

had been responding to an actively courting terminal phase male. We never saw any behavior that

suggested that group spawning was likely to occur.
NUMBER 255 13

50-

40-

N 30 -

20

10-

SPARISOMA

Terminal

phase

n = 44

1

2

r, fl

°<f 0

•rf 3

i

p p

0

i

ATOMARIUM

-|

0

18

0

1

II

0

9

n -

Initial phase

n = 100

no* = 2

2°ct

- 2 0

10

0 10 20 30 40 50 60 70 80 90 100 110

Standard length (10mm size classes)

FIGURE 10.—Pattern of sexuality in Sparisoma atomarium (for explanation

of format, see Figure 1).

This species spawned throughout the wet season

and during much of the dry, probably throughout

the year (Table 4). Not all females, however, were

continuously producing eggs.

Scarus vetula.—Scarus velula is fully sexually

dichromatic, with no indication that terminal

phase males can temporarily lose their characteristic colors. Randall (1968), Bohlke and Chaplin

(1968), and especially Chaplin and Scott (1972) provide color illustrations of the two phases. Initial

phase fish were about four times as common as

terminal phase fish (Table 1). The few data we

have show the within-site overlap in the size ranges

of the two phases to be low (two overlaps, one of

2.4 cm SL, in five collections of six terminal and

24 initial phase fish). We occasionally saw, but

could not catch, smaller terminal phase fish.

This species is diandric (Figure 11). Although

primary males were quite rare, we found them in

both color phases. No secondary males with transitional testes were collected and no secondary males

were found in the initial phase. Although we obtained only a small sample of initial phase males,

their testes were much heavier than those of terminal phase males (Table 2). The single terminal

phase primary male's testis was the same size as

those of secondary males. The sex ratio was moderately biased towards females, mainly due to the

rarity of initial phase males (Table 1). No mature

females smaller than 140 mm SL were collected.

This species was limited to fairly shallow coral

reef habitats (Table 3). Typically, we found it

along the exposed edges of reefs with heavy sculpturing and many physical complexities. Even in

this habitat it was one of the least abundant scarids.

We never saw any indication of long-term school

formation by any individuals. Initial phase fish

were found dispersed singly throughout the habitat

or in small, transient groups of up to half a dozen

fish of different sizes. Terminal phase males, which
14

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

20-

N 10-

SCARUS VETULA

Terminal

phase

n = l9

n n r-i fl

l°<f 0 0

2

o

d* I 2

i

2° *

-10

n n n

ooo o

2 11 3

Initial phase

n = l32

nd* = 3

100 110 120 130 140 150 160 170 180 190 200 210 220230240250 260270 280 290 300 310 320

Standard length (10mm size classes)

FIGURE 11.—Pattern of sexuality in Scarus vetula (for explanation of format, see Figure 1).

usually occured singly, often engaged in aggressive

interactions that strongly resembled border encounters between neighboring territory holders. Thus it

appears that large terminal phase males hold permanent territories, within which a small group

(3-4) of smaller females lived. Winn and Bardach

(1960) have made a similar suggestion. We also observed smaller, nonterritorial terminal phase males

on the peripheries of territories.

We never observed sexual activity by S. vetula,

although Randall and Randall (1963) report seeing

a terminal phase male pair spawn. The data are too

sparse (Table 4) to make any statements about the

seasonality of its breeding.

Scarus croicensis.—This common and widespread

species has been the subject of research on behavioral ecology and sexuality more than any other

parrotfish, in the Caribbean or elsewhere (Randall

and Randall, 1963; Ogden and Buckman, 1973;

Buckman and Ogden, 1973; Barlow, 1975; Robertson et al., 1976; Warner and Downs, 1977). Although we have dealt with this species in detail

elsewhere, a synopsis is presented here and new

information added where relevant.

A major problem confronts our efforts to examine certain population parameters in this

species: the existence of a complex social system

with significant variation in the composition of the

different social classes. Ogden and Buckman (1973)

first described these distinct behavioral classes.

Warner and Downs (1977) expanded on that work

by making detailed examination of the composition

of each social class in terms of its age and sexual

type. Because the social classes do differ greatly in

composition, it is difficult to sample the population

for such things as sex ratio without knowing the

proportion of the population that each social class

represents. This we have been unable to do, and

therefore our estimates of initial phase male proportions (Table 5) and sex ratio (Table 1) must be

considered rough approximations.

Scarus croicensis is fully and strongly sexually

dichromatic, with no evidence that terminal phase

males are capable of temporarily losing their characteristic color pattern. Under certain conditions,

however, their bright colors can effectively be

masked and become very dull. Randall (1968),

Bohlke and Chaplin (1968), and Chaplin and Scott
NUMBER 255 15

(1972) all contain color illustrations of the two

phases. The color phase ratio was moderately

biased towards the initial phase (Table 1). At several sites, within-site overlap in the size ranges

of the two phases was very low. A few short observations on individually recognizable fish indicate that natural changeovers from the initial to

the terminal coloration can essentially be completed in as little as 10 days.

Scarus croicensis is diandric (Figure 12), with a

high proportion of primary males in both color

phases. Because of differences in the composition

of social classes, we do not know whether the proportion of such males is significantly different in

each phase. Only one secondary male was found

among all the initial phase fish collected; this was

a relatively large fish (100 mm SL) with transitional gonads. Two other males with transitional

gonads were also collected; both were in the process of changing color phase also. The testes of

primary initial phase males weighed much more,

both absolutely and relatively, than those of primary or secondary terminal phase males (Table 2;

see also Warner and Downs, 1977, fig. 4). No

mature females smaller than 40 mm SL were

collected.

This species was common throughout the coral

reef areas that we sampled as well as the interfaces

of coral reefs and turtle grass beds or sand areas.

Overall, it was the most abundant scarid encountered (Table 3).

Three distinct social classes were recognized by

Ogden and Buckman (1973): (1) territorial groups,

composed of a terminal phase male and several

50-

40-

N 30-

20-

10-

Terminal

phase

n=l66

\°6

P

,, ra-Jihl

1 5

0 0

~l

1

4

1

L

4

0

SCARUS CROICENSIS

m n n

- i

9 4 6 13 II

2 8 24 32 19

1

-

16 23 6 0

0 0 0

n l~l PI ^ „

2 2 0 0 0

1 4 6 2 2

Initial phase

n = 231

no1 =56

I

O<J

2-6

50

-40

-30 N

-20

10

40 50 60 70 80 90 100 110 120 130 140 150 160 170

Standard length (10mm size classes)

FIGURE 12.—Pattern of sexuality in Scarus croicensis (for explanation of format, see

Figure 1).
16

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

females, all of which defend a common area (although Ogden and Buckman noted a few males

among the territorial initial phase fish they collected, all 119 initial phase fish that we collected

from harem groups were females); (2) foraging

groups or feeding schools composed of hundreds

of fishes of both color phases, and containing many

initial phase primary males; (3) small stationary

groups, with a composition similar to that of foraging groups. Evidently, there is also considerable

movement of individuals between these classes.

Permanently territorial terminal phase males

pair spawned in their territories, with the females

of their groups and with other females that wandered past. We often saw group spawnings by

small clusters of initial phase males, as well as

satellite males of both color phases participating

in the pair spawnings of territorial terminal phase

males. We also noted a few pair spawnings by

initial phase males. The initial phase male aggregations in which group spawnings occurred were

small and not found as commonly as were those

of some other labroids (see Warner and Robertson,

1978). Considerable amounts of aggression were

directed at such male aggregations by the territorial terminal phase males. Spawning occurred between midday and late afternoon, on the outer

edges of reefs. Whether some terminal phase males

set up temporary spawning territories only for the

duration of a spawning period is not clear, although Barlow (1975) made such an observation

elsewhere in the Caribbean.

Breeding took place throughout the year (Table

4), although not all females were continuously

producing ripe eggs over that period.

Scarus taeniopterus.—The two color phases of

this species, which strongly resemble those of Scarus

croicensis, have been well described (see Randall,

1968; Bohlke and Chaplin, 1968; Chaplin and

Scott, 1972). It is fully sexually dichromatic, as

far as we can tell, and terminal phase males do

not appear to be capable of temporary reversion

to the initial coloration. Reinboth (1968) showed

that this species was protogynous. We collected

few individuals of this species, which was rare in

our study area. The six terminal phase males that

we did collect, (215-265 mm SL) were secondary,

and had small testes (Table 2). The 10 initial

phase fish (173-200 mm SL) were all females. This

was too small a sample to determine if the species

is monandric or diandric.

Our only observations of S. taeniopterus occurred

on a few occasions in 5-15 meters of water on the

outer slopes of reefs with heavy coral growth. The

fish were observed singly, with each terminal phase

male overlapping several females in its range of

movement. This indicates that a harem system may

exist, similar to that of S. croicensis.

Discussion

GENERAL LIFE HISTORY PATTERNS.—In Warner

and Robertson (1978), we have discussed how we

construct life history patterns from the structure

of our samples. In that paper is given further

information on the assumptions involved in this

procedure and the sample structures that we considered would indicate a particular pattern.

The patterns of sex and coloration among the

Caribbean parrotfish are obviously complex. Are

there any instructive generalizations that we might

draw from the results given above?

Two major differences on the subfamily level are

apparent, as well as several minor ones. First, primary males are present in the Scarinae and absent

in the Sparisomatinae (which includes Cryptotomus and Sparisoma). There are enough similarities

between the subfamilies in terms of small male

distribution, behavior, and gonad weight to indicate that the small secondary males of the sparisomatines function much as do the small primary

males in the scarinines. The only scarinine species

in which primary males are known to be absent

is an Indo-Pacific species, Scarus niger. It is sexually monochromatic, while the other eight species

dealt with in detail by Choat and Robertson (1975)

are both dichromatic and diandric.

Secondly, prematurational sex change appears

common in the Sparisomatinae. Although individuals that change sex before maturity spend their

adult lives as males, and are thus functionally analogous to primary males, their gonads are definitely

derived from ovaries. This suggests there has been

a development of secondary gonochorism in these

species, which may have lost their primary males

in the evolutionary past. Very small secondary

males are found in three species of Sparisoma (S.

rubripinne, S. chrysopterum, and S. viride) and

probably occur in several others.
NUMBER 255 17

This consistent pattern of primary male scarinines versus early sex-changed sparisomatines apparently does not hold outside the Caribbean.

Choat and Robertson (1975) found prematurationally sex-changed males in four of the nine

Indo-Pacific scarinine species they examined in

detail.

The Caribbean scarinines have a common,

straightforward life history pattern. All females

appear to change sex if they live long enough;

sex change usually occurs over a small size range,

and is accompanied by color change. Primary

males change from initial to terminal coloration

within this same small size range (however, see

Choat and Robertson, 1975, for other scarinine

patterns).

In contrast, the sparisomatinines show a bewildering array of patterns, often within a single species. In species that have temporarily territorial

males, there are broad size overlaps in both sex

and color phases. Some females do not appear to

change sex at all. This was common in Sparisoma

chrysopterum and S. radians, and may also occur

in S. viride and S. rubripinne. The latter species

may also have males that retain initial coloration

through to maximum size.

Sparisoma aurofrenatum and S. atomarium, the

most strictly haremic species, show a pattern of

sex change reminiscent of that of the scarinines.

All females probably change sex, there are few

initial phase males, and the size differential between initial and terminal phase fishes is usually

quite distinct. Further on, we discuss the reasons

for this consistent pattern in haremic species.

TESTIS SIZE IN RELATION TO SPAWNING STRATEGIES.—In Warner and Robertson (1978) we have

discussed the hypothesis proposed by Robertson

and Choat (1974) and Choat and Robertson (1975)

to account for consistent, and often radical, differences in the size of the gonads of the males of the

two color phases of certain dichromatic labroids.

The hypothesis states that since males of the two

phases have different spawning strategies (group

spawning and other multimale forms by initial

phase males, and single-male spawnings by terminal phase males), selection has favored the development of larger testes in initial phase males. In

a spawning involving more than one male, increased sperm production gives an individual male

a greater share of the fertilization of the eggs of

the female(s) present in the group.

In the Caribbean scarids, the same pattern of

gonad weight differences exists as in the labrids.

Small testes were present in the terminal phase

males of all species except Sparisoma radians. All

initial phase males had large testes relative to body

weight. This was particularly marked in Sparisoma

rubripinne, S. viride, S. aurofrenatum, Scarus

vetula and S. croicensis.

Overall, these data agree with what we know

of the spawning patterns of the individual scarid

species. We have observed pair spawning by the

terminal phase males of all species except Scarus

taeniopterus. Group spawning by the initial phase

males of Sparisoma rubripinne and Scarus croicensis is also known to occur.

The pattern in Sparisoma radians also offers

support for the hypothesis. In this species, both

initial and terminal phase males (territorials included) commonly participate in multimale spawnings and both have large testes. The testes of terminal phase males of this species are relatively

smaller than those of conspecific initial phase

males, but relatively larger than those of terminal

phase males of the other species we examined. This

agrees with the observation that in S. radians,

the terminal phase males are involved in multimale

spawnings far more commonly than are terminal

phase males of other species.

Sparisoma rubripinne presents a particularly

striking pattern in regard to differences in testis

size: the testes of initial phase males increase in

size dramatically after 200 mm SL (Figure 3). The

reason for this increase remains obscure. Warner

and Downs (1977) have considered the interactions

between the expenditures of energy on growth and

gamete production in different sexual identities of

Scarus croicensis. Primary males appear to channel

more energy into growth than hermaphrodites of

the same age. This may enable them to bypass a

relatively unproductive "small male" phase and

become larger, terminal phase males more quickly.

Perhaps an analogous situation exists within the

small initial phase males of Sp. rubripinne: energy

is channeled into growth until a reproductively

profitable size is reached, and only then is energy

devoted to increasing gonad size. Such rapid increases in gonad weight did not occur in the other
18

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

labroid species we studied, which points out the

need for a thorough study of the social and mating

system of this species.

One final point deserves mention: in all the

parrotfish we studied, both sex-changed males and

primary males had large testes while in the initial

phase, and relatively small testes while in the terminal phase. In other words, testicular ontogeny

has little or no effect on testis size. This we also

found to be true in the wrasses (Warner and Robertson, 1978).

SOCIAL SYSTEMS, MATING SYSTEMS, AND THE SUCCESS OF DIFFERENT MATING STRATEGIES.—Perspective:

In the first of these two papers (Warner and Robertson, 1978), we examined the sexuality of nine labrids in the light of our previous discussions of the

evolution of protogyny and the coexistence of different sexual genotypes (Warner, Robertson, and

Leigh, 1975; Warner, 1975a; Robertson and Choat,

1974; Choat and Robertson, 1975). We wanted to

see if there was any necessity to discard, modify, or

expand these ideas. Apart from two species for

which sufficient information was not available

(unfortunately so, since the structure of their populations promises to be quite different from those

of the other species), only one, Clepticus parrae,

did not fit easily into the expected general pattern.

We discussed how C. parrae's atypical pattern of

sexuality might be related to its atypical (for a

labrid) ecology and spawning behavior. How do the

scarids fit into the predicted patterns?

Protogyny is likely to evolve in species in which

sexual selection is acting (Warner, Robertson, and

Leigh, 1975). We have argued that dichotomous

male mating strategies are possible when strong

sexual selection and sex change have led to an

abundance of females relative to the number of

terminal phase males. Territorial terminal phase

males pair spawn with females, and initial phase

males employ several mating strategies that depend

on interfering with the pair spawning of these territorial males. They may move unnoticed into

territories and steal pair spawnings or participate

in them as streakers. When present in large numbers, they often intercept females enroute to a

territorial male and induce them to group spawn.

Larger populations can have more skewed color

phase ratios than small populations of the same

species (Warner, Robertson, and Leigh, 1975). The

relatively greater numbers of females present in

such large populations lead to greater opportunities

for successful meddling by initial phase males.

Accordingly, initial phase males are common in

large populations and rare in small ones (Warner,

Robertson, and Leigh, 1975).

Robertson and Choat (1974) and Choat and

Robertson (1975) also examined the effect of interspecific differences in the structure of social and

mating systems on the ability of territorial males to

reduce the level of interference by nonterritorial

males in their spawning. They suggested that in

species in which males hold only temporary reproductive territories the anonymity of the individual

may facilitate an interference strategy. In species

with strictly haremic social systems, in which males

are permanently territorial, harem males could

indentify potential intruders and effectively eliminate the possibility of spawning interference. Few

or no small males would be expected in such species.

Haremic Species: Among the Carribbean scarids,

there do not appear to be any species that combine

sexual monochromatism, monandry, and strictly

haremic social and mating systems. In species with

these features (e.g., the labrid Labroides dimidiatus,

see Robertson and Choat, 1974) the male mates

only with the females of his permanent harem.

All members of the population live in such harems,

and there is no evidence of any males employing a

strategy of interference in the spawning activities

of territorial males. Most of the scarids we examined

(Sparisoma aurofrenatum, S. radians, S. atomarium,

the three Scarus species, and possibly Cryptotomus

roseus) apparently do form harem groups. However,

they are dichromatic and initial phase males are

present that have been shown (in some species) to

interfere in the spawning of terminal phase males.

Choat and Robertson (1975) relate the sexual

monochromatism of species of the Labroides dimidiatus type to the pattern of virtually all mating

being within a permanent group: there is, therefore, no selection for a distinctive color pattern

that serves to attract females during spawning

periods. Robertson and Hoffman (in press) amplify

this argument.

In Scarus croicensis, where the populations are

quite dense, haremic terminal phase males have

both intra- and extraharemic matings. Some males

also establish temporary spawning territories. This

puts a premium on attracting females and could
NUMBER 255 19

account for the development of sexual dichromatism

in this species.

In S. croicensis, harem groups constitute large

proportions of the populations we studied. On some

reefs, there were also large numbers of nonharemic

individuals. They apparently could not hold territories because the number of sites available was

limited. These individuals employed an alternative

strategy: swamping territory holders (see Robertson, et al., 1976). Individual initial phase males are

probably excluded from harems by terminal phase

males but can still gain food in the harem's territory

by feeding en masse. The large groups also contain

unattached females, which form a source of extraharemic matings for the harem male. This situation

further facilitates the intrusion of identically colored

initial phase males into the harem territory and

their interference in spawnings.

Of the remaining harem-forming scarids, Sparisoma radians is similar to Scarus croicensis in having

a large nonharemic segment in the population.

Group spawning regularly occurs in both as well.

Not surprisingly, there are high proportions of

initial phase males in this species. Despite these

similarities between Sparisoma radians and Scarus

croicensis, several significant differences exist between them that reflect the interaction of habitat

type, social system, and sex change: (1) the size

overlap of the two color phases is high in Sparisoma

radians and low in Scarus croicensis, and there is

a higher proportion of terminal phase fish in the

former than in the latter; (2) females of the non-sexchanging types (primary females) are strongly represented in Sparisoma radians but absent in Scarus

croicensis because females grow to much smaller

relative size in the latter species (Figures 7 and 12);

(3) haremic terminal phase males of Scarus croicensis

tend only to pair spawn, while those of Sparisoma

radians commonly participate in both single and

multimale spawnings; (4) finally, while in Sparisoma

radians there is a class of nonterritorial terminal

phase fish that employ the same interference spawning strategy as initial phase males, there is no evidence of such a class in Scarus croicensis (some

observations suggest that nonterritorial terminal

phase males of Scarus croicensis may not be breeding: feeding schools of such males have been observed to be indifferent to the spawning activity of

nearby territorial terminal phase males). Interference in spawning is greatly facilitated in Sparisoma

radians by a combination of small territory sizes,

abundant sea grass cover and cryptic coloration of

the nonterritorial males. This allows nonharemic

males to enter or hide very close to a territory, and

only a short dash is necessary to join a spawning.

The same factors also facilitate the streaking of

neighbors' pair spawnings by territorial males. In

Scarus croicensis, territories are much larger and

coral does not provide the same kind of cover.

We have no direct information on the frequencies of group spawning in either species, although

neither formed large nonterritorial male aggregations of the Thalassoma bifasciatum type (see

Warner, Robertson, and Leigh, 1975). We think

that the high frequency of multimale spawning

in Sparisoma radians raises the potential fertility

of small males, which means that more such males

can exist in the population (Warner, Robertson,

and Leigh, 1975). A lack of a pronounced mating

hierarchy among the males and high mating success

of initial phase males would also explain why the

non-sex-changing female morph exists. In the absence of a significant fertility differential between

females and males at all sizes, there would be no

selection to eliminate non-sex-changing females in

favor of sex-changing types (see Warner, 1975a).

Even if the reproductive success of large males was

higher than that of equivalent sized females, this

could be offset by higher mortality rates on such

males; i.e., the average lifetime fecundity of a

female could equal that of a larger, but shorterlived male or hermaphrodite. The brighter colors

and exposed activity during spawning time of terminal phase males could make them more vulnerable to predation and thus bring about such differential mortality rates.

In other species (Sparisoma aurofrenatum, Sparisoma atomarium, Scarus vetula, and probably Scarus

taeniopterus), there is little or no evidence of the

occurrence of nonharemic females and no indications of the occurrence of group spawning. This

latter group also contains very few initial phase

males (Figures 6, 10, and 11). Although the only

spawning interference by initial phase males that

we saw was in Sparisoma atomarium, the large testis

size of initial phase males of Sparisoma aurofrenatum and Scarus vetula (Table 1) indicate to us

that they also use an interference strategy.

We reasoned above that the occurrence of extraharemic matings enables initial phase males to
20

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

interfere in harem males' spawnings. For two reasons, we think that extraharemic spawnings are

uncommon in Sparisoma atomarium, Sparisoma

aurofrenatum, and Scarus vetula: (1) the nonharemic segment of the population appears quite

small and thus few "extra" females are probably

available; (2) the equable color phase ratios of

Sparisoma aurofrenatum and Scarus vetula indicate

that terminal phase males have only small harems

and thus can exert high levels of control over their

females. A low frequency of extraharemic matings

would reduce the chances for initial phase males

to interfere. In species where the harems are characteristically small, the loss of a single spawning is

significant to the dominant male, and strong attempts to prevent them would be expected. This

further lowers the probability of spawning success

for initial phase males. Since the proportion of

initial phase males in a population depends on their

expected reproductive success (Warner, Robertson,

and Leigh, 1975), we would expect few such males

in these three species (Table 5). This does not rule

out the possibility that elsewhere in their geographic ranges these species could be more abundant, with greater spawning opportunities for initial phase males.

Nonharemic Species: Three of the remaining

species, Cryptotomus roseus, Sparisoma rubripinne

and Sparisoma viride, fit the expected general pattern reasonably well. They lack strong harem

forming tendencies and have an abundance of

initial phase males. Initial phase males have been

seen spawning in two of the three species. The abundance of females relative to the number of terminal

phase males (Table 1) suggests that suitable conditions for the initial phase male strategy are present.

Quite distinct differences occur in the structure of

initial phase male populations of Sparisoma rubripinne and Sparisoma viride, however. Males occur

among all size classes of initial phase fish in Sparisoma rubripinne, but are restricted to the smaller

classes in Sparisoma viride. (Sparisoma radians is

similar to Sparisoma viride in this respect.) Why

this is so we cannot say.

The remaining species, Sparisoma chrysopterum,

shows a great deal of similarity to Sparisoma radians

in (1) having the highest proportions of terminal

phase males; (2) having large intrapopulational size

overlaps of the color phases; and (3) apparently

having primary females. However, the pattern in

Sparisoma chrysopterum is not as easily explained.

The abundance of terminal phase males and pronounced size overlap of the two phases suggest that

average fertility differentials between terminal phase

males and females are probably small. There is

no indication that multimale spawning is the predominant mode in Sparisoma chrysopterum, even

though it is not haremic. It is a large species that

does not spawn in small territories in dense grass

beds like Sparisoma radians. Thus conditions highly

favorable to interference in pair spawnings are

absent. Interference seems unlikely as a factor

diminishing the strength of a mating hierarchy of

terminal phase males. A thorough study of the mating system of this species is sorely needed.

Additional Factors: In Warner and Robertson

(1978) we showed that the labrids with lek-type

mating systems and large dense populations had the

highest proportions of males in the initial phase.

We reasoned that this resulted from a mating system based on strong sexual selection. In sex-changing species, this tends to bias the sex ratio heavily

towards females and promotes the development of

an alternative (interference) spawning strategy (see

Warner, Robertson, and Leigh, 1975).

The connection between high population levels

and lek-type mating systems is not as strongly developed in the parrotfishes, probably because of a

more stable and predictable food supply (see below).

Also, actual population densities are probably a less

reliable indicator of relative ability to form leks in

the parrotfishes than in the wrasses. Labrid species

tend to be uniformly smaller in size than most

parrotfishes, and so abundance measures may correlate well with the number of individuals that

gather for spawning. But the large parrotfish species

(such as Sparisoma rubripinne and Sparisoma viride)

would be able to move much larger distances than

small species such as Sparisoma radians or Sparisoma

atomarium. This could explain the poor correlation

between population density and frequency of initial

phase males among the scarids (Table 5).

The mating system, however, remains as a fairly

dependable predictor of initial phase male success.

All species that have strongly developed haremic

mating systems have very low proportions of initial

phase males (Table 5). Large, mobile species that

lack permanent territoriality tend to have many
NUMBER 255 21

initial phase males (e.g., Sparisoma viricle, Sparisoma

rubripinne). In Scarus croicensis, population density

may play a major role. Territoriality is observed in

both males and females (Buckman and Ogden, 1973),

but population density is high enough that many

individuals are not site attached and feed in large

schools, swamping the territory owners (Robertson

et al, 1976). Females from these schools participate

in spawnings with territorial males, and this facilitates interference spawning by initial phase males

(described in greater detail above).

Throughout these two discussions of labroid sexuality we have borne in mind the very real possibility that numerous sexual types can continue to

coexist within a single species because different

types are successful in different habitats. Consider,

for example, the situation in the labrid Thalassoma

bifasciatum, which we described in detail elsewhere

(Warner, Robertson, and Leigh, 1975; Warner and

Robertson, 1978). Terminal phase males are successful in small populations and initial phase males

have greater success in large populations. Planktonic larval dispersal continually redistributes all

types to all habitats, and a polymorphism of sexual

types could be maintained from a mosaic of local

population effects. The composition of sexual types

in a sample population may reflect the overall composition of populations within the area of larval

dispersal, rather than a local selective equilibrium.

Thus we should not necessarily expect significant

reproductive success of a particular sexual type in

a local population chosen at random.

This may be the explanation for the confusing

patterns of such species as Sparisoma chrysopterum

and Sparisoma rubripinne. Rather than seeking a

selective advantage for initial phase males in low

density populations, perhaps we should look elsewhere in the Caribbean for locales that support

larger numbers of the species in question. At such

sites initial phase male success may compensate for

failures elsewhere.

Social control of sex change has been demonstrated in two species of labrids, Labroides dimidiatus (Robertson, 1972), and Thalassoma bifascialum

(see Warner, Robertson, and Leigh, 1975; D. R.

Robertson, unpublished data). In the latter, a color

phase change often accompanies sex change. We

have no reason to doubt that the timing of sex

and/or color change is not controlled externally,

with social factors playing a major part, in many

of the species that we have dealt with here. In a

strictly haremic species, such as L. dimidiatus, the

cue that triggers female's sex change is simple and

clear: the death of the harem male releases the

largest female from his aggressive domination (Robertson, 1972). In species in which social relationships

are not so precisely defined, however, factors leading to sex and color change are probably more

complex. It is quite possible that the large size

overlap in sex and coloration types in some species

is evidence of a lack of precise and effective mechanism relating cues to actual sex change. If fecundity

differentials between males and females are not

large, as may well be the case in species such as

Sparisoma radians, the decline in reproductive output due to an imprecisely timed sex change would

be smaller than in a species with a larger fecundity

differential. Size range overlaps should therefore be

relatively large in species of the former type. In the

more strongly haremic species, the penalties are

probably more severe for imprecise timing because

of the ability of harem males to control outside

males. It is in this type of species that sex and

color phase size range overlaps should be small.

Examples include Sparisoma aurofrenatum, Sparisoma atomarium, Scarus vetula, and Scarus croicensis.

One final point deserves mention. We have

spoken of the social and mating system in each

species as the primary factor shaping the patterns

of sexuality. Although social systems are certainly

the proximate cause of those patterns, social systems are in turn controlled by the distribution in

space and time of the basic resources of food and

shelter. We believe that this is reflected in a major

difference between the scarids and labrids: dichromatic, haremic species are much more common

among the parrotfishes. Scarids are herbivores and

labrids carnivores. Benthic algal resources may be

more predictably available over a small area than

benthic invertebrates or plankton. This would both

encourage the defense of algal resources by a parrotfish and enable it to provide itself with an assured

supply of food in an area of defendable size (see

Schoener, 1968). Permanent feeding territoriality

may thus have permitted the development of

haremic systems (Robertson and Hoffman, in press).

Investigations of the relationships between basic
22 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

resources and social structure are badly needed,

and provide an opportunity for further research.

As our appreciation of the complexity of the

reproductive biology of this group expands so does

the realization that a continuum of types probably

exists between the extreme states of whatever attribute we care to examine (e.g., spawning patterns).

In addition to classifying species in terms of the

sexual types present, we suggest that they should

also be categorized as to (1) whether or not they are

sexually dichromatic, and (2) whether males are

present in both color phases of a dichromatic

species. This is necessary because males in each

phase are employing radically different spawning

strategies. In Table 6, we show the range of sexual

types found thus far in the labroid fishes. Although

it is useful to have reasonably precise terminology

that facilitates distinguishing major trends, we feel

that there is little value in much greater proliferation of verbiage. We suggest that the terms should

be kept to a practical minimum and be as straightforward and self-explanatory as possible. Thought

and discussion should be given to the evolutionary

sources and functions of the types of variations

encountered rather than mere classification of them.

In these two papers we have briefly surveyed

many species; the depth of our understanding of

them is limited by a lack of comprehensive information. More detailed studies will undoubtedly alter

our perspective, but we think it is likely that the

comprehensive (and often highly speculative) arguments that we have proposed will stand in substance. They have been supported by the comparative tests to which we subjected them. The exceptions

have proved especially instructive in pointing out

the conditions under which various mating systems

can operate, and in turn what life history patterns

can result. We have become particularly aware of

the complexity of alternative solutions that are

potentially available.
Appendix

Tables

TABLE 1.—Color phase ratios and estimated adult sex ratios of nine species

of Caribbean scarids (color phase data obtained by tallying the coloration

of individuals encountered in a series of 10 minute swims in suitable habitats; overall sex ratio calculated from color phase ratio and initial phase

sex ratio, the latter data from our collections)

Species

Cryptotomus

Sparisoma

rubripinne

Sparisoma

chrysopterum ... .

Sparisoma

Sparisoma

aurofrenatum ... .

Sparisoma

radians

Sparisoma

atomarium

Scarus

Scarus

croicensis

Number

of counts

10

27

40

20

31

3

8

12

21

Total number

of Individuals

from al l counts

182

989

924

1109

1147

295

355

284

7371

Color phase ratio

Terminal phase:1n1tial phase

1 "7 3

1:4.0

1:2.1

1-4 4

1:3.1

1:1.3

1:6.9

1-3 7

1:5.9

Sex ratio

*:»

1:1.4

1:1.7

1-2 4

1:2.8

1:1.04

1:5.7

1-3 3

1:4.5

TABLE 2.—Testes weights of 10 species of Caribbean parrotfishes, individuals

classified according to coloration and sexual ontogeny (the mean and its

95% confidence interval shown for both absolute testes weights and testes

weights relative to body weight; this relative weight may be read as

percent of body weight; all secondary males used in this tabulation showed

posttransitional gonads)

PHwry rales Secondary males

Gonad weight GU/BH i 100

(g) (percent)

Gonad wight

(g)

GW/BH x 100

(percent)

Sparisoma

atomarium

term

init

• 0.003

• 0.46

0.02

0.11

0.15 • 0.03

0.05 • 0.03

23
24

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 3.—Relative abundance of 10 species of Caribbean parrotfishes measured by habitat (numbers represent fish seen per 10 minutes by observer

swiming along a horizontal transect; these transects were run at the surface

for the first two habitats and along a series of depth profiles for the hard

reef)

Species

Scarus

croicensis

Sparisoaa

radians

Sparisonia

viride

SparisoM

aurofrenatua

Sparisoaa

rubripinne

Sparisona

Sparisoaa

Scarus

vetula

Cryptotoaus

roseus

Total sampling runs

Total sampling

•Inutes

Sessile

31.8

5.0

5

50

Turtle

grass

33.6

5.5

2.3

26

260

< 3

33.0

0.03

8.8

4.0

3.1

1.2

1.7

32

380

3-6

23.6

0.02

6.3

5.5

2.4

.03

0.8

29

410

Hard reef depth profiles (n)

6-9

23.0

0.03

4.6

4.9

2.6

0.4

1.0

16

205

9-12

26.3

5.2

4.6

2.8

0.1

8

95

12-15

28.8

4.4

4.4

2.7

0.2

4

65

15-18

31.5

3.9

4.2

4.8

0.1

2

85

TABLE 4.—Breeding seasonally in 10 species of Caribbean

parrotfishes (+ = male sexual displays observed; + + =

spawning and male sexual displays observed, or ripe females

collected; nd = no data available)

Species

Cryptotoaus

roseus

Sparisoaa

rubripinne ... .

Sparisoaa

chrysopteruw..

Sparisoaa

Sparisoaa

aurofrenatua..

Sparisoaa

radians

Sparisoma

atoaarfua

Scarus

vetula

Scarus

croicensis ... .

Dry season

Jan Feb Mar Apr May Jun

•+•+•+++++• +

++ + +++++ + +4

+•+++++++++ +

+++ + -f+ ++•++ +

nd nd ++•++++ +

•• nd *+ nd nd nd

++++••+++•+ +

Wet

Jul

nd

nd

nd

••

nd

season

Aug Sep

++ nd

nd nd

•4 ++

nd nd

++ •+

Oct Nov Dec

nd nd ++

+• •+ +•

nd nd nd

TABLE 5.—Rank order of abundance within a common habitat, male proportion of initial color phase, and type of

mating system for nine species of Caribbean parrotfishes

Habitat/Species

Sparisoaa radians

Sparisoaa chrysopterua ..

Sparisoaa atoaariun

Cryptotoaus roseus ..... .

Hard reef substrates

Scarus croicensis

Sparisoaa viride

Sparisoaa aurofrenatua ..

Sparisoma rubripinne....

Scarus vetula

Rank order

of abundance

1

2

3

4

1

2

3

4

5

Male proportion

of initial

color phase

.06

.05

.02

.10

.24

.13

.02

.21

.02

Prescence of hareaic

mating system

partial

absent

strong

absent?

partial

absent

strong

absent

strong
NUMBER 255 25

TABLE 6.—Summary of major features of sex and coloration found in 37

species of labroid fishes grouped by families (status: T.P. = terminal phase,

I.P. = initial phase, 1° = primary, 2° = secondary, Premat = prematiirational;

occurence: P = present, A = absent, C = common (more than 10% of stated

color phase), U = uncommon (less than 10% of stated color phase), ? = data

inadequate for firm statement)

Species

LABRIOAE

Bodianus rufus

Coris lulls

Hemipterinotus novacula

Halichoeres biv1 tutus

H. dispilus

H. qarnoti

H poecilopterus

H. poeyi

H. pictus

Pimelometopon pulchrum

Thalassona bifasciatux

T. lucasanun

SCARIDAE

CrvDtotonus roseus

Scams croicensis

S. fonusus

S. forsteri

S. qlobiceps

S. lunula

S. niqer

S. sexvittatus

SparisoM atomarium

S. aurofrenatun

S. radians

S. viride

T.P.

P

P

f

P

P

P

P

P

P

P

9

P

P

P

P

P

P

P

P

P

P

A

P

P

P

P

p

P

P

P

P

P

IV 2V

f U

A U

A? A?

C U

A

U

f

U

I

f

c

F

F

f

/

(

i

(

{

1

/

1

u

u

p

c

u

u

u

?

A

A?

C

U

A?

?

1

A?

A

P

A?

A?

) P

A

\ U

t U

I U

I U

» C

K C

I V

C

A?

C

C

A?

U

C

A

P

C

P?

A

C

C

U

C

C

U

A

U

U

U

A

A

A

A

A

A

2 V

C

C

C

C

C

C

C

C

P

C

c

c

c

c

c

c

c

c

A

C

c

c

c

c

c

c

c

c

c

Pre -

2 V

A

A

A

A

A?

A

A

A

A

P?

A

P

A?

P

P

A?

A

P

P

A

A

A

P

P?

P

P

S

p?

p?

A

A

A?

A?

A

A?

A

A

A

A?

A

A

A

1

i

A?

A

A?

A

A?

A

A?

A

P

P

P?

Authority

Warner and Robertson

Reinboth, 1975

Reinboth, 1975

Warner and Robertson

Reinboth. 1975

Warner and Robertson

Reinboth, 1975

Warner and Robertson

Warner and Robertson

Robertson, 1972

Diener, 1976

Warner, 1975b

K. Heyer, pers. COB

Warner and Hoffnn,

Robertson and Choat.

[this paper]

[this paper]

Choat and Robertson,

Choat and Robertson,

Choat and Robertson,

Choat and Robertson.

Choat and Robertson,

Choat and Robertson,

Choat and Robertson,

Choat and Robertson

Choat and Robertson

[this paper]

[this paper]

[this paper]

[this paper]

[this paper]

[this paper]

[this paper]

1978

m.

1978

, 1978

. 1978

, 1978

, 1978

, 1978

pers. com.

1974

1975

1975

1975

1975

1975

1975

1975

1975

1975
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26


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