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Transactions of the American Fisheries Society
ISSN: 0002-8487 (Print) 1548-8659 (Online) Journal homepage: http://www.tandfonline.com/loi/utaf20
Gray Triggerfish Reproductive Biology, Age, and
Growth off the Atlantic Coast of the Southeastern
USA
Amanda Kelly-Stormer, Virginia Shervette, Kevin Kolmos, David Wyanski,
Tracey Smart, Chris McDonough & Marcel J. M. Reichert
To cite this article: Amanda Kelly-Stormer, Virginia Shervette, Kevin Kolmos, David Wyanski,
Tracey Smart, Chris McDonough & Marcel J. M. Reichert (2017) Gray Triggerfish Reproductive
Biology, Age, and Growth off the Atlantic Coast of the Southeastern USA, Transactions of the
American Fisheries Society, 146:3, 523-538, DOI: 10.1080/00028487.2017.1281165
To link to this article: http://dx.doi.org/10.1080/00028487.2017.1281165
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ARTICLE
Gray Triggerfish Reproductive Biology, Age, and Growth off
the Atlantic Coast of the Southeastern USA
Amanda Kelly-Stormer
1
Graduate Program in Marine Biology, College of Charleston, 205 Fort Johnson Road, Charleston,
South Carolina 29412, USA
Virginia Shervette*
Fish/Fisheries Conservation Lab, Department of Biology and Geology,
University of South Carolina Aiken, 471 University Parkway, Aiken, South Carolina 29801, USA
Kevin Kolmos, David Wyanski, and Tracey Smart
South Carolina Department of Natural Resources, Marine Resources Research Institute,
217 Fort Johnson Road, Charleston, South Carolina 29412, USA
Chris McDonough
South Carolina Department of Natural Resources, Marine Resources Division, 217 Fort Johnson Road,
Charleston, South Carolina 29412, USA
Marcel J. M. Reichert
South Carolina Department of Natural Resources, Marine Resources Research Institute,
217 Fort Johnson Road, Charleston, South Carolina 29412, USA
Abstract
The Gray Triggerfish Balistes capriscus supports fisheries on both sides of the Atlantic Ocean. We utilized
fishery-independent samples to assess the age structure, growth, sex ratio, size and age at maturity, spawning
season, and spawning frequency of the Gray Triggerfish population off the southeastern U.S. Atlantic coast. From
1991 to 2012, 7,685 samples were collected, ranging in FL from 82 to 578 mm and ranging in age from 0 to 13 years.
Our study provides key life history information for an exploited population and is the first to comprehensively
describe age, growth, and reproduction for a Balistes species. We documented that the Gray Triggerfish is sexually
dimorphic, with adult males attaining larger sizes at age and a larger maximum size than females. Sex-specific
growth curves were fitted, yielding the following von Bertalanffy equations: FL
t
= 419[1 –e
–0.54(t+ 0.61)
] for males
and FL
t
= 352[1 –e
–0.94(t+ 0.22)
] for females. This species is characterized by a medium size at maturity (the smallest
mature female was 179 mm FL; the smallest mature male was 183 mm FL) and relatively early age at maturity (the
youngest mature female and male were age 0). Some shifts in population attributes coincided with a period of
increased fishing pressure. Due to tighter regulations on snapper and grouper fisheries, the Gray Triggerfish has
become a more targeted species. Fisheries biologists and managers should continue to evaluate potential impacts
and establish management regulations that consider the region-specific reproductive season, size and age at
maturity, and sex-specific differences in growth documented in this study.
*Corresponding author: shervette@gmail.com
1
Present address: Environmental Resources Management–Southeast, Inc., 200 Wingo Way, Suite 101, Mt. Pleasant, South Carolina 29464, USA.
Received April 20, 2016; accepted January 9, 2017
523
Transactions of the American Fisheries Society 146:523–538, 2017
© American Fisheries Society 2017
ISSN: 0002-8487 print / 1548-8659 online
DOI: 10.1080/00028487.2017.1281165
Triggerfishes (Family Balistidae) occur in almost all the
major oceans (Matsuura 2015). Species from the genus
Balistes support productive fisheries in the Pacific Ocean and
throughout the Atlantic Ocean, north and south of the equator
(Bernardes 2002; Barroso-Soto et al. 2007; NMFS 2009;
Aggrey-Fynn and Sackey-Mensah 2012), and into the
Mediterranean Sea (Kacem and Neifar 2014; Kacem et al.
2015), the Gulf of Mexico (SEDAR 2006), and the
Caribbean Sea (Matos-Caraballo 2012; SEDAR 2013).
Effective fisheries management requires a detailed understand-
ing of the life history strategies of managed species (Chale-
Matsau et al. 2001; King and McFarlane 2003); however, little
published information exists on the reproductive biology, age,
and growth of Balistes spp.
The Gray Triggerfish Balistes capriscus is a moderately
long-lived species that is associated with hard-bottom habitat
along the eastern and western coasts of the Atlantic Ocean and
supports fisheries from as far north as the Mediterranean
(Kacem and Neifar 2014), as far south as Brazil (Bernardes
and Dias 2000), and along both Atlantic coasts (SEDAR 2006;
Aggrey-Fynn 2013). Individuals of this species spend some
time in the water column as juveniles, when they are associated
with Sargassum spp. (Ingram 2001; Wells and Rooker 2004;
Casazza and Ross 2008); eventually, they settle into a more
benthic existence and are most commonly associated with nat-
ural and artificial reefs, rocky outcroppings/hard bottom, and
wrecks. Adult Gray Triggerfish feed diurnally on invertebrate
prey, such as mollusks, crustaceans, and echinoderms (Frazer
et al. 1991; Vose and Nelson 1994; Blitch 2000).
Gray Triggerfish exhibit a relatively unusual mating strategy
in comparison with other medium-sized reef fishes that are
targeted by fisheries. Harem-like reproductive behavior has
been observed in which males construct demersal nests and
perform courtship behaviors (e.g., they change color and circle
the females) to attract multiple females with which to mate
(Simmons and Szedlmayer 2012). After fertilization, parental
care of the demersal eggs by both sexes has been observed.
Typically, a female stays inside the nest and guards the eggs,
while the male guards the territory surrounding the nests. These
behaviors continue until the eggs hatch, which occurs within
24–48 h after fertilization (Simmons and Szedlmayer 2012).
Commercial and recreational fisheries target Gray
Triggerfish in the Mediterranean (Kacem et al. 2015), U.S.
Atlantic (North Carolina through Florida), U.S. Gulf of
Mexico (SEDAR 2006), Brazil (Bernardes and Dias 2000),
and Africa (Aggrey-Fynn and Sackey-Mensah 2012). Fishing
pressure in the USA is relatively high, as the Gray Triggerfish
is one of the top-10 species in terms of average landings (by
weight) within the South Atlantic Fishery Management
Council’s snapper–grouper management complex (unpub-
lished data source cited by Burton et al. 2015). Historical
commercial and recreational annual landings for Gray
Triggerfish in this area increased from near 0 kg in the
1970s to a peak of nearly 200,000 kg in the mid-1990s,
declined to around 90,000 kg in the early 2000s, increased to
over 200,000 kg in 2012, and continue to remain high (NMFS
Sustainable Fisheries Branch 2014a,2014b; Burton et al.
2015). Fishery-independent abundance indices have high-
lighted a corresponding decline in overall population numbers
during 2002–2011 (Figure 1). The Gray Triggerfish continues
to be an important fisheries species in this region.
Several published studies have reported that intense fishing
pressure appears to elicit changes in the life history patterns of
marine fisheries species (Jørgensen 1990; Harris and
McGovern 1997; Morgan and Colbourne 1999; Hunter et al.
2015). Currently, there is no published comprehensive life
history study that has described age, growth, and reproduction
in Gray Triggerfish or any Balistes species. The purpose of the
present study was to utilize fishery-independent samples to
assess the age structure, growth, sex ratio, size and age at
maturity, spawning season, and spawning frequency of the
Gray Triggerfish population off the southeastern U.S.
Atlantic coast.
METHODS
Fish collection and processing.—Gray Triggerfish were
collected through (1) the fishery-independent Southeast Reef
Fish Survey (SERFS) by the Marine Resources Monitoring,
Assessment, and Prediction Program (MARMAP) and the
Southeast Area Monitoring and Assessment Program–South
Atlantic at the South Carolina Department of Natural
Resources (SCDNR) and (2) the Southeast Fishery-
FIGURE 1. Commercial landings of Gray Triggerfish (thousands of
pounds; 1 lb = 0.454 kg) represented by handline data (the predominant
commercial fishery gear for capturing this species) and standardized CPUE
(fish·trap
–1
·h
–1
; ±SE) of Gray Triggerfish in chevron traps (reported by
Ballenger et al. 2013) off the southeastern U.S. Atlantic coast from 1990 to
2012. Rectangles indicate the two periods of interest in the present study:
1994–1997, representing a peak in commercial landings and CPUE; and
2009–2012, representing another peak in commercial landings but a rela-
tively low CPUE.
524 KELLY-STORMER ET AL.
Independent Survey conducted by the National Marine
Fisheries Service’s (NMFS) Southeast Fisheries Science
Center. Fish were obtained with chevron traps from 1991 to
2012 and were processed for analyses of age and reproduction
(n= 7,685). Chevron traps (Collins 1990) were deployed
during daylight hours in depths ranging from 10 to 110 m at
sites that were randomly chosen from a universe of known
locations of natural reef habitat (live bottom and rocky
ledges). From 1991 to 2012, approximately 2,500 live-
bottom sites were included, from which 300–900 randomly
chosen sites were sampled annually. Traps were baited using
whole and cut clupeids (mainly menhaden Brevoortia spp.)
and remained in the water for approximately 90 min. Depth,
latitude, longitude, sampling duration, and time of collection
were recorded for each trap set. Once removed from the traps,
Gray Triggerfish specimens were weighed to the nearest gram
and measured for SL, FL, and TL to the nearest millimeter.
The overall period in which we sampled Gray Triggerfish
for this study was 1991–2012. Additionally, based on abun-
dance trends combined with fisheries landings (Figure 1), we
selected two shorter time periods for comparative purposes in
examining life history trends. The additional time periods
were (1) 1994–1997, during which Gray Triggerfish landings
peaked and the fishery-independent abundance index indicated
a peak in the population; and (2) 2009–2012, when fisheries
landings peaked again, but the fishery-independent abundance
index indicated a decline in population numbers.
To determine whether the population size structure of Gray
Triggerfish changed between the two periods, we used two
separate Kolmogorov–Smirnov (K–S) tests (one for males and
one for females) to evaluate the null hypothesis that the size
structure of fish collected during 1994–1997 did not differ
from that of fish collected in 2009–2012. We also used K–S
tests to examine for significant differences in the size fre-
quency distribution between males and females within each
time period (1991–2012; and the two shorter periods,
1994–1997 and 2009–2012). To assess whether mean size
significantly differed between males and females and between
the two time periods, we utilized a two-factor ANOVA with
size (FL) as the dependent variable and with time period and
sex as the independent factors.
For our evaluation of whether fish size was correlated with
depth of capture, a subset of fish size data was selected by
using four conditions: (1) to control for possible long-term
shifts in the population’ssize structure, we only used data
from 2004 to 2012; (2) to control for latitudinal-related
water temperature trends, we established two main areas of
interest (a North Carolina area from 33°N to 35°N and 76°W
to 78°W; and a South Carolina area from 32°N to 33°N and
79°W to 80°W); (3) we selected data from two discrete depth
zones (<36 m and 40–65 m) so that size distributions could be
compared; and (4) considering that the main sampling efforts
conducted by SERFS occurred during May–September, only
samples from those months were used in the analyses. For
each area, we tested the following two null hypotheses: (1)
male or female sizes do not differ with depth of capture based
on linear regression analyses; and (2) male or female size
frequency distributions do not differ between the two depth
zones based on K–S tests.
Statistical analyses were conducted in SPSS (IBM 2012)
and RStudio (RStudio Team 2013), and the results were con-
sidered significant at P-values less than 0.05. If assumptions
for statistical tests were not met, then the data were log
transformed.
Age and growth.—The first dorsal spine is currently the
accepted structure for estimating age in Gray Triggerfish
(Moore 2001; Fioramonti 2012). The spine was removed
from the fish, cleaned of excess tissue, and stored dry until
further processing. Two sections immediately distal to the
condyle groove were cut from each spine (0.5–0.7-mm
thickness) by using a low-speed saw with a diamond-edged
blade. The sections were then mounted on glass slides with a
clear mounting medium and were viewed under a dissecting
microscope at 10–20× magnification using transmitted light.
Increment count was determined by identifying and
enumerating the pattern of faster-growing (opaque) and
slower-growing (translucent) zones that were assumed to
represent 1 year of peak growth and slow growth seasons.
Fish age was estimated for each spine section by count-
ing the number of translucent zones. Multiple readers esti-
mated ages for fish collected during 1994–1997 and
2009–2012. At least two independent readers evaluated
increments on a spine section without knowledge of the
fish’s length or date of capture. For this study, increment
counts were considered age estimates. However, age valida-
tion of the first dorsal spine has not been performed for this
species. Spine sections for which reader disagreement
occurred were re-evaluated simultaneously by both readers,
and a consensus count was recorded as the final age estimate
in whole years. Other studies have reported low between-
reader precision for age estimates based on Gray Triggerfish
spines (Fioramonti 2012;Burtonetal.2015). Therefore, we
assessed reader precision by using the same methods so that
precision estimates could be compared among studies.
Between-reader precision was estimated by calculating per-
cent agreement between readers for perfect agreement and
for agreement within ±1 year. We also computed the average
percent error (APE) for age estimates between readers
(Beamish and Fournier 1981).
Spine section margins were evaluated as either containing
the final translucent zone along the edge or containing the final
opaque zone. Using age-3, age-4, and age-5 fish collected
from 2009 to 2012, we estimated the timing of increment
formation by examining the monthly proportion of spines
with translucent zones at the spine edge. This allowed for a
reasonable approximation of increment periodicity, if not a full
validation. Fractional age estimates were calculated based on
the date of capture and the presumed birth date of July 1,
REPRODUCTIVE BIOLOGY OF GRAY TRIGGERFISH 525
which took into account the period of translucent band deposi-
tion and the peak of the spawning season.
For the 2009–2012 period, we compared the age frequency
distributions between males and females by using a K–S test
to determine whether age structure differed between the sexes.
A Student’st-test was used to examine for significant differ-
ences in mean age between males and females within the
current (2009–2012) period.
Von Bertalanffy growth curves (von Bertalanffy 1938)
fitted to observed lengths at age for males and females
sampled during 2009–2012 were used to determine the growth
rates exhibited by the current Gray Triggerfish population. To
provide a more representative estimate of von Bertalanffy
growth parameters within the population off the southeastern
U.S. Atlantic coast, we included 12 newly settled juvenile
Gray Triggerfish that were collected from Sargassum spp. off
the South Carolina coast during 2011–2014 and processed for
sex and age determination. Growth curve parameters were
compared between sexes by using analysis of residual sums
of squares (RSS; Chen et al. 1992).
Reproduction.—Gonads were removed from the fish; the
posterior portion of each gonad was fixed in an 11% solution
of seawater-buffered formalin for up to 2 weeks and then was
transferred to a 50% solution of isopropanol. Gonad samples
were processed by using standard histological procedures
(Harris and McGovern 1997; Wyanski et al. 2000; Harris
et al. 2007). The tissue samples were vacuum-infiltrated and
blocked in paraffin wax. Three transverse sections (~7 µm
thick) were cut using a rotary microtome, mounted on glass
slides, stained with double-strength Gill hematoxylin, and
counterstained with eosin-y.
Stained sections were viewed under a compound micro-
scope to determine the individual’s sex and its reproductive
phase, which was assessed according to a modified version of
the histological criteria utilized in previous reef fish studies
(Table 1; Supplementary Figures S.1–S.3 available in the
online version of this article) and with slight modification in
terminology for consistency (Brown-Peterson et al. 2011).
Two readers independently assigned sex and reproductive
phase without knowledge of the date of capture, specimen
length, or specimen age. If differences in assignments of
reproductive phase occurred, the readers examined the slide
simultaneously to attempt a consensus assignment. If no con-
sensus was reached, that specimen was eliminated from the
analyses. During this process, we noted that the gonads of
male Gray Triggerfish were unique in their structure and
function compared to other species in the snapper–grouper
management complex (Figures S.1, S.2), so we documented
the male gonad structure and its relevance to determining
reproductive phase as part of this study (Figure S.2).
To ensure that specimens in the immature and resting
phases were assigned correctly, the size frequency of fish
that were definitely mature (i.e., developing, spawning cap-
able, or regressing) was compared to the size frequencies of
immature fish and regenerating fish. Individuals of uncertain
sex or reproductive phase were excluded from this analysis. If
little or no overlap in FL was observed for immature and
regenerating specimens, then we assumed that the phases
were assessed correctly.
Spawning activity in females was denoted by the presence
of oocyte maturation and postovulatory follicle complexes
(POCs; Figure S.3). The POC stages were assigned based on
the level of degeneration present in the POC in accordance
with Moore (2001). The spawning season was defined as
extending from the first date when late oocyte maturation or
POCs were observed in a specimen to the latest date when
POCs were present in a specimen. Stage-1 POCs showed little
degeneration, large size, distinct thecal and granulosa layers,
and a highly convoluted lumen. Stage-2 POCs were smaller
than stage-1 POCs, showed degeneration of the granulosa and
thecal layers, and presented a less-distinct lumen relative to
stage-1 POCs. Stage-3 POCs exhibited a characteristic trian-
gular shape of the granulosa layer, a loss of most granulosa
cells, further degeneration of the thecal layer, and a reduced or
absent lumen. To determine spawning frequency, the methods
of Fitzhugh et al. (1993) were used to calculate overall counts
of active, nonspawning females (i.e., those with vitellogenic
oocytes) and spawning females (i.e., those with stage-2 and
stage-3 POCs) within each month and during the peak spawn-
ing season. The proportion of spawning females was calcu-
lated for each month of the spawning season as the number of
spawning females divided by the total number of active, non-
spawning females plus spawning females. The proportion of
spawning females in the peak spawning season was then
multiplied by the number of days in the peak spawning season.
We assumed that all mature females participated in reproduc-
tion throughout the spawning season. A chi-square test was
used to determine whether sex ratios significantly differed
within and between the 1994–1997 and 2009–2012 sampling
periods. Generalized linear models fitted to logistic curves
were used to estimate the length at 50% maturity separately
for males and females.
RESULTS
Fish Collection
During 1991–2012, Gray Triggerfish sampling ranged from
34.60°N, 76.19°W to 27.23°N, 80.05°W. Overall, 7,685 Gray
Triggerfish were collected (44% were male, 54% were female,
2% were of unknown sex; Table 2) from depths of 14–92 m.
The mean size of males (337 mm FL) was significantly larger
than that of females (304 mm FL; t=–13.46, P< 0.0001), and
the size frequency analysis also indicated a significant differ-
ence between the sexes (K–S test: Z= 6.3, P< 0.001; Figure 2).
Mean size of Gray Triggerfish increased significantly
from 1994–1997 to 2009–2012 (two-factor ANOVA, sex:
F
1, 1,605
= 95.8, P< 0.001; sampling period: F
1, 1,605
=
109.8, P< 0.001; Tab l e 2), and there was no significant
526 KELLY-STORMER ET AL.
TABLE 1. Histological criteria (modified from Harris and McGovern 1997 and Moore 2001) that were used to evaluate reproductive phase in Gray Triggerfish.
Terminology in the table has been modified according to Brown-Peterson et al. (2011). Photographic examples of each phase are provided in Supplementary
Figures S.2 and S.3.
Reproductive phase Males Females
Immature (never
spawned)
Small transverse section compared with
regenerating males; little or no spermatocyte
development.
Primary growth oocytes only; no evidence of
atresia. In comparison with regenerating females,
largest primary growth oocytes are smaller than
60 µm; area of the transverse section of ovary is
smaller; lamellae lack muscle and connective
tissue bundles and are not as elongate; germinal
epithelium along the margin of lamellae is
thicker; and ovarian wall is thinner. Oogonia are
abundant along the margin of lamellae.
Developing Limited spermatogenesis in the testes; elongation of
lobules and some development of spermatozoa in
the testes, but no accumulation in lobules,
efferent ducts, and spermatic ducts.
Early: previtellogenic, with only primary growth
and cortical alveolar oocytes. Cortical alveolar
oocytes are 140–200 µm in diameter.
Middle to late: Vitellogenic, most advanced
oocytes in the yolk granule or yolk globule stage.
Oocytes are 170–400 µm in diameter.
Spawning capable Early: Spermatozoa are evident in ducts;
spermatogenesis amount in the testes ranges from
limited to extensive. Greater area of structural
tissue in ducts compared to sinuses.
Middle (storage): Spermatozoa storage within
expanding ducts; over 50% of the sinus area is
densely packed with spermatozoa; amount of
spermatogenesis in the testes ranges from limited
to extensive.
Late (recent spawn): large expanded ducts, not as
densely packed with spermatozoa. Area of
sinuses greater than structural tissue. Empty
lobules are usually present toward the center of
the testes.
Oocyte maturation in the most advanced oocytes:
zona radiata becomes thin, and oocytes are
undergoing coalescence of yolk globules,
germinal vesicle migration, germinal vesicle
breakdown, hydration, or ovulation.
Postovulatory follicle complexes are sometimes
present. Atresia of vitellogenic and/or hydrated
oocytes may be present.
Regressing Limited spermatogenesis in the testes; some
residual spermatozoa in shrunken ducts/lobules
and sinuses. Overall number of ducts containing
spermatozoa is low. Increase in connective tissue
in the testes, proliferating from the center.
More than 50% of vitellogenic oocytes with alpha-
or beta-stage atresia.
Regenerating Little or no spermatocyte development; empty
ducts/lobules and sinuses. Large transverse
section in comparison with immature males.
Primary growth oocytes only; traces of atresia. In
comparison with immature females, largest
primary growth oocytes are greater than 60 µm;
area of the transverse section of ovary is larger;
lamellae have muscle and connective tissue
bundles; lamellae are more elongate and
convoluted; epithelium along the margin of
lamellae is thinner; and the ovarian wall is
thicker.
Mature specimen,
phase unknown
Mature; but an inadequate quantity of tissue or
postmortem histolysis prevents further
assessment of reproductive phase.
Mature; but an inadequate quantity of tissue or
postmortem histolysis prevents further
assessment of reproductive phase.
REPRODUCTIVE BIOLOGY OF GRAY TRIGGERFISH 527
interaction effect (P= 0.403). Size frequencies of males and
females were significantly different between the two periods
(K–S test, males: Z= 3.8, P< 0.001; females: Z=3.8,P<
0.001), with a shift to a greater proportion of larger fish for
both sexes in 2009–2012 (Figure 3).
Male size was significantly larger with increasing depth
for fish caught in the North Carolina area (R
2
= 0.49, t=
10.3, P< 0.001; Figure 4) and in the South Carolina area (R
2
= 0.24; t= 9.1, P< 0.01). Female size was also significantly
larger with depth (North Carolina area: R
2
= 0.52, t= 10.2, P
< 0.001; South Carolina area: R
2
= 0.34, t= 12.3, P< 0.001;
Figure 4). Additionally, the size frequency of females in both
areas indicated that the proportion of larger females was
significantly higher in the deeper (40–65-m) zone (K–S test,
North Carolina area: Z= 3.8, P< 0.01; South Carolina area:
Z= 5.6, P< 0.01; Figure 5). Males exhibited a similar trend
(North Carolina area: Z= 4.1, P< 0.01; South Carolina area:
Z= 4.0, P< 0.01; Figure 6).
Age and Growth
During 1994–1997, we collected 2,646 Gray
Triggerfish, and age estimates were obtained from 2,484
fish (94% of samples). Among the 1,372 Gray Triggerfish
that were caught during 2009–2012, ages were determined
for 1,261 fish (92% of samples). The remaining specimens
were unused for age estimation because their spines were
missing, broken, or unreadable. Exact agreement between
readers occurred for 43% of the spine sections, and age
estimates agreed within ±1 year for an additional 32% of
the sections. The APE in our study was 12%. By compar-
ison, Burton et al. (2015) reported exact between-reader
agreement on 34% of age estimates, agreement within ±1
year for 33% of estimates, and an overall APE of 11%.
Fioramonti (2012) also reported an APE of 11%.
For fish caught during 2009–2012, the percentage of spines
with translucent edges was approximately 50% from April to
August and then dropped to less than 30% during September and
October (Figure 7). Age frequency distributions were not sig-
nificantly different between males and females (K–Stest:Z= 0.8,
P= 0.575; Figure 8). However, mean ages differed significantly
between sexes (t=–1.97, P=0.02;Ta b le 2).
A significant difference between the von Bertalanffy
growth models for males and females was detected (analysis
of RSS: F
3, 1,258
= 511.62, P< 0.0001; Table 3). Sex-specific
growth curves were fitted, yielding the following von
Bertalanffy equations (Figure 9; parameters summarized in
Table 3): FL
t
= 419[1 –e
–0.54(t+ 0.61)
] for males and FL
t
=
352[1 –e
–0.94(t+ 0.22)
] for females.
TABLE 2. Overview of geographic, depth (m), size (FL, mm), and age (years) ranges for male and female Gray Triggerfish over time; and the total number of
fish sampled and percentages of males, females, and unknown-sex individuals in samples over time.
Variable 1991–2012 1994–1997 2009–2012
Geographic range 27.23°N, 80.05°W to
34.60°N, 76.19°W
28.95°N, 80.18°W to
34.59°N, 76.95°W
27.23°N, 80.05°W to
34.59°N, 76.93°W
Depth range (m) 14–92 15–92 15–87
Total number of fish sampled 7,685 2,647 1,372
Percent male 43 45 41
Percent female 54 53 56
Percent unknown sex 3 2 3
Overall FL range (mean FL) 82–578 (321) 82–578 (314) 155–523 (346)
Male FL range (mean) 136–578 (337) 137–578 (328) 183–523 (367)
Female FL range (mean) 82–560 (304) 82–474 (296) 155–502 (326)
Overall age range (mean age) 0–13 (5) 0–11 (4) 0–10 (4)
Male age range (mean) 0–13 (5) 0–11 (4) 0–10 (4)
Female age range (mean) 0–13 (5) 0–10 (4) 0–10 (3)
FIGURE 2. Size frequency distributions (FL, mm) for male and female Gray
Triggerfish sampled off the southeastern U.S. Atlantic coast from 1991 to
2012 (n= number of specimens).
528 KELLY-STORMER ET AL.
Reproduction
Gonads were collected from a total of 7,644 Gray
Triggerfish during 1991–2012; sex and reproductive phase
were assigned to 6,894 fish (90% of samples). To determine
the spawning season, we examined females that were collected
throughout all years because the sample sizes of females with
spawning indicators in the two sampling periods of interest
were low (95 females in 1994–1997 and 6 females in
2009–2012 compared with 176 females in 1991–2012).
In general, for many fish species, the shape of the gonads in
males and females is similar in that they (1) consist of two
lobes that are posteriorly attached and (2) release the gametes
via an oviduct (female) or a spermatic duct (male). The gonads
of female Gray Triggerfish are similar in shape to those of
other fish species, containing two lobes that are posteriorly
attached and release the eggs via the oviduct (Figure S.1).
However, we determined that the gonads of male Gray
Triggerfish consist of testes, a spermatic duct, and accessory
glands (Figures S.1, S.2) and that the accessory glands are
used to store spermatozoa before spawning. Close
examination of the testes and accessory glands is needed in
order to assign the most accurate reproductive phase to males
(Table 1; Figures S.1, S.2).
Based on the entire data set (1991–2012), the beginning
of the spawning season was April 30—the earliest date (in
any year) on which oocyte maturation or POCs were
observed in females. The end of the spawning season
was September 29, which was the latest date (in any
year) on which late-developing oocytes and POCs were
present in females. Note that during 1991–2012, only one
spawning female was captured in April (out of a total of
71 adult fish sampled), only three were captured in
September (out of 1,295 adults), and none was captured
in October (out of 40 adults). In addition, no spawning
females were captured after August 28 for that month (out
of 146 adults). Therefore, a more conservative spawning
period estimate of May 5–August 28 was used, resulting in
a spawning season of 115 d (Figure 10).
Among females with vitellogenic oocytes, the propor-
tion of females with a spawning indicator (i.e., stage-2 or
stage-3 POCs) ranged from 0.03 in May to 0.20 in April
(Tab l e 4). The overall proportion of spawning females was
0.095 during the peak spawning season (May–August), so
spawning periodicity was approximately every 10 d (or
1/0.095, the reciprocal of the overall proportion of spawn-
ing females expressed in days). With a spawning season of
approximately 115 d in the U.S. South Atlantic (May 5–
August 28), a female can potentially spawn approximately
12 times throughout a given spawning season.
For the remaining analyses, both time periods were used to
determine whether any shifts occurred in the sex ratios by FL
or the length at 50% maturity. Overall, 4,000 gonad samples
were collected during the two sampling periods (2,633 sam-
ples in 1994–1997; 1,367 samples in 2009–2012). Sex and
reproductive phase were assigned to 3,700 fish (93% of the
samples). The overall male : female sex ratio for Gray
Triggerfish collected during 1994–1997 was 1:1.19 and dif-
fered significantly from a 1:1 ratio (Table 5). Females were
more abundant than males in size-classes ≤350 mm FL, and
the sex ratio differed significantly from 1:1 for 151–350-mm
FL fish. Males larger than 401 mm FL were more abundant
than females, and the sex ratio significantly differed from 1:1
for 401–500-mm FL fish. Sample sizes in size-classes greater
than 500 mm FL were low (i.e., <10 fish); therefore, chi-
square analyses were not performed.
The overall male : female sex ratio for Gray Triggerfish
collected during 2009–2012 was 1:1.34 and differed signifi-
cantly from a 1:1 ratio (Table 5). Females 350 mm FL or
smaller were more abundant than males of those sizes, and the
sex ratio significantly differed from 1:1 for 201–350-mm FL
fish. However, males were more abundant in the smallest size-
class (151–200 mm FL), and the sex ratio did not significantly
differ from 1:1. Males that were larger than 400 mm FL were
more abundant than females, and the sex ratio differed
FIGURE 3. Size frequency distributions (FL, mm) of female (upper panel)
and male (lower panel) Gray Triggerfish sampled off the southeastern U.S.
Atlantic coast during two periods (1994–1997 and 2009–2012; n= number of
specimens used in the analysis).
REPRODUCTIVE BIOLOGY OF GRAY TRIGGERFISH 529
significantly from 1:1 for 401–500-mm FL males. We had low
sample sizes (i.e., <10 fish) for males and females that were
501–550 mm FL, so a chi-square analysis was not performed
for this size-class.
Females were more abundant than males at most ages
except ages 7 and 10 (Table 6). The sex ratio significantly
differed from 1:1 for ages 2–4 but did not differ for age 1
or ages 5–8. Chi-square analyses for ages 0, 9, and 10
were not performed due to low sample sizes.
For the periods 1994–1997 and 2009–2012, immature
Gray Triggerfish made up 3% of the specimens for which
reproductive phase was determined (n= 114; 91 fish in
1994–1997 and 23 fish in 2009–2012). Correct assignment
of reproductive tissue to the “immature”and “regenerating”
gonad categories was indicated by (1) the complete or near-
complete overlap in the left tail of the size frequency dis-
tributions for definitely mature (i.e., developing, spawning,
and regressing phases) and regenerating-phase specimens
and (2) the minimal overlap in the size frequency distribu-
tions for immature and regenerating-phase specimens
(Figure 11).
For samples collected in 1994–1997, the smallest mature
male was 165 mm FL, and the largest immature male was
265 mm FL. The youngest mature male was age 0, and the
oldest immature male was 4 years. Male size at 50%
maturity was 184 mm FL (95% confidence interval [CI] =
175–191 mm), and all males larger than 271–280 mm FL
were mature. The smallest mature female was 152 mm FL,
and the largest immature female was 297 mm FL. The
oldest immature female was 3 years. Female size at 50%
maturity was 177 mm FL (95% CI = 167–184 mm), and all
females larger than 251–260 mm FL were mature, with the
exception of the largest immature female recorded at
297 mm FL, which was 54 mm larger than the next-largest
immature female at 243 mm FL. Among age-1 fish, 79% of
males and 90% of females were sexually mature.
For 2009–2012 samples, the smallest mature male was
183 mm FL, and the youngest mature male was age 0; the
largest immature male was 268 mm FL, and the oldest imma-
ture male was 2 years. Male size at 50% maturity was 174 mm
FL (95% CI = 95–205 mm); all males larger than
281–290 mm FL and older than age 2 were mature. The
smallest mature female was 179 mm FL, and the youngest
mature female was age 0; the largest immature female was
290 mm FL, and the oldest immature female was age 4.
Female size at 50% maturity was 190 mm FL (95% CI =
166–210 mm), and all females were mature by 301–310 mm
FL. Among age-1 fish, 92% of males and 87% of females
were sexually mature.
DISCUSSION
Results from the present study provide key life history infor-
mation for an exploited population of Gray Triggerfish. This
study is the first to comprehensively describe age, growth, and
reproduction for a Balistes species. We documented that the Gray
Triggerfish is a sexually dimorphic species, with adult males
attaining a larger size at age and a larger maximum size than
females. The species is characterized by a medium size at matur-
ity and a relatively early age at maturity. We also found that some
shifts in population attributes have coincided with a period of
apparent increase in fishing pressure.
Population Size Structure, Age, and Growth
The mean length of males was significantly larger than that
of females. Similar findings have been reported for Gray
Triggerfish in the Gulf of Mexico (Hood and Johnson 1997;
Ingram 2001). Males and females also exhibited different
growth rates in our study, with males attaining a larger size
at age and a greater asymptotic length. Ingram (2001) docu-
mented a similar trend with fish collected from Alabama. To
some degree, this may be related to the mating and nesting
behaviors documented for this species. Simmons and
Szedlmayer (2012) studied the reproductive behavior of Gray
Triggerfish utilizing artificial reef habitats in the northern Gulf
FIGURE 4. Sizes (FL, mm) of male and female Gray Triggerfish in relation
to depth (m) for fish sampled during 2004–2012 from the North Carolina (NC)
area (upper panel) and the South Carolina (SC) area (lower panel; n= number
of specimens used in analysis). Linear regression analysis of the slopes was
used (NC area: R
2
= 0.5216 for females, 0.4919 for males; SC area: R
2
=
0.3389 for females, 0.2437 for males).
530 KELLY-STORMER ET AL.
of Mexico; they reported that a large dominant male patrols a
nesting territory, builds and maintains multiple nests within
the territory, and continues to guard the nesting area after
fertilization. The larger size of males is advantageous given
that they need to defend nests in order to optimize the survival
of the eggs. The relatively small females also exhibit parental
investment behaviors. Prior to spawning, the females inspect
potential nests. Once a female deposits eggs into a nest, she
FIGURE 5. Size-class frequency distributions (FL, mm) of female Gray
Triggerfish sampled from two depth ranges (open bars = <36 m; black bars
=40–65 m) in the North Carolina (NC) area (upper panel) and the South
Carolina (SC) area (lower panel) during 2004–2012 (n= number of specimens
used in analysis).
FIGURE 6. Size-class frequency distributions (FL, mm) of male Gray
Triggerfish sampled from two depth ranges (open bars = <36 m; black bars
=40–65 m) in the North Carolina (NC) area (upper panel) and the South
Carolina (SC) area (lower panel) during 2004–2012 (n= number of specimens
used in analysis).
FIGURE 7 Percent frequency of annulus (i.e., the translucent zone) presence
on the edge of the first dorsal spine in Gray Triggerfish collected off the
southeastern U.S. Atlantic coast during each month.
FIGURE 8. Age frequency distributions of female and male Gray Triggerfish
sampled off the southeastern U.S. Atlantic coast during 2009–2012 (n=
number of specimens).
REPRODUCTIVE BIOLOGY OF GRAY TRIGGERFISH 531
guards the eggs in addition to tending to them by fanning and
blowing on the eggs to provide oxygenation. Females appear
to stay within 1 m of their eggs until they hatch, which can
take up to 48 h (Simmons and Szedlmayer 2012).
The mean size of males and females increased during the
same period that fishing pressure appeared to increase across
the region; many studies have reported that fish stocks experi-
encing overfishing usually exhibit the opposite trend. The
Speckled Hind Epinephelus drummondhayi in southeastern
U.S. Atlantic waters is considered an overfished species, and
Ziskin et al. (2011) documented a decrease in the average size
of Speckled Hind caught during 2004–2007 relative to histor-
ical data collected in 1979–1981. Similarly, a comparison of
recent data to historical data revealed a decrease in the size of
Scamp Mycteroperca phenax in U.S. South Atlantic waters
(Harris et al. 2002). A decline in mean sizes after 15 years of
intense fishing pressure was also reported for several porgy
and snapper species in waters off North Carolina (Parker and
Mays 1998).
The increase in mean sizes and the greater proportion of
larger individuals within the Gray Triggerfish population may
partially be explained by a corresponding decline in the abun-
dances of co-occurring reef fish species that potentially com-
pete with the Gray Triggerfish for resources (Ballenger et al.
2013). Adult Gray Triggerfish are generalists in their feeding
habits (Blitch 2000; Goldman et al. 2016). They consume a
wide range of invertebrate prey, including sponges, crusta-
ceans (e.g., barnacles and crabs), echinoderms (e.g., sea urch-
ins, sand dollars, and sea stars), and mollusks (e.g., bivalves,
gastropods, and cephalopods). They have also been observed
to feed on fishes (V.S., unpublished data). Many of the declin-
ing reef fish species exhibit more specialized feeding strate-
gies and have narrower diets (Tremain and Adams 2012).
Thus, declines in co-occurring species, such as the Scamp,
Red Porgy Pagrus pagrus, and Speckled Hind, may have
contributed to an increase in the availability of food items
for Gray Triggerfish, which in turn could have led to increased
growth rates and ultimately a shift in the proportion of larger
individuals within the Gray Triggerfish population. Further
research is needed to examine this anomaly.
The results from our examination of spine margin zones
indicated that annulus formation occurred in the late spring to
early summer, which is consistent with the findings of other
studies (Moore 2001; Burton et al. 2015). The formation of the
translucent zone (as seen under transmitted light) during sum-
mer months would be expected given that translucent zones
represent periods of slower somatic growth. Gray Triggerfish
generally spawn during summer (May–August) and therefore
are investing more energy into reproduction to optimize the
TABLE 3. Parameters (L
∞
= asymptotic length [FL, mm]; k= Brody growth
coefficient; t
0
= theoretical age [years] at zero length) derived from von
Bertalanffy growth equations that were fitted to observed size-at-age data
for Gray Triggerfish sampled off the southeastern U.S. Atlantic coast.
Growth curves were calculated for (1) each sex; (2) the combined data set,
including juveniles caught from Sargassum habitat; and (3) the combined data
set, excluding juveniles from Sargassum.
Sex nL
∞
(SE) k(SE) t
0
Male 549 419 (1.3) 0.54 (0.010) –0.61
Female 709 352 (0.7) 0.95 (0.001) –0.22
Combined 1,258 382 (0.7) 0.67 (0.008) –0.47
Combined
(excluding juveniles)
1,247 419 (2.3) 0.30 (0.009) –2.39
FIGURE 10. Reproductive seasonality of female Gray Triggerfish collected
off the southeastern U.S. Atlantic coast during 1991–2012. See Methods for a
description of the spawning indicators.
FIGURE 9. Fork length at age for male and female Gray Triggerfish collected
off the southeastern U.S. Atlantic coast during 2009–2012, with von
Bertalanffy growth curves fitted to the sex-specific data sets (black line =
growth curve for males; gray line = growth curve for females). See Table 3 for
a summary of the von Bertalanffy parameters.
532 KELLY-STORMER ET AL.
survival of their offspring while investing less energy in
somatic growth. Moore (2001) concluded that increment for-
mation in Gray Triggerfish of the U.S. South Atlantic occurred
in June, and Burton et al. (2015) reported that increment
formation took place in June and July. Johnson and Saloman
(1984) reported that increment formation in Gray Triggerfish
occurred from April to August in the Gulf of Mexico. Other
reef fishes also exhibit spring or summer increment formation.
For example, Snowy Grouper Hyporthodus niveatus in North
Carolina and South Carolina offshore waters form annuli dur-
ing April and May (Wyanski et al. 2000). For Yellowtail
Snapper Ocyurus chrysurus in Florida, annulus formation
occurs during March and April (Garcia et al. 2003).
Speckled Hind in Atlantic waters form annuli from June to
August (Ziskin et al. 2011).
The first dorsal spine has been the main aging structure
used for triggerfish species for over 30 years (Ofori-Danson
1989; Ingram 2001; Moore 2001; Bernardes 2002; Aggrey-
Fynn 2009;Burtonetal.2015). This external bony structure
is used in defense and often breaks and twists during a
fish’s lifetime (Kelly 2014). Studies of other species have
demonstrated that external structures, including spines, sig-
nificantly underestimate the true age of fish (Buckmeier
et al. 2012;Guetal.2013;Lozanoetal.2014).
Additionally, in comparison with sagittal otolith-based age
estimates, dorsal spines were found to underestimate the age
of Gray Triggerfish (Shervette and Dean 2015). Ages based
on dorsal spines have yet to be directly validated (i.e.,
confirming the periodicity of growth zone formation), and
other studies have reported difficulties in using this struc-
ture for estimating Gray Triggerfish ages (Fioramonti 2012;
Burton et al. 2015). For example, Burton et al. (2015)
reported relatively low agreement in ages produced by two
readers: perfect agreement occurred for 34% of their sam-
ples (in our study, exact agreement = 43%), and overall
agreement increased to 67% when including estimates that
agreed within ±1 year (in our study, overall agreement
including estimates within ±1 year = 75%). Fioramonti
(2012) encountered similar issues with reader agreement,
reporting an APE of 11% (in our study, overall APE
= 12%).
Two studies have attempted to validate ages for dorsal
spines by using oxytetracycline to chemically mark labora-
tory-held Gray Triggerfish collected from the Gulf of Mexico
TABLE 4. Spawning frequency of female Gray Triggerfish based on histolo-
gical data from samples collected in 1991–2012. Spawners had middle or late
postovulatory follicle complexes (POCs). Active nonspawners were reproduc-
tively active (i.e., vitellogenic oocytes were present) but did not have stage-2
or stage-3 POCs.
Month
Number of
active
nonspawners
Number
of
spawners
Proportion
spawners
Apr 4 1 0.20
May 129 4 0.03
Jun 412 42 0.09
Jul 541 71 0.12
Aug 155 13 0.08
Sep 15 3 0.17
May–Aug 1,237 130 0.01
TABLE 5. Sex ratio within each size-class (FL, mm) for Gray Triggerfish
collected off the southeastern U.S. Atlantic coast during 1994–1997 and
2009–2012.
FL (mm)
Total number
of fish Male : female ratio P
1994–1997
151–200 105 1:1.76 <0.05
201–250 327 1:1.42 <0.05
251–300 557 1:1.86 <0.001
301–350 737 1:1.21 <0.05
351–400 500 1:1.08 0.37
401–450 204 1:0.44 <0.001
451–500 48 1:0.07 <0.001
501–550 6
551–600 1
2009–2012
151–200 11 1:0.38 0.13
201–250 39 1:2.00 0.04
251–300 236 1:2.69 <0.001
301–350 417 1:2.16 <0.001
351–400 369 1:1.17 0.13
401–450 180 1:0.36 <0.001
451–500 39 1:0.18 <0.001
501–550 4 1:0.33
TABLE 6. Sex ratio by age for Gray Triggerfish collected off the southeastern
U.S. Atlantic coast during 2009–2012.
Age (years)
Total number
of fish Male : female ratio P
0 2 1:1.00
1 82 1:1.41 0.12
2 257 1:1.73 <0.001
3 327 1:1.32 <0.05
4 248 1:1.41 <0.05
5 157 1:1.09 0.58
6 67 1:1.39 0.18
7 30 1:0.88 0.72
8 18 1:2.60 0.06
9 7 1:2.50
10 2 1:1.00
REPRODUCTIVE BIOLOGY OF GRAY TRIGGERFISH 533
(Hood and Johnson 1997; Fioramonti 2012). Hood and
Johnson (1997) marked 12 Gray Triggerfish and held them
for 1 year before sacrificing the fish and processing them for
age determination. In all 12 fish, the chemical mark was still
on the edge of the spine, indicating that no additional growth
had occurred on the spine during the year in captivity. In
contrast, Fioramonti (2012) marked four adult Gray
Triggerfish and held them for 8 months, after which they
were sacrificed and processed for age determination.
Fioramonti (2012) reported that one translucent zone formed
on the spines beyond the chemical mark. Due to the conflict-
ing results of these two studies, spines have yet to be truly
validated as an accurate aging structure for this species.
The first dorsal spine was used in our study because it is
currently the accepted aging structure for Gray Triggerfish.
However, whether our age data represent the true age is still
unknown, so caution must be used when interpreting these
data and making comparisons with other studies that have
used dorsal spines to estimate age.
In the present study, male and female Gray Triggerfish
sampled in 2009–2012 ranged in age from 0 to 10 years.
Only one other study has reported age estimates for Gray
Triggerfish from approximately the same period. Fioramonti
(2012) reported similar maximum ages for males (8 years) and
females (9 years) collected in 2003–2010; however, they also
noted the capture of a 14-year-old fish of unknown sex. A few
studies that have combined age data across several decades or
that have presented data from earlier periods have observed
older Gray Triggerfish (Johnson and Saloman 1984;
Fioramonti 2012; Burton et al. 2015). Johnson and Saloman
(1984) reported maximum ages of 13 years for males and 12
years for females, but their study period was 1979–1982.
Burton et al. (2015) reported a maximum age of 15 years.
Differences in maximum age between our study and previous
studies may not be biologically significant—rather, they may
be related to the difficulty or inaccuracy of using dorsal spines
to estimate the age of Gray Triggerfish. In addition, other
studies have focused on fishery-dependent samples, have uti-
lized samples from earlier periods, or both.
Several studies have reported that Gray Triggerfish exhibit
moderately rapid growth and obtain a relatively large size by
the end of their first year (Table 7), a conclusion that is
generally supported by our results. In fact, when we included
juvenile Gray Triggerfish sampled from Sargassum habitat,
the growth rates we calculated for males and females were
among the highest reported (Table 7). However, care should be
taken when comparing von Bertalanffy parameter values
among studies. Some studies have utilized specialized rules
for adjusting increment counts to age estimates (Ingram 2001;
Fioramonti 2012; Burton et al. 2015), while other studies have
used back-calculated sizes in the growth model (Johnson and
Saloman 1984; Escorriola 1991; Bernardes 2002) or have
forced t
0
to equal zero (Ofori-Danson 1989). Several studies
have combined data from females and males into one growth
model (Ofori-Danson 1989; Escorriola 1991; Burton et al.
2015). Only one other study has used juveniles sampled
from Sargassum in estimating the growth of Gray Triggerfish
(Fioramonti 2012). Regional variation in growth rates within a
species is not unusual (Brander 1994), so some differences in
growth for Gray Triggerfish can be partly explained by regio-
nal differences (Ofori-Danson 1989; Bernardes 2002; Aggrey-
Fynn 2009; Kacem et al. 2015). Several studies have reported
that growth parameter estimates differ depending on the sam-
ple sources (Ingram 2001; Fioramonti 2012). Our study is the
only published work based exclusively on fishery-independent
samples (Table 7), thereby reducing size- or gear-related
biases that might occur with fishery-dependent sources but
also hindering the direct comparison of our growth rate esti-
mates with those of other studies.
The youngest age-class (age 0) was observed infrequently
for both sexes in the current study. The low sample sizes of
age-0 Gray Triggerfish could reflect the association of early
life stages with Sargassum and thus their lack of availability to
FIGURE 11. Size frequency distributions (FL, mm) of female (upper panel)
and male (lower panel) Gray Triggerfish with gonads categorized as imma-
ture, definitely mature (i.e., developing, spawning capable, or regressing), or
regenerating. Fish were sampled off the southeastern U.S. Atlantic coast
during 1991–2012.
534 KELLY-STORMER ET AL.
the bottom gears used. The exact age at which larval and
juvenile Gray Triggerfish cease to associate with Sargassum
and become established in reef habitats is unknown. Another
possible factor influencing the low sample sizes of smaller and
younger specimens in this study is the abundance of predators
in the chevron traps. Smaller fish may exhibit predator avoid-
ance if larger predators are inside the traps.
Reproduction
The Gray Triggerfish is a gonochoristic species, and
females are group-synchronous, indeterminate batch spawners
(Figure S.3). We found that Gray Triggerfish in U.S. South
Atlantic waters spawned from April to September, with peak
spawning in May–August, which overlaps with the spawning
season reported for this species in the Gulf of Mexico (Hood
and Johnson 1997; Ingram 2001; Lang and Fitzhugh 2015).
Gray Triggerfish from the U.S. South Atlantic appear to have a
longer spawning season (conservative estimate was 115 d
based on the occurrence of actively spawning females) than
those in the northern Gulf of Mexico, where spawning occurs
over an 86-d period starting in May (Lang and Fitzhugh 2015).
Gray Triggerfish in the Tunisian fishery spawn during July–
September (Kacem and Neifar 2014); those inhabiting coastal
waters of Ghana spawn in October–December (Ofori-Danson
1990); and those in Brazilian waters spawn during November–
January (Bernardes and Dias 2000). A combination of several
factors may explain the differences in the timing and length of
spawning season among studies. First, regional variation in
factors such as temperature, fish community composition, fish-
ing pressure, and habitat complexity could play a role in
regulating the reproductive season. Second, the method used
to estimate reproductive season varied among studies; our
study and two other studies based reproductive seasonality
on the histological examination of gonads (Bernardes and
Dias 2000; Lang and Fitzhugh 2015), whereas the other stu-
dies relied on changes in gonadal weight or on macroscopic
assessment of gonad phases. Third, differences in sample
sources (fishery dependent versus fishery independent) could
have impacted the findings. Lastly, sampling intensity, dura-
tion, and total sample numbers varied among the studies; we
report data from examining over 6,500 gonad samples,
whereas another study examined only 658 samples (Ofori-
Danson 1990).
We estimated that females could spawn up to 12 times
throughout the spawning season, which is similar to the
8–11 times estimated for Gray Triggerfish in the Gulf of
Mexico (Lang and Fitzhugh 2015). The Gray Triggerfish
exhibits a relatively unique reproductive strategy compared
with other large-bodied species targeted by fisheries in
southeastern U.S. Atlantic waters and in the Gulf of
Mexico (Johannes 1978; Lambert and Ware 1984; Murua
and Saborido-Rey 2003). The combined benefits of major
parental investments in establishing reproductive territories,
benthic nesting and guarding by both adults (Simmons and
Szedlmayer 2012), relatively high fecundity that increases
with size (Lang and Fitzhugh 2015), a spawning season that
extends for several months, and up to 12 spawns within a
season may result in a higher survival rate for larval Gray
Triggerfish in comparison with the larvae of broadcast-
spawning species. Research on larval survival rates would
be necessary to verify this.
The gonads of male Gray Triggerfish are unique in their
structure and function in that they consist of testes, a sper-
matic duct, and accessory glands. The accessory glands are
used to store spermatozoa before spawning (Figure S.1); the
purpose of storing spermatozoa in the accessory glands
could be related to differences in the reproductive behavior
of Gray Triggerfish compared with other reef fish species.
Male Gray Triggerfish have been observed to build several
nests in the substrate, and females will lay their eggs in
those nests (Simmons and Szedlmayer 2012). Considering
the number of nests constructed and the distance between
each nest, the storage of spermatozoa in the male accessory
glands would be necessary to ensure fertilization of the eggs
in each nest.
In summary, the present results provide insights into the
Gray Triggerfish population off the southeastern U.S.
Atlantic coast and constitute essential information for fish-
eries management. Considering that males and females have
significantly different von Bertalanffy growth parameters, the
sexes may need to be modeled separately in stock assess-
ments. Additionally, as fishers tend to remove larger fish
from the population, males may be removed more frequently
than females. Furthermore, as the populations of other reef
fish species decline, Gray Triggerfish may be experiencing an
increase in the availability of prey and other resources, lead-
ing to the observed increase in growth rates and the upward
shift in the proportion of larger individuals within the
population.
Due to tighter regulations on snapper and grouper fish-
eries, the Gray Triggerfish has become a more targeted and
economically valuable species in southeastern U.S. waters of
the Atlantic. We did not detect the typical life history shifts
that have been observed to correspond with increases in
fishing pressure (Harris and McGovern 1997; Wyanski
et al. 2000; Ziskin et al. 2011; Hunter et al. 2015), but this
does not mean that Gray Triggerfish are not experiencing
negative impacts. The species’relatively unique reproductive
strategy among the fishes in its management group may
make it necessary to expand our current understanding of
the life history indicators of overfishing, as such indicators
are mainly based on data from broadcast-spawning species
that produce pelagic larvae. Fisheries biologists and man-
agers should continue to evaluate potential impacts on the
Gray Triggerfish and establish management regulations that
consider the region-specific reproductive season, size and age
at maturity, and sex-specific growth documented in this
study.
REPRODUCTIVE BIOLOGY OF GRAY TRIGGERFISH 535
TABLE 7. Comparison of von Bertalanffy growth parameter estimates (L
∞
= asymptotic length [FL, mm]; k= Brody growth coefficient; t
0
= theoretical age [years] at zero length) for Gray Triggerfish,
as calculated in the present study and in previous studies (FL = Florida; NC = North Carolina; AL = Alabama; GOM = Gulf of Mexico; NA = not available or not examined).
Study Source L
∞
(mm FL) kt
0
Peak increment
formation;
spawning season Notes
Present study Fishery-independent
data, FL–NC (2009–
2012)
Females: 352 Females: 0.95 Females: –0.22 Apr–Jun; Apr–
Sep
Significant difference between
growth curves for females and
males
Males: Males: 0.54 Males: –0.61
419 All: 0.67 All: –0.47
All: 382 All except All except
All except
juveniles: 419
juveniles: 0.30 juveniles: –2.39
Burton et al.
2015
Commercial/
recreational fisheries,
FL–NC (1990–2012)
All: 466 All: 0.38 All: –1.58 Jun–Jul; NA Adjusted ages based on margin
Kacem and
Neifar 2014;
Kacem et al.
2015
Commercial samples
from Tunisia (2008–
2010)
Females: 417 Females: 0.24 Females: –0.07 Feb; Jul–Sep Spawning season based on
gonadosomatic indexMales: 420 Males: 0.23 Males: –0.12
All: 417 All: 0.24 All: –0.10
Fioramonti 2012 Fishery-independent
data and commercial/
recreational fisheries,
northern GOM
(2003–2010)
Females: 381 Females: 0.50 Females: –0.02 Dec–Jan; NA Adjusted ages based on difference
between birthdate and translucent
zone formation; included
juveniles collected from
Sargassum habitat
Males: 403 Males: 0.49 Males: –0.01
All: 521 All: 0.27 All: –0.12
Bernardes 2002 Commercial samples
from Brazil (1984–
1985)
Females: 505 Females: 0.27 Females: –0.03 Apr–May and
Sep–Nov (i.e.,
two periods);
NA
Used back-calculated size-at-age
valuesMales: 516 Males: 0.26 Males: –0.01
All: 510 All: 0.27 All: –0.12
Ingram 2001 Recreational fisheries,
AL; and GOM
groundfish survey
(1996–2000)
Females: 514 Females: 0.21 Females: –1.61 Dec–Jan; May–
Aug
Adjusted age based on a formation
date of January 1, a spawning date
of July 1, and the date of capture
Males: 598 Males: 0.20 Males: –1.37
All: 583 All: 0.18 All: –1.58
Hood and
Johnson 1997
Commercial/
recreational fisheries,
northern GOM
(1995–1996)
Females: 421 Females: 0.33 Females: –1.20 NA; Jun–Sep Could not determine when
increment formedMales: 645 Males: 0.16 Males: –1.80
All: 556 All: 0.15 All: –1.90
Escorriola 1991 Commercial/
recreational Fisheries,
FL–NC (1981–1989)
All: 571 All: 0.19 All: –0.15 Jul–Sep; NA Used back-calculated size-at-age
values
Ofori-Danson
1989
Fishery-independent
data, Ghana (1980)
All: 408 All: 0.43 All: 0.00 NA; NA Forced t
0
=0
Johnson and
Saloman 1984
Commercial samples
from Panama City,
FL (1979–1982)
Females: 438 Females: 0.38 Females: 0.15 Jun–Jul; NA Used back-calculated size-at-age
valuesMales: 492 Males: 0.38 Males: 0.23
All: 466 All: 0.38 All: 0.19
536 KELLY-STORMER ET AL.
ACKNOWLEDGMENTS
This paper is based on the Master’s thesis of A.K.-S. As
the thesis advisor, V.S. worked closely with A.K.-S. in the
organization and writing of the thesis and co-wrote this
paper. M.R. and T.S. were thesis committee members for
A.K.-S. and provided important direction, resources, and
feedback during the development of the project and this
paper. K.K. and D.W. taught and mentored A.K.-S. on fish
reproduction and histology and provided essential guidance
and assistance in the collection, analyses, and communication
of triggerfish reproduction data. C.M. provided critical assis-
tance with growth curve analyses and interpretations. Oleg
Pashuk, formerly a biologist with the MARMAP Program, is
thanked for his early contributions to the description of
gonad morphology in male Gray Triggerfish and for devel-
oping the histological criteria used by the program to assess
reproductive phase in this species. This study was funded by
the MARMAP Program at the SCDNR (NMFS Grant
NA11NMR4540174) and by a National Oceanic and
Atmospheric Administration Marine Fisheries Initiative
grant awarded to V.S. (NMFS Grant NA11NMF4330130).
This work would not have been possible without the exten-
sive assistance of the scientific and vessel crews who con-
ducted monitoring efforts as part of SERFS. This is
contribution number 758 from the Marine Resources
Research Institute of the SCDNR.
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538 KELLY-STORMER ET AL.
TransactionsoftheAmericanFisheriesSociety146:523–538,2017
©AmericanFisheriesSociety2017
DOI:10.1080/00028487.2017.1281165
Supplement: Additional Figures
Supplementary Figure S.1. (A) The gonad of a female Gray Triggerfish, with the oviduct as the gamete
release pathway; (B) the gonad of a male Gray Triggerfish, with the efferent ducts along the testes and the
accessory glands surrounding the spermatic duct; and (C) a diagram of male gonads relative to the internal body
cavity, showing the locations of the testes, spermatic duct, accessory gland, and urinary bladder.
Supplemental Figure S.2. Histological examples of reproductive phases for the gonads of male Gray
Triggerfish as described in Table 1: (A) immature: no spermatocysts with spermatocytes developing in the
testes, no spermatozoa in the spermatic duct; (B) immature: no development in the spermatic duct, but note the
accessory gland in the middle (lighter section with elongate ducts) of the spermatic duct; (C) developing: larger
testes compared with the immature phase, limited spermatogenesis in the testes, and elongation of the lobules
compared with the immature phase; (D) developing (close view): limited spermatogenesis in testes, with light-
purple staining representing spermatids or spermatozoa and dark-purple staining representing the
spermatocytes, and note the elongation of the lobules compared with the immature phase; (E) developing:
spermatic duct has elongated sinuses compared with the immature phase; (F) spawning capable (early): larger
testes than the developing phase, with spermatozoa evident in the testes; (G) spawning capable (early):
spermatozoa evident in ducts, and a greater area of structural tissue in ducts than in sinuses; (H) spawning
capable (middle): spermatozoa storage (>50% of sinus area) in expanding sinuses within the spermatic duct; (I)
spawning capable (late): empty lobules typically present toward the center of the testes (note that this transverse
section also included an unknown [UNK] part of the fish [possibly accessory glands] that was unusable for sex
and reproductive phase assignments); (J) spawning capable (late): large, expanded sinuses that are no longer
densely packed (>50% of sinus area) with spermatozoa, and the area of the sinuses is greater than that of the
structural tissue; (K) regressing: limited spermatogenesis in the testes, and slightly more compact sinuses in the
spermatic duct; and (L) regenerating: little or no spermatocyte development in the testes, sinuses are empty (but
note the muscle bundles inside the sinuses) and are even more compact than in the regressing phase, and the
transverse section is larger than that of the immature phase.
Supplemental Figure S.3. Histological examples of reproductive phases for the gonads of female Gray
Triggerfish as described in Table 1: (A) immature phase: ovarian wall (OW) and primary growth oocyte (PG);
(B) developing (early): cortical alveolar oocytes (CA); (C) developing (mid–late): vitellogenic oocytes (V); (D)
spawning capable: thinning zona radiata (ZR) and germinal vesicle migration (GVM); (E) early stage
postovulatory follicle complexes (POCs) are encircled; (F) mid-stage POCs are encircled; (G) late-stage POCs
are encircled; (H) regressing: atresia is present in over 50% of the ovary; and (I) regenerating: primary oocytes
are present again, but this phase is distinct due to the thicker OW and the muscle bundles (encircled).
