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Sexual development and reproductive

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DOI: 10.1007/s00338-007-0304-0

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Coral Reefs (2008) 27:153–163
DOI 10.1007/s00338-007-0304-0
R EP O R T
Sexual development and reproductive demography of the green
humphead parrotWsh (Bolbometopon muricatum)
in the Solomon Islands
R. J. Hamilton · S. Adams · J. H. Choat
Received: 22 March 2007 / Accepted: 19 August 2007 / Published online: 13 September 2007
© Springer-Verlag 2007
Abstract An investigation of the reproductive biology of
the green humphead parrotWsh (Bolbometopon muricatum)
from three areas in the Western Province of the Solomon
Islands revealed that B. muricatum exhibits several features
that diVer from the pattern of reproductive development
observed in most parrotWshes. Unlike most parrotWshes,
histological evidence suggests that the sexual pattern of
B. muricatum is essentially gonochoristic with high inci-
dences of anatomical but non-functional hermaphroditism.
B. muricatum also diVers from other parrotWshes in that all
males pass through an immature female (or bisexual) phase
as demonstrated by all adult testis retaining the ex-ovarian
lumen and peripheral sperm sinuses in the gonad wall.
However, a protogynous diandric reproductive strategy
cannot be excluded given that sampling may have missed
transitional individuals. Marked variation in the demogra-
phy of male B. muricatum between the three locations
examined is considered to reXect variation in historical Wsh-
ing eVort.
Keywords Green humphead parrotWsh ·
Reproductive biology · OverWshing · Solomon Islands
Communicated by Biology Editor M.I. McCormick.
R. J. Hamilton (&)
The Nature Conservancy, Indo-PaciWc Resource Centre,
51 Edmondstone Street, South Brisbane, QLD 4101, Australia
e-mail: rhamilton@tnc.org
S. Adams · J. H. Choat
School of Marine Biology and Aquaculture,
James Cook University, Townsville, QLD 4811, Australia
Introduction
The parrotWshes, now conWrmed as scarine labrids (West-
neat and Alfaro 2005) are recognized as ecologically
important elements of the coral reef Wsh fauna. This stems
from the demonstration that parrotWshes and especially the
larger taxa may have profound eVects on the dynamics of
reef growth and sedimentation (Bellwood 1995a, b; Bell-
wood et al. 2003) and by implication modify the sessile reef
biota including corals. For this reason the larger members
of the parrotWsh fauna are seen as performing an important
functional role on present day coral reefs. The scarines are
a diverse group of reef Wshes containing approximately 96
species. While most attain a moderate size with a modal
maximum total length of 50 cm the group also contains a
suite of eight larger species with total lengths exceeding
75 cm (Choat et al. 2006). Of these the largest is Bolbo-
metopon muricatum an iconic and potentially endangered
reef species, heavily Wshed over much of its range (Hamil-
ton 2003; Donaldson and Dulvy 2004; Dulvy and Polunin
2004). Given the size range and the excavating mode of
feeding this is potentially the most important species in the
functional group of reef Wshes associated with bioerosion,
sediment transport, and coral removal on tropical reefs
(Bellwood et al. 2003). This study provides an introduction
to the biology of this species. The focus is on reproductive
biology as a prelude to more extensive demographic studies
undertaken on B. muricatum. Preliminary studies (Glad-
stone 1986; Hamilton 2004) have identiWed B. muricatum
as a group spawning species, a behavioural trait that is fre-
quently associated with over-exploitation.
In exploited reef Wsh populations sexual ontogeny and
reproductive behaviour are key elements in the develop-
ment of conservation and management protocols. Under-
standing sexual patterns becomes important in harvested
123
154
reef species as the sequence of male development and
recruitment into the reproductive population may inXuence
the response of the population to increased Wshing (Alonzo
and Mangel 2004). ParrotWshes are usually identiWed as
protogynous hermaphrodites with dual male developmental
pathways, monandry and diandry (e.g., Scarus rivulatus:
Choat and Randall 1986). Indeed recent phylogenetic
reconstructions of the scarines have mapped sexual devel-
opmental pathways onto the taxon to produce patterns of
sexual ontogeny characteristic for both genera and higher
taxonomic units (Streelman et al. 2002). Although there is
a long history of studies on parrotWsh sexual ontogeny
(Reinboth 1962, 1967; Choat and Robertson 1975; Robertson
and Warner 1978; Robertson et al. 1982) few details have
been published on the developmental pathways of the
gonads of juveniles for any species. This is critical to the
understanding of sexual patterns in Wshes, especially in
the context of identifying primary and secondary males.
In the absence of such information it has proved diYcult to
make even general distinctions of sexual patterns, such as
gonochorism, as opposed to protogynous hermaphroditism
(Sadovy and Domeier 2005).
A key assumption underlying many previous studies is
that diVerent pathways of male development may be identi-
Wed using morphological features of the testis. Individuals
displaying morphological conWguration of the testis that
includes an internal lumen and peripheral sperm ducts have
been identiWed as secondary males, deWned as those that
have undergone a functional female phase (Sadovy and
Domeier 2005). Species in which the male component con-
sists exclusively of secondary males have been classiWed as
monandric. Testes that had undergone direct development
without passing through a functional female phase have
been identiWed as primary males. Species that harbour both
primary and secondary males have been classiWed as dian-
dric protogynous hermaphrodites. Those with primary tes-
tes alone have been classiWed as gonochorists (Robertson
et al. 1982). Although the parrotWshes have been seen as
primary examples of protogynous reef Wshes displaying
dual male developmental pathways (Choat and Robertson
1975) distinctions have usually been based on gonad mor-
phology. There have been relatively few studies that exam-
ined the details of male developmental pathways (see
Robertson et al. 1982 describing Leptoscarus vagiensis for
an exception).
However, studies on presumed protogynous species
(Sadovy and Domeier 2005) have identiWed two issues.
Firstly, sexual development in protogynous Wshes can be
highly plastic. Secondly, the developmental pathways of
gonads leading to distinctive structural features may not
match the functional sexual pattern of the species con-
cerned. For example, Wshes of the families Serranidae and
Pomacentridae all display a secondary testis structure
123
Coral Reefs (2008) 27:153–163
regardless of the male developmental pathway (Asoh et al.
2001; Adams 2003; Liu and Sadovy 2004). These Wndings
have important implications for sexual classiWcation
schemes in all groups of protogynous Wshes.
The general objectives of this study were to determine:
(1) if individuals that display typical secondary testes pass
through a functional female phase; (2) if all individuals
pass through a prematuration phase of ovarian gonad struc-
ture and organization before developing as functional
males. This involved the histological examination of
gonads of individuals from a broad size range.
The large size, schooling behaviour and nocturnal aggre-
gation of B. muricatum make it a lucrative and highly
prized target of many subsistence and artisanal nighttime
spear Wsheries in the PaciWc (Gillett and Moy 2006). Mate-
rial available from the Western Solomon Islands, where
artisanal nighttime spear Wshing is practiced, provided a
unique opportunity to analyze relatively large samples of
this species (Hamilton 2003). Ethnographic studies show
that in the past two decades the B. muricatum Wsheries in
the Western Solomon Islands have undergone major tech-
nological and cultural changes, moving from subsistence-
based Wsheries to predominantly artisanal-based Wsheries
(Hamilton 2003). Evidence suggests that strong spatial var-
iation in historical Wshing eVort exists among localized
areas that may inXuence demographic and reproductive
characteristics of this species. For this reason a preliminary
investigation was conducted on the spatial variation in
reproductive biology across three sites separated by 10–
40 km.
Materials and methods
Field locations and sample collection
Three sites within the New Georgia Archipelago were sam-
pled in this study (Fig. 1). The Nusabanga and Munda sites
are both located within Roviana Lagoon, while the third
site is located at the western tip of the uninhabited Tetepare
Island. The Munda site (Fig. 1a) detailed here refers to the
continuous and expansive outer barrier reefs at the western
extremity of Roviana Lagoon. The Nusabanga site (Fig. 1b)
begins approximately 5 km east of the Munda Township
and is characterised by inner lagoon, passage and outer reef
drop oV environments. The Tetepare site (Fig. 1c) consists
of passage and outer reef drop oV environments at the
southwestern tip of Tetepare Island. A total of 245 individ-
uals were collected using underwater spearWshing tech-
niques during night time artisanal Wshing trips at the three
sites, Nusabanga, Munda and Tetepare. Fish were collected
from the Nusabanga and Munda sites throughout a 12-
month period from August 2000 to July 2001, whilst the
Coral Reefs (2008) 27:153–163
(a)
(c)
Fig. 1 Map of the New Georgia Group showing the location of the three study sites. a Munda, b Nusabanga, c Tetepare
Tetepare site was sampled in April–June 2001. Upon
returning to the shore, Wsh were measured to the nearest
millimetre (total length, TL) and weighed to the nearest
gram. Gonads were removed and weighed, and if possible,
sex was determined macroscopically. When logistically
possible, gonads were preserved in formaldehyde: acetic
acid: calcium chloride. A sub sample of 103 gonads from a
broad size range of individuals was taken for histological
examination between the months of late December 2000
and July 2001. Prior to December 2000 no suitable gonad
preservative was available in the Weld. Ages of individuals
were obtained from counts of sectioned sagittae removed
from the Wsh and processed in the laboratory (Choat et al.
1996).
Reproductive analysis
A validation of the macroscopic staging using histology
found that the method was accurate only for ripe mature
males and females throughout the sampling year. Accord-
ingly, combinations of histological and macroscopic tech-
niques were used to reproductively stage B. muricatum.
Ninety-two percent (95/103) of the gonads collected for
histology purposes were sampled between January and July
2001, with 72 gonads collected from the Nusabanga area, 1
from Munda and 30 from Tetepare. Proximal, medial and
distal portions of each gonad were histologically processed
155
(b)
to account for any gradients of germinal development along
the gonad length. These tissues were dehydrated in ascend-
ing grades of ethanol, embedded in paraYn wax and sec-
tioned at 5
m and stained with Mayers Haematoxylin and
Young’s eosin–erythrosin (Winsor 1984).
Individuals were histologically classiWed into reproduc-
tive categories based on the germinal cells present and their
state of development. IdentiWcation and terminology of
oocyte stages followed West (1990). Female maturity was
assessed based on the most advanced oocyte present (West
1990). Terminology for spermatogenesis followed Grier
(1981). ClassiWcation of gonadal developmental stages was
adapted from Fennessy and Sadovy (2002). The presence
of anatomical and functional hermaphroditism was investi-
gated following criteria listed in Sadovy and Shapiro
(1987).
Data analysis
Potential diVerences in the operational sex ratios of males
and females sampled from the Munda, Nusabanga and
Tetepare populations were examined by conducting Chi
Tests in Microsoft Excel. Only mature male and female
individuals were used in these comparisons, which are
expressed throughout as M:F. The mean total length (TL)
of mature males and females were compared within and
between the three populations by conducting a two-way
123
156 Coral Reefs (2008) 27:153–163

ANOVA in SigmaStat. The assumptions of homogeneity Ripening female (n = 10, Fig. 3)

of variance and normality were tested in SigmaStat using
the Levene Median test and the Kolmogorov–Smirnov test
respectively. The nature of signiWcant diVerences found by
ANOVA were explored using Tukey’s means comparisons.
DiVerences in the mean gonadosomatic index (GSI)
between mature males and females sampled were investi-
gated using a Mann–Whitney Rank Sum Test (SigmaStat)
since data was non-normal.
Gonads contained previtellogenic and cortical alveolar
oocytes. Considering gonads may regress to this stage
between individual spawning events, it was not possible to
determine whether this stage of the ovary had previously
ovulated or was maturing for the Wrst time (Sadovy and
Colin 1995). Ripening females ranged in size from 555 to
640 mm.

Mature, ripe female (n = 15; Fig. 4a)

Results
Gonads were enlarged and contained previtellogenic, corti-
Description of gonad developmental stages cal alveolar oocytes and vitellogenic oocytes. Mature ripe
individuals ranged in size from 490 to 830 mm. Oocytes
Gonads were bi-lobed and were attached by long mesenter- displayed asynchronous development.
ies to the dorsal wall of the body cavity. Mature male
gonads and ripe female gonads were easily identiWable Hydrated female (n = 8; Fig. 4b)
macroscopically. Ripe ovaries ranged from pale yellow to
dark yellow, and a mass of oocytes was clearly visible Ovaries of hydrated females possessed hydrated oocytes,
when a transverse section of a ripe ovary was cut. Ripe tes- indicating the female was in close proximity to spawning.
tes were white, compact and Wrmer than ripe ovaries, with Previtellogenic and vitellogenic oocytes stages were also
extractable milt. Very small individuals that had no obvious
gonad development (<1 g) were recorded as immature, and
likewise, small individuals that were sampled in August-
mid-December 2000 and could not be accurately staged
macroscopically (Gonads <5 g) were also recorded as
immature.

Inactive bisexual (n = 3; Fig. 2)

The term bisexual used in this context does not imply sex-
ual function, rather, it refers to anatomical hermaphroditism
only (Fennessy and Sadovy 2002). Gonads contained both
spermatogenic and oogenic tissue that was neither atretic
nor mature. These gonads consisted of closely packed pre-
vitellogenic oocytes (Fig. 2a) and spermatocysts in early
spermatogenesis (Stage 1 and 2 spermatocytes) (Fig. 2b). Fig. 3 Ripening female gonad showing the presence of gonia (gn),
Inactive bisexual individuals ranged in size from 540 to previtellogenic perinucleolar (pn) and cortical alveolus (ca) stage
610 mm. oocytes within a female ovary of uncertain maturity

Fig. 2 a An inactive bisexual

gonad showing early
spermatogenic tissue (*) co-
occurring with previtellogenic
oocytes within a female ovary of
uncertain maturity. lu Lumen.
b MagniWed view of (a) showing
spermatocysts of spermatocytes
(sc2) together with
previtellogenic, perinucleolar
stage oocytes (pn) gonia (gn)
and eosinophillic blood cells (bl)

123
Coral Reefs (2008) 27:153–163 157

Fig. 4 Ovary of mature female

Bolbometopon muricatum in
diVerent reproductive stages
including a ripe showing
asynchronous oocyte
development, b hydrated and
c resting. pn perinucleolar stage
oocyte, yg yolk globule stage
oocyte, lu lumen, hy hydrated,
ao atretic vitellogenic oocytes,
ca cortical alveolus

present in most individuals. Hydrated females ranged in

size from 610 to 920 mm.

Mature resting female (n = 1; Fig. 4c)

Mature, resting females were those females that had com-

pleted spawning for a given season. Gonads were domi-
nated by previtellogenic oocytes and widespread atresia
of vitellogenic oocytes was often observed. Intralamellar
muscle bundles in resting ovaries were common. The
mature resting female was 570 mm.

Immature male (n = 1, Fig. 5)

The immature male gonad showed directional male devel-
opment in the form of spermatocysts containing primary
and secondary spermatocytes together with spermatozoa.
This directional male development appeared to be taking
place within an immature female ovary as indicated by only
pre-vitellogenic oocytes present, a thin gonad wall, small
transverse-sectional area and no evidence of previous
spawning in the form of intralamellar muscle bundles and/
or atretic vitellogenic oocytes. Although spermatozoa were
present, it had not yet progressed to the peripheral sperm
sinuses. Therefore the individual was concluded to be an
immature male. The immature male was 590 mm.
Mature ripe male (n = 65; Fig. 6)
Testis of all mature males possessed an ex-ovarian lumen
and peripheral sperm sinuses within the ex-ovarian wall
(Fig. 6a, b). All stages of spermatogenesis were present yet
the testis was dominated by spermatozoa. Spermatozoa
Fig. 5 Gonad of an immature male showing directional male develop-
ment as indicated by spermatocysts of primary (sc1), secondary sper-
matocytes (sc2), together with spermatozoa (sz), within an immature
female ovary. pn Perinucleolar stage oocytes, lu lumen
were never observed in the gonadal lumen. Males under the
size of 650 mm (n = 31) had previtellogenic oocytes (stages
1 and 2) throughout the gonad and often in high abundance
(Fig. 6c). Half of the males in the 650–699 mm size class
(n = 8) had previtellogenic oocytes (chromatin nucleolar
and perinucleolar stages) present throughout the gonad.
However, previtellogenic oocytes were not seen in the testis
of males larger than 700 mm (n = 25). Mature, ripe males
ranged in size from 470 to 1,115 mm.
Size at maturity
Female B. muricatum reach maturity over a broad size
range (Fig. 7a). Whilst females begin to mature at around
500 mm TL, 100% maturity is reached at a much larger size

123
158
Fig. 6 Sections of a mature ripe
testis of a male Bolbometopon
muricatum showing
a ex-ovarian lumen (lu),
b spermatozoa (sz) within
peripheral sperm sinuses (ss) in
the ex-ovarian gonad wall (gw)
and c perinucleolar stage
oocytes (pn) within the testis
lobules
being 700 mm TL. On average, females mature between
550 and 650 mm TL. This estimate of the size of 50%
maturity was further supported by the disproportionate
increase in gonad weight of individuals in this size class
(Fig. 7a). This estimate of 50% maturity represents an age
range of 7–9 years, with 100% female maturity obtained
at 11 years of age (Hamilton 2004). Males also reach
maturity over a broad size range similar to female B.
muricatum (Fig. 7b). However, males appeared to begin
maturing at smaller sizes and younger ages than females.
Mature males were more abundant than mature females in
size classes below 550 mm TL, and the smallest mature
male sampled was a 470 mm 5-year-old while the small-
est mature female observed was a 490 mm 6-year old
(Hamilton 2004). It is noteworthy that the immature Wsh
in Fig. 7 were individuals with no or very little gonad
development, whose gonads were not examined histologi-
cally. Thus, these immature individuals (which were sam-
pled from the Nusabanga region) are likely to include a
combination of small immature males, bisexual and imma-
ture or ripening females.
Variation in the sex speciWc size structure and sex ratio
There was a substantial variation in the sex speciWc size
structures and sex ratios between the three sites sampled.
There was a large degree of overlap in the female and male
size distribution in the Nusabanga population of B. murica-
tum and males showed a bimodal length frequency distribu-
tion, whereby the higher abundances were in the lower size
classes (Fig. 8a). In the Nusabanga population the number
of mature males was signiWcantly greater than the number
of mature females (1.64:1, n = 88,
2 = 5.07, P < 0.05). The
123
Coral Reefs (2008) 27:153–163
sex speciWc length frequency distribution of the Munda
B. muricatum population diVered markedly from the other
two locations in that there was minimal overlap between
the male and female size distribution (Fig. 8b). Further-
more, the sex ratio was not diVerent from 1:1 (1:1.35,
n = 47,
2 = 1.04, P = 0.31). This was in contrast to the sex
ratios from the remaining two locations that were signiW-
cantly male biased. The overlap in the male and female size
distribution from the Tetepare B. muricatum population
was intermediate compared to the remaining two locations
(Fig. 8c). Similar to Nusabanga, the sex ratio in Tetepare
was signiWcantly diVerent from 1:1 in that it was heavily
biased towards males (3.5:1, n = 41,
2 = 10.76, P = 0.001).
There was a signiWcant interaction between the location
sampled and sex in the average size of individuals
(F2,160 = 20.772, P < 0.001). Tukey’s post hoc tests revealed
that males were signiWcantly larger than females in the
Munda (P < 0.001) and Tetepare sites (P < 0.001 but not in
the Nusabanga site (Fig. 9, P < 0.679). The mean size of
males sampled from Nusabanga were signiWcantly smaller
than those sampled at Munda and Tetepare (P < 0.001),
while the mean sizes of males in Munda and Tetepare were
not signiWcantly diVerent. The average size of females did
not diVer signiWcantly between the three regions sampled
(Fig. 9).
Gonadosomatic index and spawning patterns
On average, the median GSI of ripe females was signiW-
cantly greater than that of ripe males (Mann–Whitney U
statistic = 2319.000, T = 7235.000, P < 0.001). Ripe female
gonads could attain up to 7% of body weight, whereas testis
of most males attained only 2% body weight. However,
Coral Reefs (2008) 27:153–163 159

Fig. 7 a Size speciWc percentage (a) 1000

2 1 1 6 5 6 10 12 26 23 12 10 8 6 4 3
frequency distribution of 100
immature Bolbometopon
muricatum (white bars) and
800
mature female B. muricatum 80
(grey bars). b Size speciWc

Mean gonad weight (+/- SE)

percentage frequency
distribution of immature 600

% Frequency
60
B. muricatum (white bars)
and mature male B. muricatum
(grey bars). Black dots indicate
40 400
mean gonad weight (g) §1 SE
for each size class

20 200

0 0

100-149
150-199
200-249

250-299
300-349
350-399

400-449
450-499
500-549

550-599
600-649
650-699

700-749
750-799
800-849

850-899
900-949
Size class (mm TL)

(b) 350
2 1 1 6 5 6 10 15 27 19 9 2 2 2 8 16 11 16 9 4
100

300

80
250

Mean gonad weight (+/- SE)

% Frequency

60 200

150
40

100

20
50

0 0
100-149
150-199
200-249
250-299
300-349
350-399
400-449
450-499
500-549
550-599
600-649
650-699
700-749
750-799
800-849
850-899
900-949
950-999
1000-1049
1050-1099
1100-1049

Size class (mm TL)

four ripe males of intermediate size had comparable GSIs All hydrated females (n = 8) were captured around full
to that of ripe females of similar sizes (Fig. 10). Ripe males moon or at the very beginning of the last lunar quarter, sug-
and females were collected every month during the August gesting that spawning in B. muricatum may have a set lunar
2000–July 2001 sampling period, and hydrated females periodicity, with the majority of individuals spawning
were collected in the months of February–July 2001, that around the full moon.
being on 6 of the 8 months that females were sampled for
histological examination. Seven out of eight hydrated
females were sampled from passage environments (i.e., Discussion
Honiavasa Passage in the Nusabanga area and the unnamed
passage in the Tetepare area) with the eighth hydrated Most of the scarine species examined to date display pro-
female captured on the outer reef. Since hydrated oocytes togynous hermaphroditism with diandric or monandric
are a sign of imminent spawning (Colin et al. 2003) these male pathways (Choat and Robertson 1975; Robertson
preliminary results suggest that spawning typically occurs and Warner 1978; Randall and Bruce 1983; Choat and
in passage habitats, a Wnding that is consistent with Weld Randall 1986). However, relatively few studies have
observations of spawning in this species (Hamilton 2004). conWrmed the processes underlying male developmental

123
160 Coral Reefs (2008) 27:153–163

(a) 14
Nusabanga population
12
inactive bisexual
10 ripening female
mature female
8 mature male
immature male
6

0
475

525

575

625

675

725

775

825

875

925

975

1025

1075

1125
(b) 14 Munda population
12

10

8
N.o. of fish

0
475

525

575

625

675

725

775

825

875

925

975

1025

1075

1125
(c) 14 Tetepare population
12

10

0
475

525

575

625

675

725

775

825

875

925

975

1025

1075

1125

Size class (mm TL)

Fig. 8 a Size frequency distribution of Bolbometopon muricatum size classes (n = 47). Size frequency distribution of B. muricatum from
from the Nusabanga area in 50 mm size classes (n = 91). b Size fre- the Tetepare area in 50 mm size classes (n = 41). Midpoint values of
quency distribution of B. muricatum from the Munda area in 50 mm each size class are shown

pathways through histological analysis that included
immature individuals. In most cases it has been assumed
that a secondary male testis is indicative of these individu-
als passing through a functional female phase. The present
study found no evidence of functional sex change in the
form of transitional individuals. Furthermore, the histologi-
cal evidence of an immature male, the absence of a female
biased sex ratio, coupled with high frequencies of small
males around the size that females mature suggested that
the Solomon Island population of B. muricatum was func-
tionally gonochoristic. However, as the sampling may have
missed transitional individuals, a protogynous diandric
reproductive strategy cannot be excluded. The marked
prevalence of anatomical hermaphroditism in the species
suggests that at least some of individuals in a population
pass through a bisexual phase of development to male, a
feature that occurs in other families of reef Wshes (Sadovy
and Domeier 2005).

123
Coral Reefs (2008) 27:153–163 161

1100 (a) 8
Mean Total Length (mm +/- 1SE)

1000
6

900

GSI
4

800

2
700

600
0
Nusabanga Munda Tetepare 0 200 400 600 800 1000 1200
Location
Total Length (mm)

Fig. 9 Mean size of males (black) and females (white) at each three
locations; Nusabanga, Munda and Tetepare (b) 8

In B. muricatum primary males have the potential to
retain the ex-ovarian lumen from a historic immature
female stage. This combined with the peripheral sperm
sinuses in the ex-ovarian wall gives the testis the same
appearance as that of “true” secondary males that have
functioned previously as a female (Reinboth 1962; Shapiro
and Rasotto 1993). Males that develop directly in many
other protogynous labrids (primary males) have testicular
duct structures entirely diVerent to those males that have
functioned previously as a female (secondary males) (Shap-
iro and Rasotto 1993). Interestingly, the only two other spe-
cies of scarine that have been found to be gonochoristic
share the same mode of male gonadal development via an
immature female ovary, often misleadingly called “premat-
urational sex change” (Leptoscarus vaigiensis, Robertson
et al. 1982; Sparisoma cretense, Girolamo et al. 1999).
Whilst not common in the scarines, this form of testis
development has been described in representatives of the
Serraninae (Hastings 1989; Kingsford and Webb 1992),
Epinephelinae (Siau 1994; Adams 2003), and Pomacanthi-
dae (Kuwaruma and Nakashima 1998). The retention of
a membrane-lined cavity (lumen) and the formation of
peripheral sperm sinuses in the ex-ovarian wall cannot be
used in the diagnosis of protogyny in this group.
The functional signiWcance of the inactive bisexual indi-
viduals in B. muricatum is unclear. This is especially true in
many diandric serranids where inactive bisexual individu-
als attain large sizes (Fennessy and Sadovy 2002) and can
mature to the extent where ripe gametes of both sexes occur
in the one gonad (Sadovy and Colin 1995; Adams 2002).
However, in B. muricatum all inactive bisexual individuals
are around the size at which females Wrst mature. Further-
more, there was histological evidence that some males mature
from an immature female ovary. This suggests that the bisex-
ual stages are intermediate phases in male maturation from
6
GSI
4
2
0
0 200 400 600 800 1000 1200
Total Length (mm)
Fig. 10 a Gonadosomatic index (GSI) values for mature females
(n = 62) versus total length (mm), for Bolbometopon muricatum sam-
pled from Nusabanga, Munda and Tetepare between August 2000 and
July 2001. b GSI values for mature males (n = 104) versus total length
(mm) for B. muricatum sampled from Nusabanga, Munda and Tetepare
between August 2000 and July 2001
immature females. In other words, they represent the begin-
nings of directional development towards male in immature
females. A similar form of bisexuality has been found in
the gonochoristic fairy basslet, Gramma loreto (Asoh and
Shapiro 1997) and the pomacentrid, Dascyllus albisella
(Asoh et al. 2001). Similar to B. muricatum, evidence of
male structures and/or germ cells disappear as females
mature (Asoh and Shapiro 1997; Asoh et al. 2001).
The large overlap in the female and male size structure,
coupled with the high abundance of small males in the
Nusabanga population gave further evidence for gonocho-
rism in B. muricatum (Sadovy and Shapiro 1987; Sadovy
and Colin 1995). However, the Tetepare and Munda
populations showed strong bimodal size distributions, a
characteristic associated with monandric protogynous
hermaphroditism (Sadovy and Shapiro 1987). An analysis
of sex speciWc growth in B. muricatum has found that males

123
162
have signiWcantly faster growth than females from a very
early age. Such sex speciWc diVerences in growth have been
found to create bimodal size distributions in a number of
gonochoristic species and therefore are not a reliable indi-
cator of functional sex change (Sadovy and Shapiro 1987;
Asoh et al. 2001). Furthermore, the age-frequency distribu-
tion of male and female B. muricatum in the Nusabanga
population supports a diagnosis of gonochorism, with
females obtaining the same maximum longevity as males;
despite obtaining far smaller maximum sizes (Hamilton
2004).
The generally larger size of males compared to females
suggests that there is some advantage to being a male when
large. The signiWcantly lower GSI of males compared to
females suggests the advantage may be in reproduction
whereby one male will pair spawn with numerous females.
Similar to protogynous species, large males can often have
greater advantage over small males as they can aggres-
sively defend, and pair spawn exclusively with, a number
of females (Warner 1984). All documented accounts of B.
muricatum spawning report pair spawning between a large
male and female that takes place above a slowly moving
aggregation of B. muricatum (Gladstone 1986; Hamilton
2004). Similar spawning behaviour for the species has been
observed on the Great Barrier Reef (J. H. Choat, personal
observation). The small number of intermediate size males
with comparable gonad GSIs to that of ripe females sug-
gests that some sperm competition in the form of sneaking
may occur. However, this cannot be concluded without fur-
ther behavioural observations of spawning individuals.
Despite the fact that this study found no evidence of
functional sex change, it is possible that sampling may have
missed transitionals at the less sampled locations of Munda
and Tetepare. This issue aside, on the basis of available his-
tological and demographic data, the most parsimonious
hypothesis on the sexual pattern of B. muricatum is that it is
gonochoristic in the Western Solomon Islands. The pres-
ence of anatomical hermaphroditism in B. muricatum at
smaller sizes are likely to represent intermediate phases of
male development from immature females.
Marked variation across sites was seen in the reproduc-
tive demography of B. muricatum in the size structure of
males, presence of bisexual individuals, and the sex ratio.
Males were signiWcantly smaller and bisexuals were only
present in reasonable numbers in the Nusabanga region
compared to the other sites. In addition, highly male biased
sex ratios occurred in the Nusabanga and Tetepare sites yet
the sex ratio was no diVerent from 1:1 in the Munda region.
Sampling bias could have caused the variation in the repro-
ductive demography, and cannot be discounted. Alterna-
tively, diVerences in reproductive demography may be a
result of habitat or movement, or spatial diVerences in his-
torical Wshing eVort. The implications of these location and/
123
Coral Reefs (2008) 27:153–163
or habitat associated diVerence in size and reproductive
structure must await a more complete analysis on age spe-
ciWc demography and abundance patterns in this species.
In conclusion, this study has contributed to our knowl-
edge on the reproductive biology of scarines by showing
that the sexual ontogeny of B. muricatum populations in the
Western Province of the Solomon Islands are essentially
gonochoristic, with some individuals passing through a
bisexual phase of development. The results have made a
signiWcant contribution to the understanding of reproduc-
tion in this group. B. muricatum is the third species of the
family to display gonochorism. Whilst the potential for sex
change cannot be excluded in this species, the results
emphasise that an ex-ovarian lumen in the testis cannot be
used as conclusive evidence of hermaphroditism in the
scarine. Our study has also shown that the reproductive
demographics of B. muricatum populations have consider-
able small-scale variation, which may have resulted from
site-speciWc variations in historical Wshing eVort. However,
the evidence of a Wshing eVect remains equivocal due to the
potential confounding of factors such as habitat and/or
spawning preferences as well as the low sex speciWc sample
sizes in some sites. In order to further understand the eVects
of Wshing on the reproductive demography of B. muricatum
a more complete size range and age structure of this species
needs to be sampled from replicated un-Wshed sites in the
Western Solomon Islands.
Acknowledgments We thank all of the artisanal spearWshermen who
assisted in this study, and are particularly gratefully for the tireless Weld
assistance of Warren Kama and Michael Giningele. We also thank the
National and Provincial Governments of the Solomon Islands and the
Roviana communities for permission to carry out this research. We
thank J. Ackerman, W. Robbins and the histological facility School of
Marine Biology James Cook University for assistance with processing
of reproductive tissues. Finally, we thank Less O’Neill, Anthropology
Department, University of Otago, for producing Fig. 1. Financial sup-
port for this work was provided by The PADI FOUNDATION, The
PADI AWARE Project, The John D. and Catherine P. Macarthur
Foundation (Award # 60243) and a University of Otago PhD Scholar-
ship to Richard Hamilton.
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