Download Testing a new version of the size-advantage hypothesis for sex

Behavioral Ecology Vol. 15 No. 1: 129–136
DOI: 10.1093/beheco/arg086
Testing a new version of the size-advantage
hypothesis for sex change: sperm competition
and size-skew effects in the bucktooth
parrotfish, Sparisoma radians
Roldan C. Muñoz and Robert R. Warner
Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara,
Santa Barbara, CA 93106–9610, USA
A variety of field studies suggest that sex change in animals may be more complicated than originally depicted by the sizeadvantage hypothesis. A modification of the size-advantage hypothesis, the expected reproductive success threshold model,
proposes that sperm competition and size-fecundity skew can strongly affect reproductive pay-offs. Size-fecundity skew occurs if
a large female’s fecundity is markedly higher than the aggregate of the other members of her social group and, together with
paternity dilution from sperm competition, can produce situations in which large females benefit by deferring sex change to
smaller females. Deferral by large females can create sex-size distributions characterized by the presence of large females and
small sex-changed males, and it is precisely these distributions that the traditional size-advantage model cannot explain. We
tested the predictions of the new model with the bucktooth parrotfish, Sparisoma radians, on coral reefs in St. Croix, U.S. Virgin
Islands. Collections and spawning observations determined that the local environmental regime of S. radians is characterized by
pervasive sperm competition (accompanying 30% of spawns) and factors that can produce substantial size-fecundity skew in
social groups. Dominant male removal experiments demonstrate that the largest females in social groups often do not change
sex when provided an opportunity. Instead, smaller, lower-ranking females change sex when a harem vacancy arises. This pattern
of sex change is in contrast to virtually all previous studies of social control of sex change in fishes, but provides strong support
for the general predictions of the expected reproductive success threshold model. Key words: coral reefs, Labridae, protogyny,
Scaridae, seagrass beds, size-fecundity skew, social control of sex change, sperm competition. [Behav Ecol 15:129–136 (2004)]
equential hermaphroditism (functioning as male during
one life phase and as female during another) is common
in marine fishes (Francis, 1992; Kuwamura and Nakashima,
1998; Shapiro, 1987; Warner, 1984), with protogyny (sex
change from female to male) predominating. The sizeadvantage model (Ghiselin, 1969; Warner, 1975; Warner
et al., 1975) has been highly successful in explaining the
adaptive significance of sequential hermaphroditism. In
essence, the model proposes that individuals should change
sex if reproductive success increases with size or age more
rapidly for one sex than for the other. Protogyny is predicted
if males gain in reproductive success with size or age faster
than do females (e.g., when large males monopolize matings;
Warner, 1978, 1984, 1988), and protogynous life histories are
frequently found in fishes with haremic social systems in
which dominant males control access to females (Robertson
and Warner, 1978; Ross, 1990; Warner and Robertson, 1978).
In these species, sex change is often under social control
(Fishelson, 1970; Fricke and Fricke, 1977; Robertson, 1972;
Ross et al., 1983; Shapiro, 1980; Warner and Swearer, 1991);
on removal of the dominant male, the largest remaining
female changes sex and takes over the harem (Ross, 1990;
Warner, 1988).
Despite the success of the size-advantage hypothesis in
predicting patterns of sex allocation, a variety of field studies
S
Address correspondence to R.C. Muñoz, who is now at NOAA
Beaufort Laboratory, Center for Coastal Fisheries and Habitat
Research, 101 Pivers Island Road, Beaufort, NC 28516, USA. E-mail:
[email protected].
Received 4 June 2002; revised 12 February 2003; accepted 27
February 2003.
suggest that the process of sex change may be more
complicated than originally depicted by the traditional
hypothesis. For example, in some protogynous fishes, the
largest females do not necessarily change sex when provided
an opportunity (Cole, 1983; Cole and Shapiro, 1995;
Lutnesky, 1994). In many species with clear histological
evidence of the capability of sex change, males may not be
the largest individuals in local populations and may not even
be predominant in the largest size classes (de Girolamo et al.,
1999; Robertson and Warner, 1978). This suggests that the
simplest form of the size-advantage hypothesis is incomplete.
Muñoz and Warner (2003a) proposed a new version of the
size-advantage hypothesis (the expected reproductive success
threshold, or ERST model) in an attempt to reconcile these
anomalous field data with the traditional hypothesis. The
ERST model predicted the probability of an individual
changing sex in local social groups by examining the effects
of sperm competition and size-fecundity skew on expected
reproductive success as a male or as a female. Size-fecundity
skew occurs if a large female’s fecundity is markedly higher
than the aggregate of the other females in her social group.
Since a newly sex-changed individual mates with all remaining
female harem members but no longer reproduces as a female,
size-fecundity skew can create conditions for large females in
which expected reproductive success as a male is actually
lower than current reproductive success as a female. In
addition, paternity dilution from sperm competition lowers
expected male reproductive success but does not change
fitness pay-offs to females. Although unconsidered in previous
models of sex change, sperm competition and size-fecundity
Behavioral Ecology vol. 15 no. 1 International Society for Behavioral Ecology 2004; all rights reserved.
Behavioral Ecology Vol. 15 No. 1
130
skew were found to affect reproductive expectations strongly,
and the model predicted a variety of circumstances in which
the largest females remaining in a social group should not
change sex on disappearance of a dominant male. These same
conditions were found to promote sex change in smaller
females. The model suggested that deferral of sex change
should be more common in species in which intense sperm
competition is prevalent (such as fishes living in or adjacent to
seagrass beds). This prediction was consistent with general
patterns seen in nature (Muñoz and Warner, 2003a), but an
experimental test has been lacking. The purpose of this study
is to test the ERST model for protogynous sex change by
conducting dominant male removal experiments in a system
in which the model predicts that the largest female will defer
sex change to a smaller female. The Caribbean bucktooth
parrotfish, Sparisoma radians, is an ideal species for this test.
Applicability of the ERST model to Sparisoma radians
Sparisoma radians is a monandric (i.e., all males have changed
sex from a prior female phase; Robertson and Warner, 1978)
protogynous parrotfish. It is a common herbivorous fish in
Caribbean seagrass beds and is one of the most abundant
species in this habitat (Lobel and Ogden, 1981; Randall, 1968;
Weinstein and Heck, 1979). Populations of S. radians form
isolated aggregations in seagrass habitats (Ogden and Zieman, 1977; Robertson and Warner, 1978), within which
dominant, brightly colored males in terminal phase (TP)
coloration defend contiguous territories and harems of drab
colored females in initial phase (IP) coloration. These allpurpose territories are used for feeding, mating (external
fertilization), and shelter. In St. Croix, S. radians also occurs
on patch reefs where both large and small males maintain
territories and harems; in patch reef habitats particularly,
individuals can attain extraordinarily large sizes (Muñoz and
Warner, 2003b). In the seagrass, nonterritorial males roam
across territories as ‘‘bachelors’’ and can be either TP or IP
males (those having retained the female coloration; Farm,
1993; Robertson and Warner, 1978). The fish spawn daily each
afternoon (usually between 1500–1730 h) during a 30–90-min
spawning period, and mating tends to be assortative by size
(for further details of reproductive biology, see Farm, 1993).
Territorial males normally spawn singly with a female (pair
spawning) but will occasionally engage in sperm competition
by rushing in and contributing sperm to an ongoing mating
between a neighboring male and female (‘‘streaking’’; Warner
and Robertson, 1978). In contrast, bachelor males nearly
always face sperm competition because most of their matings
involve streaking a larger male and female pair, or group
spawning in which several males mate simultaneously with
a female (Farm, 1993; Marconato and Shapiro, 1996;
Robertson and Warner, 1978). Sparisoma radians shows
a peculiar sexual pattern given its protogynous life history
and haremic social system, characterized by high overlap
between male and female size distributions, with sexually
mature individuals ranging in size from 20–300-mm standard
length (SL) and high-fecundity females occupying the largest
size classes in the population (Robertson and Warner, 1978;
this study) (Figure 1A). Despite their sometimes larger size,
females remain subordinate to the territorial male in their
harem (Muñoz RC, personal observation).
Specifically, S. radians exhibits features identified by the
ERST model that may critically affect the sex change process:
the species resides in habitats that appear to facilitate sperm
competition (i.e., large aggressive males may have difficulty
preventing other smaller males from interfering with spawning because the abundant cover of seagrass allows intruders
to enter or hide very close to a territory and subsequently
parasitize a spawning pair; Robertson and Warner, 1978;
Robertson et al., 1982), and the large size range of mature fish
may allow significant size-fecundity skew in local social groups.
A comparison of seven of the eight members in the genus
Sparisoma (Table 1) shows that S. radians has the largest
mature female size distribution, the highest proportion of
spawns that are streaked, and the largest male gonadosomatic
index (GSI, a measure of the proportion of the body weight
devoted to reproduction and an indicator of sperm competition; see Harcourt et al., 1981; Harvey and Harcourt, 1984;
Marconato and Shapiro, 1996; Møller, 1988; Warner and
Robertson, 1978). Furthermore, within larger comparisons of
parrotfishes and wrasses (n ¼ 12–30 species), S. radians
maintains one of the largest mature female size distributions,
the highest proportion of spawns that are streaked, and the
second largest GSI (Table 1).
To test the ERST model, we determined quantitative
estimates of key demographic features within local social
groups that we then used to direct subsequent dominant male
removal experiments. Our aim was to initiate sex change in
a range of social groups, including those in which the ERST
model predicted sex change by females smaller than the
largest remaining females.
METHODS
Study site
This study took place on patch reefs in Tague Bay (64 359420
W, 17 459450 N) on the northeast coast of St. Croix, U.S.
Virgin Islands, from April–August 1998–2000. A bank barrier
reef bounds Tague Bay to the north (Adey, 1975), and a series
of patch reefs averaging about 1500 m2 in area (Gladfelter and
Gladfelter, 1978) are interspersed throughout a mixed seagrass community. Turtlegrass, Thalassia testudinum, is the
dominant seagrass, whereas varying quantities of manatee
grass, Syringodium filiforme, and shoal grass, Halodule wrightii,
are locally predominant (Robblee and Zieman, 1984). Depths
within the study site range from 2–6 m.
Quantitative estimates of female fecundity and incidence
of sperm competition
Female S. radians were collected with long-handled monofilament hand nets (1.0 3 0.5-m net aperture, 1-cm mesh size)
shortly before the spawning period. Fish were measured for
SL and total length (TL) and weighed to the nearest gram. We
determined female fecundity by expressing their eggs into
graduated tubes for measurement of wet settled volume
following the methods of Schultz and Warner (1989), except
that we washed the eggs with fresh water rather than with
ethanol. Fish were then held in coolers of aerated seawater for
a recovery period of approximately 2 h and subsequently
returned to their home reefs.
To estimate male reproductive success and the incidence of
sperm competition, we conducted daily spawning observations of territorial males. We determined the proportion of
spawns accompanied by interfering males, the frequency of
male mating, and the size and number of females in harems.
We estimated harem size (number of females) from the
location of female home ranges and from the number of
spawns that we observed for a given male, because repeated
spawning observations made on consecutive days showed
good agreement in the daily number of spawns obtained per
male (Muñoz RC, unpublished data). We commenced
spawning observations approximately 30 min before the first
observed spawn of the focal male and concluded the
observations after 30 min had passed without further sexual
Muñoz and Warner
•
Testing a new version of the size-advantage hypothesis
131
activity. We recorded the number of interfering males and the
time for each spawn that occurred.
Experimental procedure
Given the female size-fecundity relationships and incidence of
sperm competition in Tague Bay, we identified local social
groups for which the ERST model (Muñoz and Warner,
2003a) predicted that the largest female should defer sex
change when given an opportunity for such a change via
experimental removal of dominant males. We removed
dominant males from 22 harems on eight patch reefs in an
attempt to initiate sex change in the remaining harem
members. Removals took place outside the spawning period.
We confined our removals to large fish on patch reefs because
the larger size of reef fish, the larger size-skew of reef harems,
and the lower densities of harems on patch reefs (Muñoz and
Warner, 2003b) allowed us to observe the effects of removals
more easily in this habitat than in seagrass.
After removals, we conducted daily searches during the
spawning period, monitoring experimental patch reefs for
sex-changing individuals or roving bachelors attempting to
take over the experimental harems. The rate of bachelor male
arrival decreases across Tague Bay with distance from the
barrier reef, and under natural conditions, roving bachelors
may quickly fill harem vacancies as they arise near the barrier
reef. In contrast, sex-changed males may recruit from within
harems to fill vacancies that arise on more isolated patch reefs
further away from the barrier reef (Muñoz and Warner,
2003b). In the removal experiments, we hoped to increase the
probability that harem takeover would come from within the
reef harem, but our experimental patch reefs were located at
varying distances from the barrier reef. Therefore, bachelors
were removed and transplanted to distant patch reefs when
seen. We identified sex-changing individuals by the initiation
of male behaviors and/or coloration (Muñoz and Warner,
2003b).
Once transitional individuals were identified, they were
observed on a daily basis during the spawning period to
determine the onset of their participation in mating. We
validated our observations of external morphology and male
behavior by tracking the fertilization rate of unstreaked pair
spawns between transitionals and females over several
consecutive days (Muñoz and Warner, 2003b). The onset of
substantial fertilization rates (i.e., more than 80%, approximately the median fertilization rate of unstreaked pair spawns
in nonexperimental fish; Muñoz and Warner, 2003b) was
taken as an indicator of completed sex change. We determined fertilization rates and sperm concentrations by
collecting gametes that were spawned, following procedures
outlined in Shapiro et al. (1994).
To confirm that any sex change observed was the result of
our removals (i.e., to control for spontaneous sex change), we
monitored 14 harems on four additional unmanipulated
patch reefs. We determined the identities of resident fish
through unique natural color markings, individual sizes, and
home range locations. We searched for transitional individuals and took a census of all fish every 3 days for 1 month.
Analyses
Before parametric analyses, data were tested for normality
with the Kolmogorov-Smirnov (Lilliefors’ correction) test and
for homoscedasticity
with the Levene Median test, or transpffiffiffi
formed by 1/ x when necessary.
Figure 1
Sparisoma radians. (A) Sex-size distribution on patch reef habitats
derived from visual censuses. Fish size was determined indirectly by
comparing the size of the focal animal against an object on the reef,
which was later measured. Other studies show that seagrass habitats
contain a higher number of smaller fishes (Robertson and Warner,
1978). (B) Female fecundity (m) versus total length (TL). Exponential
curve fitted to these data: m ¼ 0.263e0.103(TL). Eggs are approximately
590 lm in diameter (Marconato and Shapiro, 1996), and 1 ml of eggs
equals approximately 9300 eggs. Note the log10 y-axis.
RESULTS
Fifty-one female S. radians were sampled for fecundity. These
fish ranged in size from 5.25–22.5 cm TL (mean 6 SE ¼
12.52 6 0.70 cm) and ranged in weight from 2.96–204.4 g
(51.81 6 54.03 g). A strong positive relationship between
female body size and fecundity emerged from these data, with
some larger reef-based females 1.5 to two orders of magnitude more fecund than smaller females (Figure 1B).
Sperm competition is prevalent in the mating system of S.
radians, with 30% of 66 spawns observed on patch reefs
accompanied by interfering streaker males (Muñoz and
Warner, 2003b).
Patterns of sex change and the ERST model
Eight different patch reefs were chosen for experimental
removals, and characteristics of their residents are shown in
Behavioral Ecology Vol. 15 No. 1
132
Table 1
Conditions identified by the ERST model that may affect or be relevant to the expected reproductive success threshold between female
fitness and fitness after sex change to a malea
Sparisoma
radians
Median (range) for
other Sparisomab
Median (range) for other labroids
(parrotfishes and wrasses)c
Mature female size range (mm)
No. of species
160
116 (50130)
6
79 (50160)
23
Percentage of spawns with sperm competition
No. of species
56
1.2 (014.1)
6
3.0 (011.4)
5
Male GSI (100 3 [gonad wt./total body weight])
No. of species
0.76
0.11 (0.060.2)
5
0.15 (0.090.85)
13
a
Conditions were identified in broadcast-spawning scarid and labrid fishes. When more than one male mating type existed in the population (e.g.,
TP and IP), only the largest (TP) male mating type was used. When more than one estimate of proportion of spawns experiencing sperm
competition existed, the largest estimate was used.
b
Other members of the genus Sparisoma include the stoplight parrotfish, Sparisoma viride; redband, S. aurofrenatum; yellowtail, S. rubripinne; redtail,
S. chrysopterum; greenblotch, S. atomarium; and Mediterranean, S. cretense. Data are not available for the remaining member of the genus, the
strigate parrotfish, S. strigatum. Data from de Girolamo et al. (1999), Robertson and Warner (1978), and van Rooij et al. (1996).
c
Labroids for which data are available include the greensnout parrotfish, Scarus spinus; globehead, S. globiceps; surf, S. rivulatus; bridled, S. frenatus;
swarthy, S. niger; queen, S. vetula; chameleon, S. chameleon; palenose, S. psittacus; Schlegel’s, S. schlegeli; striped, S. iserti; bullethead, Chlorurus
sordidus; spinytooth, Calotomus spinidens; bluelip, Cryptotomus roseus; Spanish hogfish, Bodianus rufus; slippery dick wrasse, Halichoeres bivittatus;
puddingwife, H. radiatus; yellowhead, H. garnoti; clown, H. maculipinna; rainbow, H. pictus; blackear, H. poeyi; Creole, Clepticus parrae; bluehead,
Thalassoma bifasciatum; and the Cortez rainbow wrasse, T. lucasanum. Data from Choat and Robertson (1975), Robertson (1981), Robertson et al.
(1982), Warner (1982), Warner and Robertson (1978), and Warner et al. (1975).
Table 2. Harems on control patch reefs showed characteristics
within the range of experimental patch reefs. A total of seven
females from five different patch reefs changed sex after
removal of dominant males (behavioral details of the sex
change process will be reported elsewhere). The most striking
result of the removal experiments was the size of females that
initiated sex change (Table 3). All but one of the sex changers
were smaller than the largest females remaining in the
harems, demonstrating that overall, the largest female S.
radians in local social groups do not change sex. In addition,
the females that changed sex included individuals smaller and
larger than the average size of dominant males, indicating
that large females are physically capable of changing sex but
in certain circumstances appear to defer sex change to smaller
females (Muñoz and Warner, 2003a,b). Harems in which sex
change occurred tended to be larger than harems in which
sex change did not occur (sex change: 5.71 6 0.64 females, n
¼
pffiffiffi7; no sex change: 4.27 6 0.49 females, n ¼ 15; t test on 1/
x transformed data: t ¼ 1.92, p ¼ .069, df ¼ 20).
Equally striking as the pattern of sex change was the lack of
sex change on three of the eight patch reefs (three of 98, two
of 99, and one) and in 15 of 22 experimentally manipulated
harems. In an effort to identify other correlates of sex change,
we quantified the following estimates for harems with and
without sex change: female size and fecundity difference
between smallest and largest females, female aggregate
fecundity, and fecundity skew (for this case only, we refer to
skew in the statistical sense [g1], i.e., the third central moment
divided by the cube of the standard deviation; Sokal and
Rohlf, 1995). Harems without sex change appeared similar to
harems with sex change (for all comparisons, p . .05) (Table
4). When examining entire reefs, there was a trend for reefs
with sex change to harbor a greater number of harems than
did reefs without sex change (sex change reefs: 3.60 6 0.74
harems, n ¼ 5; reefs without sex change: 1.33 6 0.33 harems,
n ¼ 3; t test: t ¼ 2.21, p ¼ .069, df ¼ 6), but it is unclear
whether this is an effect of reef size per se or simply an artifact
of larger numbers of harems on larger reefs.
Because observations continued for 53 days after removal,
well beyond the control reef observations, it is unlikely that
sex change ever occurred in these harems owing to any
experimental manipulation. Instead, remaining females
simply continued spawning with small seagrass or reef TP
males and, in most cases, were incorporated into the harems
of adjacent smaller males. In a few cases, we witnessed large
females making short migrations out of their home ranges to
spawn with males in the seagrass and then returning to the
reef (Muñoz and Warner, 2003b).
Finally, no transitionals were seen during censuses of
unmanipulated control patch reefs, suggesting that our
removals were responsible for the incidences of sex change
observed.
DISCUSSION
Support for the general predictions of the ERST model
Although the protogynous life history of parrotfishes has long
been known (Choat and Robertson, 1975), our removal
experiments provide the first field evidence of social control
of sex change in these common tropical herbivorous fishes
(Muñoz and Warner, 2003b). Dominant male removal experiments in Sparisoma radians demonstrate that in most cases, the
largest females in a harem do not change sex when provided
an opportunity. Instead, smaller lower-ranking females
change sex and fill harem vacancies. This pattern of
protogynous sex change contrasts with virtually all previous
studies of sex change in fishes (for review, see Kuwamura and
Nakashima, 1998; Shapiro, 1984; Warner, 1984; but see Cole,
1983; Cole and Shapiro, 1995; Robertson and Warner, 1978).
Most of these previous studies lend support to the standard
size-advantage model, which has come to be a widely accepted
tenet in evolutionary ecology (Ross, 1990). This traditional
theory, however, cannot adequately explain the presence of
sex change in subordinate individuals.
More recent models of sex change have broadened our
understanding of sex change theory by indicating that
additional factors beyond size can affect reproductive expectations, including costs to sex change itself, differential growth
and mortality, and the magnitude of future reproductive value
relative to current reproductive value. These factors can
generate conditions that favor gonochorism (separate sexes),
Muñoz and Warner
•
Testing a new version of the size-advantage hypothesis
133
Table 2
Local social group characteristics of Sparisoma radians on experimental removal patch reefs
a
b
Reef
No. of
harems
15
13
8
2
3
2/99
3/98
1
5
5
3
1
4
2
1
1
Harem size
Size difference
(cm) between largest
and smallest femalea
Fecundity difference
(ml) between largest
and smallest femaleb
4
4.4
3.6
5
6.5
4.5
7
4
9.88
5.72
1.67
5.2
7.5
4.9
8.12
2.5
54.91
5.63
2.91
7.81
1.88
2.12
5.08
3.93
(0.89)
(0.40)
(0.88)
(1.55)
(0.5)
(2.70)
(0.55)
(1.01)
(1.73)
(1.5)
(36.75)
(1.78)
(2.51)
(0.70)
(1.48)
Values are mean (SE).
Female size was determined either directly by capture and measurement or indirectly by comparing
the size of the focal animal against an object on the reef, which was later measured. Females measured out
of water were immediately returned to their home ranges after measurement.
Fecundity was determined directly as described in Methods or indirectly from the exponential
relationship between fecundity and total length in S. radians (see Figure 1B).
sex change with an extended nonreproductive period
between male and female function, or a decrease in
reproductive effort with size (Charnov, 1986; Iwasa, 1991;
Rogers and Sargent, 2001). The ERST model for protogynous
sex change (Muñoz and Warner, 2003a) generates novel
predictions by indicating that sperm competition and sizefecundity skew can create conditions that inhibit sex change
in large females yet promote sex change in small females; this
mode of sex change can give rise to sexual patterns seen in S.
radians and other fishes (de Girolamo et al., 1999; Robertson
and Warner, 1978) that can be viewed as anomalous by the
traditional size advantage model.
Fishes are believed to show the widest range of sperm
competition for any animal group, ranging from complete
mate monopolization and monogamy to the explosive
breeding of communal spawners, and there is ample evidence
that sperm competition affects the reproductive anatomy and
behavior of fishes (see Petersen and Warner, 1998; Robertson
and Warner, 1978; Stockley et al., 1997; Taborsky, 1998;
Warner and Robertson, 1978). A high incidence of streaking
can dramatically lower male reproductive pay-offs and,
therefore, on a local level should decrease the benefits gained
from protogynous sex change. The level of interference
experienced by S. radians males is high relative to levels
reported for the few other broadcast spawning species for
which data exist. For example, sperm competition accompanies 30% and 56% of spawns on patch reefs in St. Croix
(this study), and in the seagrass in Panama (Table 1),
respectively. In comparison, the stoplight parrotfish, S. viride,
shows the next highest reported level of sperm competition
within the genus Sparisoma; yet, streaking males accompany
only 14.1% of its spawns (van Rooij et al., 1996) (Table 1).
Similarly, the Cortez rainbow wrasse, Thalassoma lucasanum,
shows the highest level (11.4%) of sperm competition
reported for the broadcast spawning wrasses (Warner, 1982);
yet, the proportion of spawns streaked in this species is still
markedly lower than conditions experienced by S. radians
(Table 1). The sex-size distributions of a number of other
species (e.g., bullethead parrotfish, Chlorurus sordidus; puddingwife wrasse, Halichoeres radiatus; redtail parrotfish, Sparisoma chrysopterum) also show high overlap between male and
female size distributions, a feature that seems to be associated
with mating systems in which sperm competition is prevalent
(Muñoz and Warner, 2003a). This suggests that more detailed
studies of the mating systems of a number of these species
may reveal comparable levels of sperm competition to S.
radians, and perhaps deferral of sex change by large females.
If the mature size distribution of a species is sufficiently
large, the relationship between body size and fecundity can
critically affect fitness gain from sex change, because the
aggregate fecundity of remaining females may not exceed the
actual fecundity of a single large female. For example,
fecundity in S. radians increases exponentially with female
body size (note the log y-axis in Figure 1B); combined with
the large size range of mature females, this can result in
significant size-fecundity skew in local social groups. The
ERST model predicts that in these circumstances (regardless
of sperm competition), large females may not change sex.
Importantly, smaller females can still realize an increase in
sex-changed fitness because the aggregate fecundity gained as
a male is more likely to exceed their own fecundity. The size
range of mature females in S. radians is large, similar to other
labroid species with anomalous sex-size distributions (Choat
and Robertson, 1975; de Girolamo et al., 1999; Robertson and
Warner, 1978; Warner and Robertson, 1978). However, it
should be noted that the presence of large females can be
both the cause and the result of deferral of sex change, so
comparisons across species are more difficult here. Overall,
the results of our removal experiments demonstrate strong
Table 3
Removal experiments in Sparisoma radians harems in which sex
change occurred
Female size (cm)
Harem
15FC
13B
13A
8A
8B
2
3C
30.1
30.1
19.2
17.8
16.2
16.2
13.6
21.4
20.0
18.2
17.4
13.8
17.0
16.2
16.2
13.4
12.3
15.5
15.0
14.5
14.0
21.0
20.5
19.4
17.5
17.5
18.1
16.5
15.5
15.3
12.9
13.8
11.3
10.9
10.5
9.3
8.8
8.0
7.5
6.5
Females are arranged in size order, and the individual shown in
bold was the one to change sex.
Behavioral Ecology Vol. 15 No. 1
134
Table 4
Social group characteristics of Sparisoma radians harems with and without sex change
Size difference (cm)
between largest and
smallest female
Fecundity difference
(ml) between largest
and smallest female
Aggregate
fecundity (ml)
Fecundity
skewa
7
6.61 (1.83)
32.38 (27.64)
74.50 (57.17)
0.73 (0.28)
15
6.16 (1.01)
7.30 (3.27)
16.61 (5.45)
0.69 (0.23)
n
Harems with sex
change
Harems without sex
change
a
Values shown are means (SE). Measures of size and fecundity as in Table 2.
Statistical skew (g1, the third central moment divided by the cube of the standard deviation) measured as
in Sokal and Rohlf (1995).
support for the general predictions of the ERST model for sex
change.
Precision of the ERST model
Given the qualitative support for the ERST model, could the
model be used to make specific predictions regarding which
individual in a social group should change sex after dominant
male disappearance? The answer to this question is a qualified
yes, given sufficient information. Three pieces of information
are necessary: (1) local population/harem size, (2) the
incidence and consequences of sperm competition, and (3)
size-fecundity skew of females in the harems. Given these data,
it is possible to calculate expected male and female reproductive success by using formulae generated by the ERST
model (see Muñoz and Warner, 2003a). Briefly, a female’s
instantaneous expected reproductive success equals her
fecundity, and the equivalent maximum reproductive success
she could accrue after sex change equals the aggregate
fecundity of all remaining females in the group. To account
for the effects of sperm competition, sex-changed male
reproductive success must be discounted by the proportion
of spawns that experience sperm competition and the
paternity retained in the presence of sperm competition. In
order for sex change to be favored in the short term, an
individual needs to experience a gain in reproductive success
by changing sex. Because an individual’s ability to dominate
others often depends on its size (Archer, 1987; Taborsky,
1998), we predicted the largest individual out of that subset of
individuals that stands to gain in reproductive success from
sex change (in the short term) should be the one to change
sex (Muñoz and Warner, 2003a).
For S. radians, we lack data on the degree of paternity
retained by a male when faced with sperm competition. By
using an estimate of 50% paternity retained (data from the
bluehead wrasse, Thalassoma bifasciatum; Wooninck LM and
Warner RR, in preparation), the ERST model was precise in
two of the seven harems that experienced sex change (no sex
change occurred in 15 remaining harems, see below). One of
these two cases also happened to be the only instance in which
the largest female changed sex, and this female’s harem
contained the greatest number of females (n ¼ 8), which
appears to facilitate sex change (see below; Cole and Shapiro,
1995). In the other five harems, females even smaller than
predicted by the model changed sex, suggesting that male
paternity expectations may be even lower than we estimated.
Using the ERST model, the observed patterns of sex
change, and female body size-fecundity relationships in S.
radians, it is possible to predict the range of paternity likely to
be obtained by dominant males in the presence of sperm
competition. Paternity values generated in this manner are
very low or even negative (and therefore meaningless),
suggesting again that male paternity is lower than the values
derived from T. bifasciatum. Indeed, the GSIs of interfering IP
male S. radians are larger than those of IP male T. bifasciatum
(3.35 versus 2.71, respectively; Robertson and Warner, 1978;
Warner and Robertson, 1978), suggesting that they may be
more effective in securing fertilizations. Alternatively, these
very low paternity estimates may indicate that other factors,
such as growth rate or mortality differences (see below), may
also influence the decision to change sex. Although progress
has been recently made in paternity estimates for nestbuilding demersal spawners and internal fertilizers under
conditions of sperm competition (Evans and Magurran, 2001;
Fu et al., 2001; Fuller, 1999; Mjølnerød et al., 1998; Munehara
and Takenaka, 2000), there are no other estimates for the
distribution of paternity retained for a broadcast spawning
fish faced with sperm competition, such as S. radians. It is
noteworthy that in substrate-spawning bluegill sunfish, Lepomis macrochirus, dominant males fertilize an average of only
22% of eggs in the presence of sperm competition (Fu et al.,
2001). If such rates are characteristic of S. radians, quite small
females would be those predicted to change sex.
The precision of our predictions may also have been
affected by the fact that the ERST model, as currently
developed, examines male and female reproductive success
at a single point in time, and growth and mortality rates
between the sexes are assumed equal. In fact, there is
evidence of sex-specific growth rates in some species of
parrotfishes, with males being consistently larger than females
at a given age (Choat et al., 1996). Additionally, Clifton and
Robertson (1993) showed that territorial male S. radians in
grassbeds appear to suffer higher predation from roving
yellow jack (Caranx bartholomaei) than do seagrass females.
Higher male mortality might decrease the benefits of sex
change and would favor sex change in smaller females that
have more to gain relative to larger females. On the other
hand, risk of predation probably decreases with size (Colin
and Bell, 1991), so this effect could counter the effect of
higher male mortality. Finally, territorial behavior is known to
increase the risk of predation (Lima and Dill, 1990, and
references therein; Martel, 1996; Martel and Dill, 1995), so
males engaged in territorial defense may experience higher
mortality than females. A dynamic ERST model might
increase its predictive capability by using reproductive value
to examine the effects of differential mortality and growth on
sex change (for an example of such an approach, see Rogers
and Sargent, 2001).
Another factor that the ERST model did not consider is the
effect of roving bachelors on the sex change process.
Aldenhoven’s (1986) work with the bicolor angelfish, Centropyge bicolor, has shown that the frequency of bachelor males
Muñoz and Warner
•
Testing a new version of the size-advantage hypothesis
is negatively correlated with the incidence of female sex
change. Those study sites characterized by a greater number
of bachelors had fewer females immediately change sex and
take over harems after dominant male disappearance,
compared with those other sites where the reverse pattern
prevailed. Similar to these patterns for C. bicolor, in the present
study, there was a decreasing trend across Tague Bay in the
number of days after male removal before the first appearance of a transitional fish; transitionals tend to appear faster
on those patch reefs further away from the barrier reef, where
the frequency of bachelor arrival is lower (Muñoz and Warner,
2003b). This suggests that differing arrival rates of bachelors
across Tague Bay may produce local conditions that facilitate
alternative contexts of sex change and harem takeover, as are
known from Centropyge angelfishes (Aldenhoven, 1986; Sakai,
1997).
Sex change was not induced on all patch reefs
Although sex change in individuals smaller than the
dominant female occurred on most experimental patch reefs,
we cannot be certain why some removals completely failed to
stimulate sex change. A high arrival rate of bachelors might
decrease the probability of sex change in remaining females,
but the three patch reefs without sex change were located far
away from the barrier reef and had a low rate of bachelor
arrival (Muñoz and Warner, 2003b).
Even on patch reefs where sex change did occur, it did not
occur in all harems on these reefs. The difference in size
between the largest and smallest females appeared similar for
harems with sex change and those without sex change (Table
4). However, harems in cases with sex change tended to be
larger than in those harems without sex change. These data
are in concordance with a study of the protogynous bridled
goby, Coryphopterus glaucofraenum, by Cole and Shapiro (1995),
who found that the proportion of groups in which a female
changed sex increased with the number of females in the
group.
Why should some harems experience sex change when
others do not? Aside from larger harem size and variability in
bachelor male arrival, at least two other factors may prevent
sex change in these harems. First, small males present in the
area have two complementary effects: they are already present
and ready to mate, and they can lower a sex-changed male’s
reproductive expectations through sperm competition. Second, after our male removals, females interacted more
strongly with females from other harems than when dominant
males exerted some control over their movements (Muñoz
and Warner, 2003b). Thus, the onset of sex change by the
transitional female may have been communicated to the
group as a whole (through direct contact or water borne-cues;
Cole and Shapiro, 1995). These repression effects cannot
explain the complete lack of sex change observed on other
patch reefs, of course, but these small reefs tended to support
a smaller number of harems than reefs where we witnessed sex
change.
Rather than predicting that some species will defer sex
change and others will not, the ERST conditions suggest
a continuum of social and environmental situations for any
sex-changing species, such that, in some cases, the largest
females will defer sex change. At one end of the continuum
are species such as the protogynous T. lucasanum, in which the
expected reproductive success threshold is seldom crossed,
possibly because most mating takes place in groups with
intense sperm competition. Sex change appears to be
a relatively rare event in T. lucasanum, and the species is
essentially a functional gonochore (Warner, 1982; Warner and
Hoffman, 1980). At the other end of the continuum are
135
species such as the Spanish hogfish, Bodianus rufus, in which
strict male control allows only the largest individuals in local
populations to exceed their ERSTs, and then only in the
absence of the dominant male. In between these two
endpoints are species such as S. radians, in which protogynous
life history combines with reduced male control and habitat
preferences that may expose them to sperm competition.
These factors can create conditions in which small females’
thresholds are sometimes crossed before those of large
females. In these species, females smaller than the dominant
female may change sex, as occurs for S. radians in St. Croix. It
remains to be seen how many additional species in a variety of
geographic locations are similarly affected by sperm competition and size-fecundity skew.
We thank J. Claisse, D. Pinkard, M. Scott, M. Sheehy, S. Swearer, A.
Warner, and L. Wooninck for assistance in the field. J. Reichman and
S. Rothstein provided valuable comments on the manuscript. R.M. was
supported by the Animal Behavior Society, the Lerner-Gray Fund for
Marine Research of the American Museum of Natural History, the
Raney Fund of the American Society of Ichthyologists and Herpetologists, the Explorer’s Club, the Partnership for Interdisciplinary
Studies of Coastal Oceans (PISCO), and the Graduate Division at UC
Santa Barbara. This is PISCO contribution no. 100.
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