Kolmos et al.: Temporal changes in the life history of Hyporthodus niveatus off North and South Carolina 
317 
1.0 - 
a r 
/ / 
i mature 
o o 
O) CO 
_i_i_ 
/ / 
/ / 
/ / 
/ / 
/ # 
/ i 
/ / 
/ / 
o 
1 0.4 - 
Q. 
/ i 
/ i 
1 i 
/ / 
/ / 
— 1979-94(0=564) 
-- 2008-12(0=1289) 
^ 0.2 - 
1 i 
/ / 
/ / 
0.0 - 
J / 
n-1-1-1-1- 
20 40 60 80 100 
Total length (cm) 
1.0 - 
B 
« 0.8- 
1 0.6- 
/ / 
/ / 
/ / 
/ / 
/ / 
/ / 
/ / 
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c 
o 
■■g 0.4 - 
CL 
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/ / 
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— 1979-94(0=425) 
-- 2008-12(0=1212) 
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Cs 
i i i i i 
5 10 15 20 25 
Age (years) 
Figure 6 
Proportion of female snowy grouper ( Hyporthodus niveatus ) 
that were mature, by (A) total length and (B) age. Ages are 
counts of annual increments from otolith readings. Speci¬ 
mens were collected off North and South Carolina during 
1979-1994 and 2008-2012. For size at maturity from the 
generalized linear model (GLM), the predicted intercept 
and slope are -35.51 (standard error [SE] 7.45) and 0.066 
(SE 0.014), respectively, for 1979-1994 and -17.36 (SE 1.06) 
and 0.029 (SE 0.002), respectively, for 2008-2012. For age 
at maturity from the GLM, the predicted intercept and 
slope are -5.52 (SE1.07) and 1.130 (SE 0.195), respectively, 
for 1979-1994 and -3.15 (SE 0.28) and 0.566 (SE 0.044), 
respectively, for 2008-2012. n=number of fish examined. 
individuals may be detected if the population is given 
more time to recover. 
The size at age of snowy grouper rose sharply from 
the 1980s to the 1990s during a time of heavy fishing 
pressure, but size at age declined in the 2000s once 
regulations were implemented (Fig. 3). Wyanski et al. 
(2000) speculated that the increase in the size at age of 
snowy grouper in the 1990s was the result of moderate 
to high fishing pressure. Increases in size at age have 
also been observed for other species, including the gag 
(Mycteroperca microlepis ), the red grouper (Epinephelus 
morio), and the red porgy (Pagrus pagrus), that were 
experiencing moderate to high levels of exploitation 
off the coasts of the southeastern United States in the 
Atlantic Ocean and Gulf of Mexico (Johnson et al., 1993; 
Johnson and Collins, 1994; Harris and McGovern, 1997). 
The significant reversal of this trend from the 1990s to 
the 2000s is a positive sign for the population of snowy 
grouper off North and South Carolina. We detected only 
slight differences in the von Bertalanffy growth param¬ 
eters between periods, because of the low number of 
specimens at ages >15 years (21 specimens in the 1990s, 
9 specimens in the 2000s; Fig. 3). 
Reproduction 
Although Moore and Labisky (1984) and Wyanski et al. 
(2000) presented evidence of protogynous hermaphrodit¬ 
ism in snowy grouper, that evidence was not conclusive. In 
both studies, males were reported to have represented older 
fish, with ages of 6-27 years (Moore and Labisky, 1984) and 
ages of 8-29 years (Wyanski et al., 2000). Aspects of popu¬ 
lation structure (e.g., size distributions and sex composi¬ 
tion) generally are not reliable indicators of sexual pattern 
(Sadovy and Shapiro, 1987); however, a bimodal age- 
frequency distribution (i.e., males are older than females) is 
less problematic. The following features of gonad morphol¬ 
ogy strongly indicate protogyny, as described by Sadovy 
and Shapiro (1987): 1) membrane-lined central cavities in 
testes; 2), in transitional individuals, gonads that contain 
degenerating tissue of one sex and proliferating tissue of 
the other sex; and 3) atretic bodies within testes that are 
clearly derived from atretic vitellogenic oocytes, and sperm 
sinuses in the gonadal wall. 
Wyanski et al. (2000) concluded that the presence of pri¬ 
mary growth oocytes in 2 gonads with predominantly male 
tissue and membrane-lined central cavities was indicative 
of a nearly completed sex transition, but evidence of atretic 
(a-stage) vitellogenic oocytes and sperm sinuses was not 
present in the samples they analyzed. We met the criteria 
set by Sadovy and Shapiro (1987) in 2 specimens caught 
in August 2008 (Fig. 4). An additional criterion, laboratory 
observations of functional sex change in identified individ¬ 
uals, put forward by Sadovy de Mitcheson and Liu (2008) 
has yet to be observed in snowy grouper. We noted that 
18 specimens were undergoing sex transition, and most 
(16) of those fish were collected during the spawning sea¬ 
son. In contrast, low numbers of transitional specimens in 
samples collected during the spawning season led Moore 
and Labisky (1984) and Wyanski et al. (2000) to specu¬ 
late that transition likely occurs during the non-spawning 
period. More samples need to be collected outside the 
spawning season (April-September) to clearly determine 
the timing of sex transition. 
There was also a significant increase in L 50 mat from the 
combined value for the 1980s and 1990s (529 mm TL) to 
the value for the 2000s (596 mm TL), a potentially density- 
dependent reaction (Rothschild, 1986) that is an indication 
of some recovery (Fig. 6A). Changes between periods in 
A 50 mat were similar to results for L 50 mat . Values increased 
by almost a year from the combined A 50 mat for the 1980s 
and 1990s (5.0 years) to that for the 2000s (5.8 years), a 
significant difference (Fig. 6B). 
