Growth Variation, Settlement, and Spawning of Gray Snapper across a Latitudinal Gradient

Abstract

Newly recruited juvenile gray snapper Lutjanus griseus were collected each fall for two consecutive years (2000 and 2001) from sites in Florida and North Carolina. Spawning, settlement, and growth patterns were compared across sites based on otolith microstructure. Larval otolith growth trajectories were generally similar for larvae from different sites and years; however, the mean pelagic larval duration (PLD) was 1 d longer for fish from North Carolina than for fish from the more southern sites. As a result, fish were larger at settlement to North Carolina. Estimated juvenile growth rates ranged between 0.62 and 0.88 mm/d and differed across sites and years, growth being generally faster at the southern sites. Water temperature accounts for some of this variability; however, site-specific differences in other factors probably contributed to some of the observed differences in growth. Back-calculated spawning patterns showed a lunar association with the new and first-quarter moons at all sites except for North Carolina. Settlement patterns were lunar cyclic as well: settlement pulsed during the third-quarter and new moons at all sites, and in North Carolina an additional pulse associated with the full moon was present. Patterns of larval and juvenile growth coupled with recruitment dynamics across the latitudinal gradient are consistent with northward Gulf Stream transport of larvae from southern spawning sites.

Full text

1339
Transactions of the American Fisheries Society 133:1339–1355, 2004
q
Copyright by the American Fisheries Society 2004
Growth Variation, Settlement, and Spawning of Gray Snapper
across a Latitudinal Gradient
K
ELLY
D
ENIT
*
AND
S
U
S
PONAUGLE
Division of Marine Biology and Fisheries,
University of Miami, Rosenstiel School of Marine and Atmospheric Science,
4600 Rickenbacker Causeway, Miami, Florida 33149, USA
Abstract.—Newly recruited juvenile gray snapper Lutjanus griseus were collected each fall for
two consecutive years (2000 and 2001) from sites in Florida and North Carolina. Spawning,
settlement, and growth patterns were compared across sites based on otolith microstructure.Larval
otolith growth trajectories were generally similar for larvae from different sites and years; however,
the mean pelagic larval duration (PLD) was 1 d longer for fish from North Carolina than for fish
from the more southern sites. As a result, fish were larger at settlement to North Carolina. Estimated
juvenile growth rates ranged between 0.62 and 0.88 mm/d and differed across sites and years,
growth being generally faster at the southern sites. Water temperature accounts for some of this
variability; however, site-specific differences in other factors probably contributed to some of the
observed differences in growth. Back-calculated spawning patterns showed a lunar association
with the new and first-quarter moons at all sites except for North Carolina. Settlement patterns
were lunar cyclic as well: settlement pulsed during the third-quarter and new moons at all sites,
and in North Carolina an additional pulse associated with the full moon was present. Patterns of
larval and juvenile growth coupled with recruitment dynamics across the latitudinal gradient are
consistent with northward Gulf Stream transport of larvae from southern spawning sites.
A complete understanding of the population dy-
namics of a marine organism necessitates collec-
tion of data on all components of its life history.
The complex life histories of benthic marine fish
create difficulties in studying the pelagic larval
phase. Consequently, we have relatively little
knowledge of events occurring during larval life,
including where larvae go and where successful
settlers have come from.
Although the gray snapper Lutjanus griseus is
ecologically and economically important and basic
fishery data have been collected on adults (Man-
ooch and Matheson 1984; Rutherford et al. 1983;
Burton 2001), relatively little is known about lar-
val life and the transition to settled juveniles. The
geographic range for this species covers the west-
ern Atlantic from Florida through Brazil, including
Bermuda, the Caribbean, and the northern Gulf of
Mexico (Robins et al. 1986). Even though gray
snapper do not survive the winter water temper-
atures of higher latitudes (Burton 2001), juveniles
have been reported from as far north as Massa-
chusetts (Sumner et al. 1911), and settlement stage
larvae have been found in icthyoplankton samples
from North Carolina (Hettler and Barker 1993;
Tzeng et al. 2003). The majority of gray snapper
* Corresponding author: kdenit@rsmas.miami.edu
Received August 29, 2003; accepted April 23, 2004
landings from the southeast USA occur in Florida
(Burton 2001).
As one of the top predators in sea grass beds
and on coral reefs, gray snapper have an important
ecological role in marine ecosystem communities.
In sea grass beds, gray snapper have been shown
to consume mainly shrimp, crabs, and fish—es-
pecially toadfish (Croker 1962; Starck and Schroe-
der 1971). Snapper removal from an ecosystem has
been associated with significant changes in the
food web on coral reefs in Cuba (Claro 1991) and
the Florida Keys (Ault et al. 1998).
Adult gray snapper are associated with coral
reefs, shipwrecks, rocky outcroppings, mangroves,
and other natural live-bottom areas (Miller and
Richards 1980; Claro et al. 2001; Ley and McIvor
2002). During new and full moons of summer
months, adults aggregate on outer reef tracts in the
Florida Keys for spawning (Starck and Schroeder
1971; Domeier et al. 1996; Lindeman et al. 2001;
but see Allman and Grimes 2002). However, the
geographic destination of eggs and larvae from
these spawning events is unknown.
After a pelagic larval duration (PLD) of 22–42
d (Lindeman 1997; Allman and Grimes 2002;
Tzeng et al. 2003), larvae settle into shallow es-
tuarine sea grass and mangrove nursery areas
(Laegdsgaard and Johnson 2001; Nagelkerken et
al. 2001). With an intermediate PLD and the pos-
sibility of entrainment into the Gulf Stream, a

1340
DENIT AND SPONAUGLE
F
IGURE
1.—Map of the southeastern United States in-
dicating the five study sites by name and abbreviation.
broad geographical range of dispersal is possible
for gray snapper. The question is whether these
settlers are transported varying distances from a
common spawning area or come from multiple
sources.
Recruitment of juveniles into a population clear-
ly influences population dynamics. However, var-
iability in recruitment is difficult to predict without
understanding the details of events occurring dur-
ing the larval phase. This study was designed to
measure the scope of variability in several early
life history traits of gray snapper. Growth rates
and survivorship are influenced by various phys-
ical and biological factors such as diet and envi-
ronment (e.g., Boehlert and Yoklavich 1983; Mill-
er et al. 1988; Buckel et al. 1995; Tupper and Bou-
tilier 1995; Johnson and Evans 1996). Growth fur-
ther influences larval duration (Searcy and
Sponaugle 2000), which, in turn, theoretically con-
strains maximum dispersal distances. Fortunately,
valuable information about the early life history
phases can be obtained from otoliths (ear stones).
Daily increment deposition in otoliths and changes
in deposition (appearance) during life history tran-
sitions provide a measure of age, including PLD
and postsettlement age at capture (Campana and
Neilson 1985). These data can be used to back-
calculate the timing of settlement and spawning,
and the widths of increments provide a measure
of relative growth at particular ages.
We used otoliths to investigate variation in early
life history traits of gray snapper from Florida and
North Carolina. Based on the collection of recruits
(successful settlers), we compared the timing of
settlement and spawning over this same spatial
scale to examine the linkages between larval
growth, PLD, and the timing of settlement. We
analyzed larval otolith growth trajectories to in-
vestigate the relationship between growth and
PLD, and we explored the possible effects of lat-
itudinal differences in environmental conditions
(i.e., temperature) by analyzing growth during the
juvenile period. Larval and juvenile growth pat-
terns combined with lunar settlement and spawn-
ing relationships provide a better understanding of
the larval and juvenile life stages of gray snapper
and insight into the possible source areas and
transport of these fish.
Methods
Sample collections.—Early-stage(young-of-the-
year) juvenile gray snapper were collected in 2000
and 2001 from four sites along the Florida coast
(Sebastian Inlet, Jupiter, Biscayne Bay,and Florida
Bay) and one site off the coast of North Carolina
near Beaufort Inlet (Core Sound; Figure 1). A min-
imum of 15 fish were collected at each site each
year in September and October (Table 1). Samples
were collected with a 21.3-m push seine with 1-
mm mesh at all sites except Core Sound and Flor-
ida Bay. In Core Sound and Florida Bay, a 3-m-
long otter trawl with 6.4-mm mesh was used for
collections. Florida Fisheries and Wildlife Com-
mission and National Oceanic and Atmospheric
Administration–National Marine Fisheries Service
Beaufort laboratory personnel collected these sam-
ples as part of their routine sampling. During sam-
pling, data collected included GPS position, bot-
tom type, shore type, water temperature, salinity,
and tidal stage. Florida Bay was not sampled in
2001 because of permit restrictions. Samples were
frozen and transported to the University of Miami–
Rosenstiel School of Marine and AtmosphericSci-
ence (RSMAS) for analysis.
Daily age estimation and growth.—All fish col-
lected were used for otolith age estimation. Before
dissection, each fish was weighed (wet weight, g)

1341
GROWTH VARIATION AND SPAWNING OF GRAY SNAPPER
T
ABLE
1.—Distribution of aged juvenile gray snapper at five different sites during 2000 and 2001. Fish were collected
from mid-September to mid-October from Florida Bay (FLB), Biscayne Bay (BIS), Jupiter (JUP), Sebastian Inlet (SEB),
and Core Sound (COS) and are shown by month of collection. The average monthly temperature (
8
C) is also given.
Month
Number or
temperature
2000
FLB BIS JUP SEB COS
2001
FLB BIS JUP SEB COS
Sep
Oct
Number
Temperature
Number
Temperature
0
28.7
15
26.9
32
29.7
20
27.4
22
32.0
12
30.5
0
28.7
49
26.8
28
25.6
18
21.0
0
28.6
0
27.3
0
28.9
31
27.4
25
28.5
10
26.5
0
28.2
40
26.8
17
25.4
13
20.4
F
IGURE
2.—The transverse section of a sagittal otolith from a Core Sound gray snapper, the core and settlement
areas being indicated by arrows. All readings were made along the anterior dorsal area of the otolith from the core
to the outer edge. The otolith was taken from a 31.73-mm (SL) juvenile that was 53 d old.
and its standard length (SL) was measured to the
nearest 0.1 mm by digital calipers. Standard tech-
niques were used to dissect each fish to remove
the sagittal otoliths (Brothers 1987). One sagitta
was used for aging. A randomly selected otolith
from each fish was mounted in epoxy, sectioned,
polished, and read according to standard protocols
(Secor et al. 1991). Otoliths were examined under
a Leica transmitted-light microscope at 400
3
. The
microscope image was captured with a frame grab-
ber and displayed on a computer screen. Using
Image-Pro image analysis software (Media Cy-
bernetics 1998), we enumerated increments along
the anterior dorsal section of the otolith from the
core to the outer edge. A consistent reading axis
was selected that was not the longest axis of either
larval or juvenile otolith growth, but one along
which increments were visible to the edge. Otolith
radius (
m
m)-at-age was recorded for every day of
the larval and juvenile periods. The timing of set-
tlement was determined by examining otoliths for
optical marks associated with settlement (Figure
2). Using these data, we could determine the larval
duration and juvenile age (including a 3 d correc-
tion for time to first ring formation; Lindeman
1997), as well as daily growth rates (increment
widths) during larval and juvenile periods. Age-
specific otolith growth rates were obtained for sev-
eral periods during the larval stage. Somatic
growth rates were estimated by linear regression
of SL on age, based on otolith microincrement
counts (Szedlmayer and Conti 1999).
Based on age validation studies by Allman
(1999) and Ahrenholz (2000), each increment was
assumed to reflect 1 d of growth. We followed a
standard protocol for reading and interpreting the

1342
DENIT AND SPONAUGLE
otoliths. First, all unclear, abnormally shaped
(nonlinear growth axis) sagittae were discarded. A
sagitta from each specimen was read twice inde-
pendently by the same reader. If the increment
counts were within 5% of each other, one mea-
surement was randomly selected for analysis
(Searcy and Sponaugle 2000). If the increment
counts differed by more than 5%, the otolith was
read again. If the increment counts from the third
reading differed from the other readings by more
than 5%, the otolith was discarded. If the differ-
ence on the third count was less than 5% of one
of the former readings, then one of these two mea-
surements was randomly selected for analysis.
Data analysis.—The larval increment width data
(growth trajectories) were analyzed by using
repeated-measures analysis of variance (MANO-
VA). This technique allows comparisons to be
made at the resolution of an individual fish (Cham-
bers and Miller 1995; Meekan and Fortier 1996)
and is needed for longitudinal data where data
points are not independent (i.e., more than one
measurement from each fish). MANOVA compar-
isons were made among groups with the null hy-
pothesis of no differences among groups. The in-
teraction term used was Wilk’s
l
, which is based
on sample size, number of groups in the compar-
ison, and number of intervals being analyzed. Sep-
arate one-way analyses of variance (ANOVAs)
were used to compare PLDs and otolith size at
settlement within each year because Florida Bay
was not sampled in the second year (Underwood
1997). Where applicable, Tukey’s multiple com-
parison test was used to identify site-specific dif-
ferences (Zar 1984).
Analysis of covariance (ANCOVA) was used to
compare the slopes (growth rates) of the regres-
sions of standard length on days postsettlement
(Sokal and Rohlf 2000). In 2001, no small (SL
,
25 mm) juvenile fish were collected at Core Sound,
which created a problem. The length–age regres-
sion line for the fish from Core Sound produced
a y-intercept of 4.0 mm. Because settlement at a
size of 4 mm is not biologically realistic, this result
is most likely an artifact of the lack of younger
fish. The regressions for fish from all the other
sites in both years, including Core Sound fish from
2000, had a y-intercept of 7–11 mm (see Results).
In North Carolina, Tzeng et al. (2003) found in-
gressing gray snapper to have a size range of 11–
16 mm. We estimated size at settlement for the
Core Sound fish from the otolith radius at settle-
ment. Relationships of SL to otolith radius by site
for all of the fish collected were calculated and
compared by ANCOVA. The resulting statistics
showed that in the year 2000 the SL–otolith radius
for Florida Bay fish was significantly different
from all the other sites (ANCOVA, P
,
0.01; Tu-
key’s test, P
,
0.01). For the fish collected in 2001
there was no significant difference among sites in
the relationship between SL and otolith radius
(ANCOVA, P
5
0.74). When fish from Florida
Bay in 2000 were excluded, there was no signif-
icant difference between years (ANCOVA, P
5
0.32). Combining all of the SL–otolith radius data
(except Florida Bay) generated a regression equa-
tion of y
5
0.1017x
2
9.7 (R
2
5
0.86). From this
equation, the mean otolith radius at settlement for
fish from Core Sound in 2001 (199.82
m
m) was
equivalent to a size at settlement of 10.62 mm.
Given this more realistic size at settlement, we
forced the regression for the Core Sound fish from
2001 through this y-intercept. All statistical com-
parisons were made by using this adjusted regres-
sion line.
To determine whether settlement peaked during
a particular time of the lunar month, day of set-
tlement was assigned a lunar day, from 1 (new
moon) to 29 and the distribution of settlement over
the lunar cycle was analyzed by using Rayleigh
circular statistics (Zar 1984). The same technique
was used to analyze back-calculated spawning pat-
terns.
Results
We collected a total of 514 juvenile gray snapper
over all sites, 382 (74%) of which had readable
otoliths. Of those, 342 (90%) had increment counts
that were within 5% of each other and therefore
were included in the final analysis. The wet
weights of collected fish ranged from 0.05 to 8.49
g, the size range from 11.6 to 65.1 mm, SL, and
postsettlement age from 2 to 60 d. In 2000, Florida
Bay fish had the highest mean size and postsettle-
ment age, followed by Core Sound (Figure 3). In
2001, Core Sound fish had the greatest mean size
and postsettlement age (Florida Bay was not sam-
pled).
The larval otolith growth trajectories for year
2000 fish were not significantly different among
sites (Table 2; Figure 4). In 2001, the only sig-
nificant difference was between Jupiter and Se-
bastian Inlet fish, the Jupiter fish having signifi-
cantly faster growth in the week before settlement.
Larval otolith growth trajectories for fish at a given
site did not differ between years (Table 2).
Pelagic larval duration is related to larval
growth in that faster-growing larvae often settle

1343
GROWTH VARIATION AND SPAWNING OF GRAY SNAPPER
F
IGURE
3.—Standard length and age histograms for juvenile gray snapper captured in (A) 2000 and (B) 2001.
The study sites are plotted from top to bottom in order of their latitudinal location (north at the top, south at the
bottom). See Figure 1 for site abbreviations.

1344
DENIT AND SPONAUGLE
T
ABLE
2.—Results of repeated-measures MANOVA of
larval otolith growth increments of gray snapper collected
from the sites identified in Table 1. P-values are provided
for the interaction terms; asterisks indicate significant dif-
ferences at P
,
0.05.
Years(s) Site
Site
BIS JUP SEB COS
2000 FLB
BIS
JUP
SEB
0.450 0.496
0.790
0.246
0.407
0.052
0.155
0.329
0.581
0.269
2001 BIS
JUP
SEB
0.213 0.359
0.032*
0.223
0.575
0.590
2000–2001 0.597 0.200 0.534 0.391
earlier (Searcy and Sponaugle 2000). Despite sim-
ilar larval growth trajectories, PLDs of fishes dif-
fered significantly among sites (ANOVA; P
5
0.001 for year 2000, P
5
0.014 for year 2001, P
5
0.037 between years). The PLDs of fish from
the most northern location were longer than those
from southern locations in both years. In 2000,
Core Sound fish had significantly longer PLDs
than fish from Biscayne Bay and Jupiter (Table 3;
Figure 5). In 2001, Core Sound and Sebastian Inlet
fish had significantly longer PLDs than fish from
Jupiter. Within sites, fish from Biscayne Bay and
Sebastian Inlet had significantly longer PLDs in
2001 than in 2000.
Size at settlement (as reflected in the otolith set-
tlement radius) is a function of larval growth rates
and PLD. During both years, snapper from the
more northern sites had larger otolith radii at set-
tlement than did those from the more southern sites
(ANOVA; P
,
0.01 for year 2000, P
5
0.009 for
year 2001; Table 4). In 2000, Core Sound fish had
a significantly larger otolith radius at settlement
than did fish from all of the other sites. In addition,
Sebastian Inlet juveniles had a significantly larger
otolith radius at settlement than Biscayne Bay ju-
veniles. This trend of larger size at settlement for
the northern sites compared to the southern sites
also was evident in 2001, but differences were only
significant between Core Sound and Jupiter, and
between Sebastian Inlet and Jupiter (Table 4).
Within sites, only fishes settling to Biscayne Bay
had a larger mean otolith size at settlement in 2001
(ANOVA; P
5
0.006; Table 4).
To examine juvenile growth, we calculated
growth rates for each site by regressing standard
length on juvenile (postsettlement) age (Table 5;
Figure 6). Growth rates ranged from 0.62 to 0.88
mm/d. In 2000, juvenile growth rates differed sig-
nificantly across sites (ANCOVA; P
5
0.002);
Florida Bay fish grew significantly faster than the
Core Sound and Sebastian Inlet fish (Table 5). In
2001 (ANCOVA; P
5
0.001), the only significant
difference in growth rates occurred between Ju-
piter and Sebastian Inlet, with Jupiter fish having
faster growth rates than fish from Sebastian Inlet
(Table 5). There also were differences within sites
between years (ANCOVA; P
5
0.006); at Core
Sound, snapper growth rates during 2001 were sig-
nificantly faster than in 2000 (Table 5). There was
a significant positive relationship between juvenile
growth rate and mean temperature, indicating that
temperature contributed to some variation in
growth rate (Figure 7).
To examine the relationship between PLD and
the timing of settlement (whether differences in
PLD resulted in differences in the timing of set-
tlement), we examined the timing of settlement to
each site over a lunar cycle (Figure 8). In 2000,
the distribution of gray snapper settlement to Se-
bastian Inlet and Biscayne Bay was not uniformly
distributed over the lunar cycle. Peaks in settle-
ment occurred at days 29.7 and 23.4, correspond-
ing to the third-quarter and new moons, respec-
tively. In 2001, fish from Core Sound and Sebas-
tian Inlet had nonuniform settlement distributions,
settling in peaks associated with the first-quarter
moon (day 5.3) and new moon (day 27.8), re-
spectively. Overall, settlement occurred frequently
around the third-quarter and new moons, except
at Core Sound where additional fish settled be-
tween the first-quarter and full moons, leading to
an overall statistically uniform distribution in
2000.
In both years, back-calculated spawning dates
ranged from late June to early October, peaking in
July and August. In 2000, spawning dates ranged
from late June to early October. In 2001, spawning
dates covered a slightly narrower window from
early July to late September. When the data were
collapsed into a single lunar cycle, fish that settled
to Biscayne Bay and Sebastian Inlet in 2000 were
spawned nonuniformly over the lunar cycle (Fig-
ure 9). Biscayne Bay fish were spawned primarily
during the new moon (day 2.5), whereas Sebastian
Inlet fish were spawned during the first-quarter
moon (day 8.0). In 2001, fishes from Biscayne Bay
and Sebastian Inlet had nonuniform spawning dis-
tributions with peaks associated with the new
moon (days 26.8 and 2.8, respectively), and gray
snapper from Core Sound were spawned mainly
during the first-quarter moon (day 9.7). Overall,
in both years, spawn dates were clustered around

1345
GROWTH VARIATION AND SPAWNING OF GRAY SNAPPER
F
IGURE
4.—Mean increment width as a function of larval increment number plotted to the mean pelagic larval
duration for each year (without 3-d correction) for fish captured in (A) 2000 and (B) 2001 at the sites identified
in Figure 1.

1346
DENIT AND SPONAUGLE
T
ABLE
3.—Mean pelagic larval durations (PLD; d) by site and year for gray snapper collected from the sites identified
in Table 1. P-values are for Tukey pairwise tests comparing pelagic larval duration between sites for 2000 and 2001
and within sites between years; asterisks indicate significant differences at P
,
0.05.
Year and
statistic
Site
FLB BIS JUP SEB COS
2000
Mean PLD
n
24.4
15
24.5
52
24.7
47
24.9
48
26.1
46
P
FLB
BIS
JUP
SEB
1.000 1.000
0.992
0.931
0.880
0.699
0.059
0.002*
0.002*
0.054
2001
Mean PLD
n
25.6
36
25.3
35
26.7
39
26.9
23
P
BIS
JUP
SEB
0.901 0.233
0.048*
0.170
0.040*
0.973
2000–2001
P 0.037* 0.066 0.001* 0.102
F
IGURE
5.—Pelagic larval durations of gray snapper collected in 2000 and 2001 from five sites. The histograms
are plotted from top to bottom in latitudinal order (north at the top, south at the bottom); sites are identified in
Figure 1.

1347
GROWTH VARIATION AND SPAWNING OF GRAY SNAPPER
T
ABLE
4.—Mean otolith radius at settlement (
m
m) as a proxy for size at settlement by site and year for gray snapper
collected from the sites identified in Table 1. P-values are for Tukey pairwise tests comparing radius at settlement
between sites for 2000 and 2001 and within sites between years; asterisks indicate significant differences at P
,
0.05.
Year and
statistic
Site
FLB BIS JUP SEB COS
2000
Mean otolith radius
n
180.92
15
179.09
52
182.17
47
190.80
48
204.97
46
P
FLB
BIS
JUP
SEB
0.998 1.000
0.948
0.402
0.018*
0.248
0.000*
0.000*
0.000*
0.003*
2001
Mean otolith radius
n
192.77
36
179.38
35
195.86
39
199.82
23
P
BIS
JUP
SEB
0.108 0.95
0.024*
0.715
0.012*
0.931
2000–2001
P 0.006* 0.632 0.274 0.277
T
ABLE
5.—Juvenile growth rates (mm/d) of gray snapper collected from the sites identified in Table 1 by site and
year based on least-squares regression of standard length on days postsettlement. The P-values from an ANCOVA
comparing the growth rates from each site for 2000 and 2001 and within sites between years are provided for each
comparison; asterisks indicate significant differences at P
,
0.05.
Year and
statistic
Site
FLB BIS JUP SEB COS
2000
Slope
Intercept
R
2
n
0.8736
8.230
0.86
15
0.7953
7.214
0.83
52
0.8848
6.590
0.82
34
0.6865
9.113
0.90
48
0.6172
10.949
0.74
46
P
FLB
BIS
JUP
SEB
0.141 0.858
0.343
0.013*
0.582
0.009*
0.001*
0.175
0.000*
0.937
2001
Slope
Intercept
R
2
n
0.8060
8.080
0.78
36
0.8023
9.242
0.74
35
0.6757
10.071
0.92
39
0.7187
10.620
0.76
23
P
BIS
JUP
SEB
0.071 0.203
0.000*
0.990
0.260
0.209
2000–2001
P 0.321 0.962 0.245 0.000*

1348
DENIT AND SPONAUGLE
F
IGURE
6.—Regression of standard length on days postsettlement for gray snapper captured in (A) 2000, and
(B) 2001 from the sites identified in Figure 1. Slopes and intercepts are given in Table 5.

1349
GROWTH VARIATION AND SPAWNING OF GRAY SNAPPER
F
IGURE
7.—Regression of mean juvenile growth rate
on mean temperature (September and October) for gray
snapper juveniles captured in 2000 and 2001 from the
five collection sites. See Table 1 for site-specific tem-
peratures. A least-squares regression line was fit to the
data from both years (y
5
0.0249x
1
0.0849; R
2
5
0.49,
P
,
0.001).
F
IGURE
8.—Back-calculated settlement pattern, by site and year, of juvenile gray snapper plotted over a single lunar
cycle. Rayleigh circular tests (Z-statistic) were used to test uniformity; where settlement was nonuniform, arrows
indicate the mean lunar day of settlement. Day 1
5
new moon; day 15
5
full moon. Site codes as in Figure 1.
the new and first-quarter moons. The exception
was in 2000, where additional spawning was as-
sociated with the full and third-quarter moons at
Core Sound, which led to an overall statistically
uniform distribution (Figure 9).
Discussion
Larval Growth Trajectories
Larval otolith growth trajectories for juvenile
gray snapper were similar across sites in both years
except that in 2001 fish from Jupiter grew signif-
icantly faster than fish from Sebastian Inlet. The
significant difference in growth occurred only dur-
ing the last week before settlement as the larval
growth trajectories of Sebastian Inlet fish leveled
off before settlement relative to fish from the other
sites. Latitudinal differences in water temperature
are unlikely to be the cause of this difference be-
cause Sebastian Inlet and Jupiter are geographi-
cally close and had similar water temperatures.
Further, larval growth rates of Core Sound fish did
not differ from those at Sebastian Inlet, which

1350
DENIT AND SPONAUGLE
F
IGURE
9.—Back-calculated spawning pattern, by site and year, of juvenile gray snapper plotted over a single lunar
cycle. Rayleigh circular tests (Z-statistic) were used to test uniformity; where settlement was nonuniform, arrows
indicate the mean lunar day of settlement. Day 1
5
new moon; day 15
5
full moon. Site codes as in Figure 1.
would be expected if differences in water temper-
ature were significantly influencing the last portion
of larval growth. A site-specific difference such as
decreased primary production near Sebastian Inlet
may have contributed to reduced larval growth be-
fore settlement as well as lower juvenile growth
rates (see below). Overall, however, the trends of
larval growth were similar among sites and years,
suggesting that fish settling to different sites may
have occupied a similar water mass during their
larval phase and may have been transported from
spawning sites by analogous paths.
Pelagic Larval Duration
Settlement marks on the otoliths of gray snapper
appeared similar to those of several other reef fish
species (Brothers and McFarland 1981; Victor
1982; Sponaugle and Cowen 1994): a darker ring
followed by narrower and more regular growth
rings during juvenile life. The PLDs measured for
juvenile gray snapper in this study were very sim-
ilar to those calculated for juvenile gray snapper
along the west coast of Florida (25 d; Allman and
Grimes 2002), in Florida and Cuba (25–40 d; Lin-
deman 1997), and for newly settled juveniles col-
lected along the coast of North Carolina (30 d;
Tzeng et al. 2003; for consistency with this study,
we added to Tzeng et al.’s increment counts a 3-
d correction factor for time to first ring formation).
The higher range in PLDs for snapper in Linde-
man’s (1997) study may result from inclusion of
snapper from Cuba. Cuban fish may be spawned
from an island source population (C. Paris, UM–
RSMAS, personal communication) and thus may
have different PLDs than do fish spawned along
the southeastern United States. Despite the overall
similarity in larval growth trajectories for fish in
the present study, the PLDs of these fish were sig-
nificantly different between the northern site and
the southern sites. In both years, Core Sound fish
had longer PLDs than fish from more southern
sites. Although differences among sites were not
always significant, there was a consistent trend in
both years for longer PLDs at more northern sites.

1351
GROWTH VARIATION AND SPAWNING OF GRAY SNAPPER
The difference in PLDs, despite similar larval
growth trajectories, suggests that habitat avail-
ability, rather than growth, determined the timing
of settlement. Other reef species have been shown
to delay settlement until suitable habitat is found
(Victor 1986; Cowen 1991; Sponaugle and Cowen
1994).
Similar larval growth trajectories and slightly
longer northern PLDs suggest that snapper larvae
occupied the same or similar water masses origi-
nating south of North Carolina. If fish were trans-
ported north from Florida by the Gulf Stream, a
small time lag may have been associated with find-
ing suitable settlement habitat. Rough calculations
indicate that PLDs are sufficient for larvae to be
transported from known spawning aggregation
sites around the Dry Tortugas (Domeier et al.
1996; Lindeman et al. 2001) 2,790 km to Cape
Lookout, North Carolina (close to Core Sound).
Based on an average Gulf Stream speed of 1.25
m/s (Hare and Cowen 1996), a planktonic organ-
ism could travel 2,808 km in 26 d, which places
gray snapper larvae at approximately the right lo-
cation by the time of their mean PLD. The inter-
action of active larval behavior and real Gulf
Stream currents would result in variation around
this estimate. Gray snapper larvae may be trans-
ported by way of the Gulf Stream to North Car-
olina and then across the continental shelf (Govoni
and Pietrafesa 1994) into nearshore estuarine hab-
itats, as are other larval fishes that utilize estuaries
(Hare et al. 1999). Although analysis of juvenile
gray snapper from Georgia and South Carolina
would allow for greater spatial resolution, low
numbers of juveniles precluded collections from
these areas (J. Hare, NMFS Beaufort, personal
communication).
Size at Settlement
Otolith size (radius) at settlement (reflecting so-
matic size at settlement) is related to larval growth
rates and PLD. Although faster growing larvae
typically have larger sizes-at-age, they are often
smaller at settlement because they spend a shorter
period in the plankton (Searcy and Sponaugle
2000). As a result of the longer time spent in the
larval stage (i.e., longer PLD), Core Sound fish
were significantly larger at settlement than fish
from many of the other sites in both years. Fish
from Sebastian Inlet also were larger at settlement
than fish from Jupiter (2001) and Biscayne Bay
(2000). Given that the mean increment width for
snapper just before settlement was approximately
15
m
m, one additional day in the larval period for
Core Sound fish led to a significant increase in
otolith radius. Such PLD-induced differences in
otolith radius are apparent among years as well:
2001 Biscayne Bay fish had a significantly larger
otolith radius at settlement than those in 2000 be-
cause the PLD was significantly longer in 2001.
Thus, despite generally similar larval growth tra-
jectories, longer PLDs of fish settling to the north-
ern site led to additional somatic and otolith
growth and an increased size at settlement for
those fish. Calculated size at settlement based on
the regression of standard length on postsettlement
age for fish from Core Sound in this study is con-
sistent with settlement sizes found in a study of
ingressing gray snapper in North Carolina (Tzeng
et al. 2003).
Juvenile Growth Rates
The characteristics of water masses occupied by
larval gray snapper collected in this study are not
known; however, juveniles were collected from
distinct locations characterized by different envi-
ronmental conditions. A trend of faster juvenile
growth for fish from the more southern sites was
evident in the growth rates calculated by regress-
ing standard length on postsettlement age. In both
years growth rates were significantly different
among sites. Juvenile growth rates tracked the lat-
itudinal gradient in both years, but these differ-
ences were most apparent in 2000 when fishes
from the southern sites, Florida Bay and Jupiter,
grew the fastest, and fishes from the northernmost
site, Core Sound, grew the slowest. In 2000 the
mean water temperature in September–October
ranged from 28.7
8
C to 27.4
8
C in Florida Bay and
from 25.6
8
C to 21.0
8
C at Core Sound. Water tem-
perature was highest in Jupiter (32–30.5
8
C), where
fish had the highest growth rate. Latitudinal var-
iation in water temperature is a probable expla-
nation, given that growth is directly related to wa-
ter temperature for many species (e.g., Lang et al.
1994; Nixon and Jones 1997). However, changes
in other environmental factors cannot be ruled out.
For example, in 2001, fish from Sebastian Inlet
grew more slowly than fish from Jupiter despite
rather similar water temperatures in that year. The
broader shelf of Sebastian Inlet likely results in a
different oceanographic regime, which could, for
example, influence prey availability.
In general, temperature differences among sites
accounted for at least half of the variability in
juvenile growth rates. Clearly, other factors must
have contributed to this variability. We have no
data on prey availability or consumption differ-

1352
DENIT AND SPONAUGLE
ences among sites. All of the juveniles were col-
lected in sea grass beds, the fish in Florida being
collected in sea grass beds near mangroves. No
doubt there are differences in species of sea grass
and other community parameters, but no compa-
rable work is available on habitat-specific differ-
ences in growth, so robust habitat differences can-
not be evaluated in this study.
Overall, the mean juvenile growth rates calcu-
lated in this study (0.62–0.88 mm/d) were similar
to the growth rates calculated for juvenile gray
snapper by other workers. Lindeman’s (1997) cal-
culated growth rate of 0.92 mm/d may be slightly
higher because of the inclusion of Cuban gray
snapper, which may be experiencing different en-
vironmental conditions. Tzeng et al. (2003) used
newly settled (11–16 mm) snapper to calculate a
lower mean growth rate of 0.50 mm/d for snappers
from North Carolina. The difference between our
Core Sound growth rate and Tzeng et al.’s (2003)
may be due to the larger size range (20–55 mm
SL) of fish used in our study. Selective mortality
of slower growers over time (see review by Sogard
1997) may skew the growth trajectories of older
survivors toward faster growth. This also may
have contributed to differences in growth rates be-
tween years at Core Sound in our study. Allman
and Grimes (2002) sampled juveniles from the en-
tire west coast of Florida and found growth rates
of 1.0 mm/d in 1996 and 0.6 mm/d in 1997. In
contrast to the present study, they found no sig-
nificant difference in growth rates among fish
across a latitudinal gradient from the panhandle to
the southwestern tip of Florida.
Settlement and Spawning
The timing of settlement was generally coherent
among most sites in Florida. In 2000, settlement
of gray snapper to Biscayne Bay and Sebastian
Inlet pulsed with the third-quarter and new moons.
Settlement to Florida sites was less distinct in 2001
(only Sebastian Inlet fish had a significant pulse
during the third-quarter to new moon), but the pat-
terns were roughly similar to those seen in 2000.
Settlement to Core Sound during 2000 occurred
during the same period, but another pulse occurred
during the first-quarter to full moon, 15 d later.
Settlement of 2001 fish to Core Sound was entirely
different, pulsing during the first-quarter moon. In
general, fish at all of the sites except Core Sound
settled in pulses associated with the third-quarter
and new moons. These results differ somewhat
from previous studies on the settlement pattern of
gray snapper. Tzeng et al. (2003) found that major
pulses of ingressing snapper in North Carolina oc-
curred during the new moon, with smaller numbers
arriving around the full moon over the course of
a 2-year study. Tzeng et al.’s (2003) study used
settlement-stage gray snapper to analyze settle-
ment patterns, whereas in this study we focused
on early juveniles. Therefore, the slight difference
in lunar settlement patterns might be the result of
selective mortality. Allman and Grimes (2002)
found settlement along the west coast of Florida
to be marginally associated with the new moon in
one of the years of their sampling but not in the
other. Contrary to Smith (1995), who found no
correlation between settlement and the lunar cycle
in Sebastian Inlet, during both years of this study
gray snapper settlement to Sebastian Inlet was sig-
nificantly associated with the third-quarter to new
moon. Settlement during this time of the lunar cy-
cle may reflect both light levels and tidal amplitude
cycles. Predation risk is thought to be lower during
the waning moon because of reduced light levels
(Johannes 1978), which may increase the likeli-
hood of survival for larvae settling during the
third-quarter and new moons. Core Sound snapper
exhibited the greatest variability in the timing of
settlement, which may reflect longer transport
times to Core Sound. If snapper are transported
from distant sources, larvae may have fewer op-
tions and be less able to synchronize their settle-
ment to environmental cues. The trade-off between
remaining in the plankton and settling during op-
timum conditions probably shifts as larvae get old-
er (Sponaugle and Pinkard 2004a, 2004b).
Back-calculated successful spawning dates were
also more similar among Florida sites. In the year
2000, recruits from Biscayne Bay and Sebastian
Inlet were spawned primarily during the new and
first-quarter moons. A similar pattern was apparent
in 2001. In contrast, successful spawning of Core
Sound fish was associated with the first-quarter
moon in 2001 but was not significantly different
from uniform timing in 2000 because of a strong
peak associated with the full to third-quarter moon
and a weaker peak at the new first-quarter moon.
Spawning pulses during the new moon agree with
previously published data. Tzeng et al. (2003)
found that juvenile gray snapper collected from
North Carolina had back-calculated spawning
dates associated with the new moon. Domeier et
al. (1996) concluded that adult spawning peaked
during the new and full moons. Allman and Grimes
(2002) found a marginal association of spawning
with the lunar cycle in 1 year of sampling but no
association in the second year. The difference in

1353
GROWTH VARIATION AND SPAWNING OF GRAY SNAPPER
successful spawning patterns between Core Sound
fish and the other sites may be related to the con-
straints associated with long-distance transport.
The differences in the settlement patterns of
gray snapper from the Florida sites and Core
Sound despite similar larval growth rates are con-
sistent with transport of larvae up the southeastern
U.S. coast. Similar larval otolith growth trajec-
tories suggest that larvae occupy the same or sim-
ilar water masses, such as the Gulf Stream.Slightly
longer PLDs for fish settling to North Carolina are
not due to differences in larval growth rates but
more likely are the result of lack of access to suit-
able settlement habitat. Our findings are consistent
with the idea that these larvae are Gulf Stream
exports (Burton 2001); however, future studies
will combine these age and growth data with oto-
lith microchemistry data to gain a better under-
standing of the population connectivity for this
species.
Acknowledgments
This study was conducted as part of a larger
study on snapper population connectivity in col-
laboration with S. Thorrold (WHOI), J. Hare
(NMFS, Beaufort), R. Cowen (UM- RSMAS), and
L. Barbieri (FFWCC). This work is a result of
research sponsored in part by NOAA Office of Sea
Grant, U.S. Department of Commerce, under Grant
No. NA96RG00025 to the Virginia Graduate Ma-
rine Science Consortium and Virginia Sea Grant
College Program. The U.S. Government is autho-
rized to produce and distribute reprints for gov-
ernmental purposes, notwithstanding any copy-
right notation that may appear hereon. We thank
J. Hare, NMFS Beaufort Laboratory, and L. Bar-
bieri and E. McDevitt, Florida Fish and Wildlife
Conservation Commission, for sample collection.
J. Fortuna (UM-RSMAS) and E. Laban (NMFS
Beaufort) provided guidance in the techniques of
preparing otolith sections. The manuscript bene-
fited from conversations with or comments of S.
Thorrold, J. Hare, R. Cowen, J. Serafy, D. Benetti,
C. Paris, K. Lindeman, K. Grorud-Colvert, and
three anonymous reviewers.
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