Spatial and temporal distribution of grouper larvae (Serranidae: Epinephelinae: Epinephelini) in the Gulf of Mexico and straits of Florida.
Subject: Fishes (Analysis)
Authors: Marancik, Katrin E.
Richardson, David E.
Lyczkowski-Shultz, Joanne
Cowen, Robert K.
Konieczna, Malgorzata
Pub Date: 01/01/2012
Publication: Name: Fishery Bulletin Publisher: National Marine Fisheries Service Audience: Academic Format: Magazine/Journal Subject: Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Marine Fisheries Service ISSN: 0090-0656
Issue: Date: Jan, 2012 Source Volume: 110 Source Issue: 1
Product: Product Code: 0910000 Fishing NAICS Code: 11411 Fishing
Organization: Government Agency: United States. National Marine Fisheries Service
Geographic: Geographic Scope: Gulf of Mexico; Louisiana; Texas Geographic Code: 0GULF Gulf of Mexico; 1U7LA Louisiana; 1U7TX Texas
Accession Number: 281789626
Full Text: Abstract--Little is known about the seasonality and distribution of grouper larvae (Serranidae: Epinephelini) in the Gulf of Mexico and Atlantic Ocean off the coast of the southeast United States. Grouper larvae were collected from a transect across the Straits of Florida in 2003 and 2004 and during the Southeast Area Monitoring and Assessment Program spring and fall surveys from 1982 through 2005. Analysis of these larval data provided information on location and timing of spawning, larval distribution patterns, and interannual occurrence for a group of species not easily studied as adults. Our analyses indicated that shelf-edge habitat is important for spawning of many species of grouper--some species for which data were not previously available. Spawning for some species may occur year-round, but two peak seasons are evident: late winter and late summer through early fall. Interannual variability in the use of three important subregions by species or groups of species was partially explained by environmental factors (surface temperature, surface salinity, and water depth). A shift in species dominance over the last three decades from spring-spawned species (most of the commercial species) to fall-spawned species also was documented. The results of these analyses expand our understanding of the basic distribution and spawning patterns of northwest Atlantic grouper species and indicate a need for further examination of the changing population structure of individual species and species dominance in the region.


Adult grouper (Serranidae: Epinephelini) are commercially and recreationally important species that are highly susceptible to overfishing (Coleman et al., 1996), largely due to their spawning behavior and slow growth (Manooch, 1987; Shapiro, 1987; Coleman et al., 1996). Many species of groupers aggregate at consistent locations and time of year for spawning (Nemeth et al., 2007; Starr et al., 2007), and these aggregations are often targeted by fishermen (Burton et al., 2005). Fishing pressure on adult grouper and changes to habitat at all life-history stages of grouper have made evident the need for more effective fisheries management strategies. Most research on Gulf of Mexico grouper focuses on single species (e.g., Brule et al., 1999, 2003), over a very limited area (e.g., single spawning aggregations: Nemeth, 2005; off the coast of a single state or county: Coleman et al., 1996), or over short temporal durations (e.g., Eggleston, 1995).

Plankton surveys provide a reliable source of fishery-independent data for fishery management purposes and grouper larvae are routinely collected in these surveys (Houde, 1982; Marancik et al., 2005; Hernandez et al., 2010). Ichthyoplankton surveys provide data on seasonal (Hernandez et al., 2010), spatial (Ditty et al., 2004), and environmental characteristics associated with spawning (Richardson et al., 2009), all of which are particularly useful for species that are rare, elusive, or endangered as adults. For example, data on abundance and habitat use for early life stages have been directly integrated into fisheries management of blue-fin tuna (Thunnus thynnus) through stock assessment calculations (Scott et al., 1993). Spatial and temporal distribution and frequency of collection of larvae reflect changes in the juvenile and adult population structure (Richardson et al., 2010), which, coupled with climate models, may provide a means of forecasting the abundance and distribution of future populations (Hare et al., 2010).

Recent examination of larval grouper morphological characters from the most comprehensive collections available in the U.S. southeast region resulted in more precise taxon identification than had been previously attainable (Marancik et al., 2010). With these newly identified larvae, our purpose here is to describe the spatial and seasonal distribution patterns of 15 species (whose larvae could be identified) and four multispecies groups (whose larvae could not be identified to species but which share similar physical attributes). Specifically, our objectives were to describe 1) the spawning season; 2) locations of spawning; 3) environmental factors associated with larval grouper habitat; and 4) decadal-scale variability in the distribution and habitat use of grouper larvae. Our work is focused on grouper larvae from the Straits of Florida and the northern Gulf of Mexico.


Materials and methods


Samples were collected as part of two separate sampling programs: one across the Straits of Florida and one in the northern Gulf of Mexico.

Straits of Florida A 17-station transect crossing the Straits of Florida at 25.5[degrees]N was sampled as part of a larval billfish (Istiophoridae and Xiphiidae) project conducted by researchers at the University of Miami, Rosenstiel School of Marine and Atmospheric Science. Samples were collected at the beginning of each month from January 2003 through December 2004 (Fig. 1A). The transect extended from the Florida shelf break to the Great Bahama Bank. The three easternmost and three westernmost stations were approximately 2 km apart; the remaining stations were approximately 5.5 km apart. Samples were collected with an asymmetrical MOCNESS (multiple opening-closing net and environmental sensing system) consisting of a 4-[m.sup.2] frame with 1000-[micro]m mesh nets and a 1-[m.sup.2] frame with 150-[micro]m mesh nets (Guigand et al., 2005). The MOCNESS sampled in 25-m depth bins from 0-50 m at the westernmost station or 0-100 m at deeper stations. Surface waters (0-0.5 m) were sampled with a combined neuston net composed of a 1x2 m mouth with 1000-[micro]m mesh net and a 1x0.5-m mouth with 150-[micro]m mesh net. Samples were collected between sunrise and sunset, and the entire transect was generally sampled within a 48-hour period. At least 16 of the 17 stations were successfully sampled on all but three cruises; weather limited sampling in December 2003, January 2004, and November 2004. Samples were immediately preserved in 95% ethanol and, after 2-5 days, were transferred to 70% ethanol for long-term storage. Llopiz and Cowen (2008) and Richardson et al. (2010) provide further details of the Straits of Florida sampling survey.

In the laboratory, all larval fish were removed from all neuston samples, samples collected in 2003 with both the l-[m.sup.2] and 4-[m.sup.2] MOCNESS, and samples collected in 2004 from only the 4-[m.sup.2] MOCNESS. Genetic sequencing of the cytochrome oxidase subunit I gene (as in Richardson et al., 2007) was used to identify a subset (approximately 40%) of the Straits of Florida grouper larvae to species (Marancik et al., 2010). The remaining larvae were either identified to species or grouped with morphologically similar species according to physical attributes (Marancik et al., 2010). Body length and developmental stage were recorded for each fish. Developmental stage refers to the upward (dorsal) flexion of the notochord tip (urostyle) concurrent with caudal fin base and principal ray formation (Moser, 1996): the preflexion stage occurs when the notochord is straight; the flexion stage occurs when the notochord is obviously flexed and caudal rays are forming; and the postflexion stage occurs when the notochord tip is aligned vertically with the caudal base plate (hypural) elements. Owing to a single grouper larva collected in neuston samples (1 individual in 383 neuston stations), only MOCNESS samples were used in analyses.

Gulf of Mexico Grouper larvae were collected from the Southeast Area Monitoring and Assessment Program (SEAMAP) resource surveys conducted in the United States territorial waters of the Gulf of Mexico by the National Marine Fisheries Service (NMFS) Southeast Fisheries Science Center. All SEAMAP plankton samples included in our analyses were collected from 1982 through 2005 with either a bongo net consisting of a 61-cm frame and 335-[micro]m mesh nets towed obliquely from 2-5 m off the bottom or to a maximum depth of 200 m, or with a neuston net with 1x2 m frame and a 950-[micro]m mesh net towed at the surface. Samples were collected throughout the day and night depending on when the ship reached each station. Environmental data consistently collected over the entire SEAMAP time series were surface temperature, surface salinity, and water depth and therefore these were the only environmental variables considered in analyses. Plankton samples were initially fixed in either 5-10% unbuffered formalin (the majority of samples) or 95% ethanol. Formalin-fixed samples were transferred to 95% ethanol after 48 hours, and samples initially fixed in ethanol were transferred to fresh 95% ethanol after 24 to 36 hours. All fish larvae were removed from samples, identified to the lowest taxonomic level possible, and measured at the Sea Fisheries Institute, Plankton Sorting and Identification Center in Szczecin, Poland. Grouper larvae were further identified on the basis of morphological characters (Marancik et al., 2010).

Plankton collections were made in all months of the year during the 23 years of SEAMAP surveys included in our analyses. The greatest effort was conducted in May (2419 neuston and 1529 bongo samples) and September (2167 neuston and 1904 bongo samples); the least effort occurred in February (40 neuston and 41 bongo samples) and March (50 neuston and 178 bongo samples; Table 1). The most complete sampling coverage of the continental shelf of the northern Gulf of Mexico began in 1986 and continues to the present. Unfortunately, the months of November through March, likely the peak spawning season for many grouper species (Hood and Schlieder, 1992; Coleman et al., 1996; Nemeth et al., 2007), were rarely and inconsistently sampled during SEAMAP. Grouper larvae have been re-examined and identified from collections through 2005; therefore only data from SEAMAP surveys from 1986 through 2005 were statistically analyzed.

The most temporally and spatially consistent sampling effort was conducted during two dedicated SEAMAP plankton surveys: the spring and fall surveys (Fig. 1B). Within these two annual surveys, sampling coverage was fairly consistent from 1986 through 2005. The percentage of stations sampled gulf-wide, roughly representing the area covered, ranged from 28.7% to 54.0% (mean=45.1%) in the spring and from 26.1% to 76.7% (mean=61.3%) in the fall, and the targeted survey area was usually represented over its entire north-south and east-west extent (Table 2; Lyczkowski-Shultz and Hanisko, 2007; Muhling et al., 2010). The most consistent sampling occurred in April-May and September-October except for three years during which sampling began late (spring 2003, spring 2004, fall 2005) and one year which finished early (fall 1997).

The spring and fall surveys targeted different bathymetric zones with overlap at the shelf edge. During the spring plankton survey, conducted in April and May (1982-present), stations were sampled from the shelf edge to the United States Exclusive Economic Zone (EEZ) within a 0.5[degrees] x 0.5[degrees] (56-km) grid. The second dedicated plankton survey, called the "fall plankton survey," was conducted from late-August through October (1986-present) from the coast to the continental shelf edge (10-200 m water depth) and from south Texas to south Florida. Additional specimens and data came from plankton sampling conducted by the National Marine Fisheries Service (NMFS) Southeast Fisheries Science Center during SEAMAP summer and fall trawl surveys, winter plankton surveys, squid-butterfish surveys, Alabama summer and fall plankton surveys, and the fall pelagic fish survey in the Gulf of Mexico (Table 3; see Lyczkowski-Shultz and Hanisko, 2007, for details).


Seasonal and spatial occurrence The spatial consistency and monthly frequency of sampling in the Straits of Florida makes these data the best suited for determining the seasonality of larval grouper occurrence and, in turn, presumed seasonality of spawning. Only specimens identified to species were used in analyses. We used quotient analysis to define potential and peak season of occurrence and cross-transect distribution, using the Straits of Florida data. With this analysis, the ratio of the proportion of larval occurrence to the proportion of observations was determined within environmental (spatial or temporal) bins in order to discover when or where larvae were collected with higher (or lower) frequency than would be expected if larvae were evenly distributed. Quotient values >1 indicate a relatively higher occurrence of larvae (based on the number of observations) than expected, whereas values <1 indicate lower than expected occurrence (van der Lingen et al., 2001). Significance of the quotient values (above or below the null of 1) was determined by a bootstrapping technique similar to that used in Bernal et al. (2007). Quotient analysis is relatively robust for data sets containing many zero values, allowing analysis of the complete data set and cross-transect relationships despite the rarity of grouper larvae in collections. Analyses were conducted by using functions written for MATLAB (for Mac, vers. R2010a; The MathWorks Inc., Natick, MA).

Before formal analyses of larval grouper distributions, steps were taken to control for inconsistencies in sampling effort over the long time-scale of SEAMAP sampling. Each station sampled during SEAMAP was assigned to a cell within a 0.5[degrees] x 0.5[degrees] resolution grid encompassing the northern Gulf of Mexico (23-30[degrees]N latitude, and 81-98[degrees]W longitude; Fig. 1B). If more than one station was sampled within a grid cell during a single month of any year, the mean value of each environmental variable was taken. This procedure provided a sampling regime that was consistent over time and facilitated comparisons between environmental and larval fish data. Owing to the uneven spatial sampling effort among seasons and the low total abundance of grouper in Gulf of Mexico samples, 1) larvae were standardized to presence or absence within each grid cell for each month of each year sampled, 2) no size-specific analyses were conducted, 3) larvae collected from bongo and neuston samples were combined, and 4) statistical analyses were limited to samples collected during spring (April-May) and fall (September-October) from 1986 through 2005.

Influence of environmental factors and change over time Interannual variability in Gulf of Mexico regional larval grouper habitat use was examined by using generalized additive models (GAMs), a regression technique used to fit nonlinear relationships. Seasonal mean surface temperature, mean surface salinity, mean water depth, and year for subregions of the Gulf of Mexico were modeled to predict interannual variability in percent frequency of occurrence (%FO; Hastie and Tibshirani, 1990; Wood, 2006). The northern Gulf of Mexico (north of 23[degrees]N) was divided into subregions (labeled a-e in Fig. 2) that reflected the presence of grouper larvae and orientation of the coastline in relation to bathymetry. Within each subregion, %FO was calculated as the number of grid cells in which any grouper were present divided by the number of grid cells sampled during spring (April-May; 1986-2005) or fall (September-October; 1986-2005) surveys. GAMs are most effective for data sets with few zeros (years sampled, but no grouper collected); therefore GAMs were generated only for subregions and seasons (i.e., spring or fall) during which grouper were collected in at least 60% of the years being analyzed. Models of data collected during spring surveys were limited to depths <900 in to reduce the number of grid cells included in analyses owing to the near absence of grouper larvae at depths >900 m. With these restrictions, only 3 of the 5 subregions (Fig. 2, subregions b-d) contained enough data on which to base a model. Data from both bongo and neuston net samples were combined in order to include as many larval grouper data as possible. GAMs generated for bongo data provided similar, but weaker, results; therefore the combined data are presented. The full model used to explain %FO within subregion (r) and season (s) was the following:

[y.sub.r, s] = [a.sub.r,s] + [g.sub.1]([year.sub.r,s]) + [g.sub.2]([stemp.sub.r,s] + [g.sub.3]([ssal.sub.r,s]) + [g.sub.4]([wdep.sub.r,s]) + [e.sub.r,s],


a = the subregion by season intercept;

g = the nonparametric smoothing function for each term;

stemp, ssal, and wdep = the mean surface temperature, mean sur face salinity, and mean water depth for each subregion by season for each year, respectively; and

e = a normally distributed random error term with a mean of zero and finite variance.


The model was run with all combinations of covariates to find the best subset of covariates (best fit) required to explain %FO for each subregion by season. Two evaluation techniques were used to select the best model. The generalized cross-validation (GCV) score is a measure of the predictive squared error of the model (Wood, 2006). Akaike's information criterion with a low-sample-size bias-correction term (AICc; Burnham and Anderson, 2002) evaluates the trade-off between the number of covariates in a model and the likelihood of the model accurately predicting new data (Akaike, 1973)--therefore reducing the chances of a model with redundant covariates appearing to better explain the data. The best model was indicated by the lowest value of each evaluation score, and in all cases, both techniques yielded the same results (data not shown). AICc scores were also used to calculate a relative likelihood of each model being the best model (Burnham and Anderson, 2002). GAMs were created with the MGCV library (vers. 1.6-1) in R software (for Mac, vers. 2.11.0; R Development Core Team, 2008).


Grouper larvae were generally collected in low numbers during both the fine-scale sampling in the Straits of Florida and the broad-scale sampling in the Gulf of Mexico. A total of 665 individuals (521 individuals identified to species) were collected in 384 stations (both MOCNESS frame sizes and all depths combined) from the Straits of Florida. A total of 544 individuals were collected in 16,950 samples from the Gulf of Mexico (433 individuals in 7848 bongo samples; 111 individuals in 9102 neuston net samples).

Seasonal occurrence

Grouper larvae were collected during all months of sampling in the Straits of Florida (Table 4) and in all months except March and December in the Gulf of Mexico (Table 1). Most Straits of Florida larvae, specifically preflexion larvae whose presence indicate recent spawning, occurred during February through May. A second, less diverse and less numerous group of larvae was present from July through October (Table 4). The high apparent abundance of larvae in February was due to a single collection of >150 specimens of preflexion Epinephelus guttatus (red hind) at one station. The lowest occurrence and species richness (number of species captured) of larvae were observed during the months of January, July, August, and December.

Spatial occurrence

Straits of Florida Larvae were distributed in two distinct assemblages across the Straits of Florida: an eastern assemblage and a western assemblage (Fig. 3). Five species occurred significantly more frequently within the eastern 10 km of the transect (Fig. 3, A-E). For most of these species, the pattern was the same for all developmental stages. Cephalopholis cruentatus (graysby), one of the more abundant species, was collected across the transect across the straits, but was collected most frequently on the eastern side at the preflexion stage, whereas flexion and postflexion stage larvae were collected across the transect, occurring at no stations significantly more or less frequently (Fig. 3, F-G). Four species were collected significantly more frequently on the western side of the transect (Fig. 3, H-K). The remaining six species were not collected at high enough frequencies to analyze statistically (<5 specimens) or were collected evenly across the transect (Paranthias furcifer, Fig. 3L).

Gulf of Mexico Distribution patterns of grouper larvae of all sizes were categorized into five subregions of occurrence in the northern Gulf of Mexico (Fig. 4). Small (1.3-4.3 mm NL) preflexion larvae without prominent dorsal and pelvic spines are indicative of recent spawning and were collected in 18 of 23 years of SEAMAP surveys. Repeated occurrence of these earliest stage larvae gave evidence of three of the subregions as areas of spawning activity: the Texas-Louisiana Shelf west of the Mississippi River (TX-LA; north of 27.5[degrees]N and west of 90[degrees]W; Fig. 2 subregion b), the north-central Gulf shelf off the coasts of Mississippi, Alabama, and northern Florida (MS-AL-nFL; north of 27.5[degrees]N and between 90[degrees] and 85[degrees]W; Fig. 2 subregion c), and the west Florida shelf (wFL; north of 23[degrees] N and between 85-81[degrees]W; Fig. 2 subregion d). These three subregions accounted for the vast majority of grouper larvae collected (n=314) and were the only subregions containing early-stage larvae. Later-stage larvae were also collected farther offshore in two additional subregions (Fig. 4, A-C and F). Sampling was conducted off the coast of the Yucatan Peninsula in the southern Gulf of Mexico during January and February 1990. Although grouper larvae were collected (n=14), the data were not included in our analyses because of the timing (winter) and infrequency (a single year) of sampling in the area.

Graysby were the most abundant group of larvae collected in the Gulf of Mexico that could be identified to species. Graysby larvae occurred during both spring and fall surveys. Most specimens were collected during July-October and were distributed primarily along the west Florida shelf (n=35). A few larvae were collected on or near the Louisiana shelf and Mississippi-Alabama-north Florida shelf during the fall survey (n=2) and in deep offshore waters off southwestern Florida during the spring survey (n=5; Fig. 4A).

Small Mycteroperca spp. larvae (i.e., specimens with dorsal-ventral tail pigment; Table 1) were collected during April-June and September and November in all three presumptive spawning subregions of the northern Gulf identified in this study (Fig. 4D; spring: all three, fall: TX-LA, MS-AL-nFL). These specimens were primarily collected along the shelf break. A similar spatial and temporal distribution pattern was observed for several slightly larger larvae identified as either E. itajara or Mycteroperca spp. based on the presence of pigment on the cleithral symphysis, standard tail pigment, and broad-based, long and curved spinelets (Marancik et al., 2010). These specimens also were collected during April-June and September-November along the shelf break of all three presumed spawning subregions (spring: all three, fall: TX-LA and wFL; Fig. 4E, Table 1). The largest Mycteroperca spp. specimens, identified by anal-fin ray counts >10 (Smith, 1971), were collected in the northern Gulf of Mexico only during April-June and primarily on the TX-LA shelf (Fig. 4F; Table 1). In addition, two larger Mycteroperca spp. larvae were collected in January and February off the Yucatan Peninsula in the southern Gulf of Mexico.


Like the Mycteroperca spp., members of two multispecies groups (larvae with small spinelets, and those with long, curved spinelets) were collected in April-June and September-November in all three identified Gulf of Mexico spawning subregions (Fig. 4, B-C). Specimens of the group of species with standard tail pigment and long and curved spinelets collected in the spring survey were mostly collected on and near the shelf break off the coasts of Texas, Louisiana, Mississippi, and Alabama (TX-LA and MS-AL-nFL). Specimens collected during the fall survey, however, occurred only on the wFL shelf (Fig. 4C). Members of this species group may include postflexion Epinephelus drummondhayi, E. itajara, Hyporthodus flavolimbatus, H. nigritus, H. niveatus, members of the Mycteroperca genus that lack cleithral symphysis pigment, or a combination of these species (Marancik et al., 2010).


Four species (C. fulva, H. mystacinus, Gonioplectrus hispanus, and Paranthias furcifer) and a two species complex (either E. striatus or M. venenosa) also were collected in SEAMAP survey samples, but in very low numbers (Table 1). These larvae occurred on the TX-LA shelf and offshore of the wFL shelf. There were too few larvae to define seasonal patterns.

Influence of environmental factors

The generalized additive models used to evaluate the influence of select physical variables measured during SEAMAP plankton surveys in the Gulf of Mexico did reasonably well in predicting presence or absence of grouper in a subregion for a year under a given set of environmental conditions. The percent deviance from the null model explained by the best of these models ranged from 14.3% to 94.5%. The TX-LA shelf models examined explained very little of the deviance in the data, and several models fit the data almost equally (low AICc weights; Table 5). Thus, grouper occurrence in this subregion is not well explained by any combination of surface temperature, surface salinity, water depth, or year. The west Florida shelf model based on the fall survey data and the Mississippi-Alabama-north Florida shelf model based on the spring survey data were the most successful in predicting the occurrence of grouper larvae, describing 94.5% and 84% of the deviances, respectively. The significant covariates in each subregion by season GAM revealed changes in frequency of occurrence over time and regionally specific influences of water depth, surface salinity, and surface temperature (Table 5). Annual frequencies of grouper collections were sufficient for generating GAMs for the three subregions characterized by the presence of the smallest larvae for the fall season (Fig. 2, subregions b-d). The only spring data set with larvae collected in enough years to warrant modeling was the MS-AL-nFL shelf subregion. Models of Gulf subregions east of 90[degrees] W longitude (wFL shelf and MS-AL-nFL shelf) were positively correlated with year, with higher occurrence since the early to mid 1990s (Fig. 5). The west Florida shelf model was also significantly influenced by mean surface temperature (>29[degrees]C), mean surface salinity (>35.5), and water depth (>129 m) (Table 5, Fig. 5). The occurrence of grouper larvae in the gulf west of 90[degrees] W longitude (TX-LA shelf) was significantly influenced by mean surface temperature (>28[degrees]C; Table 5, Fig. 5), although this relationship was weak. The occurrence of grouper larvae in the north central Gulf (MS-AL-nFL) increased from 1990 to 2000, but was highest after 1995, in midrange surface salinities (34-35), and in mean water depth <350 m (Table 5, Fig. 6).

Change in occurrence over time

The Gulf of Mexico subregion by season GAMs revealed a change in grouper occurrence over the SEAMAP survey time series, with %FO highest after the mid 1990s. This shift was evident in the patterns of occurrence of the more abundant grouper species and species groups (Fig. 7). Before 1995, grouper occurrences were higher in the spring than in the fall. Since 1995, higher occurrences have been observed in the fall than in the spring. No Mycteroperca spp. (three size groups combined) were collected in the fall before 1995, but since 1995, these larvae have occurred in fall survey samples. Similarly, larval graysby were rarely collected before 1995 (occurring in 2 of the 10 years between 1986 and 1995), but they have become more common in samples during recent decades (7 of the 10 years between 1996 and 2005) and are often collected in multiple months within a year. Graysby larvae have also become a significant percentage of the total catch of grouper larvae collected in the recent decade: 3-33% (mean=18.7%) before 1995; 5-100% (mean=40.3%) after 1995. A comparison of survey coverage for the two periods (1986-95, 1996-2005) revealed comparable sampling effort during spring and fall surveys. Compared with percent coverage during the period since 1995, the percent coverage during fall surveys before 1995 was similar or slightly higher, whereas in spring the percentages were similar or slightly lower before 1995. Therefore, differences in sampling effort did not likely cause the observed increase in fall-spawned grouper larvae in the years since 1995.




Seasonal occurrence

Larval grouper seasonality, as defined by the occurrence of larvae in collections from the Straits of Florida, relates directly to spawning season. Spawning likely occurs approximately one month (average pelagic larval duration <45 days; Colin et al., 1997; Lindemann et al., 2000; Fitzhugh et al., 2005) before occurrence of post-flexion-stage larvae, and within two weeks of the occurrence of preflexion-stage larvae (Glamuzina et al., 2000; Leu et al., 2005). Because larvae were generally collected at the beginning of each month during collections in the Straits of Florida, actual spawning could have occurred in the month before collection. Although larvae were collected year-round, most larvae were collected during early February and March (Table 4)--a period that would correspond with a January through March spawning season. This is generally considered the primary spawning season of most northwest Atlantic groupers (Collins et al., 1998; Johnson et al., 1998; Brule et al., 2003; Nemeth et al., 2007; Starr et al., 2007). A second period of high larval species richness was observed during early September and October, indicative of spawning from August to October (Table 4; Bullock et al., 1996; Sadovy and Eklund, 1999; Richards et al., 2005).

Analysis of larval seasonal occurrence indicated longer spawning seasons than those identified in studies of adult groupers. Graysby are considered fall spawners throughout their range (Richards et al., 2005), and most graysby larvae were collected during July-October in shallow shelf waters on the west Florida Shelf (mean depth of 49.2 m vs. >60 m for all other taxa). However, a few specimens were collected during April and May in deep offshore Gulf of Mexico waters (Fig. 4A). These larvae were morphologically identical to the larvae collected on the shelf; therefore misidentification is unlikely. Unlike the fall-spawned graysby, the spring-spawned graysby were collected in neuston nets (surface <0.5 m) and at stations with water temperatures warmer than surrounding stations (data not shown), indicating an association with Loop Current water that is transported north from the Caribbean Sea into the eastern Gulf of Mexico. These specimens may have been spawned locally and entrained in a Loop Current eddy or may have originated south of the study area (Campeche Bank or Caribbean Sea) and been carried north. Either way, these larvae represent an expanded spawning season (April-October) not previously recorded in the literature.


Similarly, spawning season determined through observation of adult red grouper in the Gulf of Mexico was limited to January-March (Johnson et al., 1998, Brule et al., 1999). A significant number of red grouper larvae from the Straits of Florida sampling were captured in May, indicating a spawning season extending from January to May. Burgos et al. (2007) collected spawning females from mid February to mid June in North and South Carolina--a period coinciding with the timing of our collection of larvae.

Spatial occurrence

Grouper larvae, in general, have a narrow distribution pattern regardless of water properties such as temperature and salinity. Grouper larvae were collected along the shelf break throughout much of the northern Gulf of Mexico from Texas to southern Florida. Similarly, most of the Straits of Florida larvae were collected from stations closest to the coasts of Florida and the Bahamas (Fig. 3). A similar affinity for shelf edge habitat has been observed among adult grouper (Koenig et al., 1996; Brule et al., 1999; Sadovy and Eklund, 1999; Brule et al., 2003), and most spawning occurs inshore of or along the shelf break (Collins et al., 1998; Brule et al., 2003; Nemeth et al., 2007). Further, a higher specimen-to-sample ratio was observed in the Straits of Florida (665 individuals in 384 MOCNESS stations)than that from the Gulf of Mexico (544 individuals in 16950 bongo and neuston stations). Sampling gear (MOCNESS vs. bongo), sampling strategy (discrete depth vs. oblique), and location of sampling all contributed to the wide differences in the numbers of grouper larvae collected during the two sampling programs. The MOCNESS sampled more water per tow than the bongo nets, and proportionately more of the sampling occurred at depths likely to contain grouper larvae (<50 m). In addition, more of the Straits of Florida (including the area upstream from the sampling area) includes shelf edge habitat than the basin-wide sampling area of the Gulf of Mexico. This was especially the case during the spring SEAMAP survey (season of highest grouper occurrence) when the target sampling area is deep offshore water within the Gulf of Mexico. Thus, a higher percentage of grouper habitat (subsurface waters over shelf edge) was sampled along the transect through the narrow Straits of Florida than in the broad SEAMAP survey area within the Gulf of Mexico and likely accounted for many of the differences in catch rates between the two sampling programs.

Analysis of the larval data supported the conclusion that most Gulf of Mexico grouper species depend on shelf-edge habitat for spawning. Juveniles of many of these species move inshore to coastal and estuarine nursery habitats (Eggleston, 1995; Ross and Moser, 1995; Lindemann et al., 2000; Fitzhugh et al., 2005). However in the Straits of Florida, flexion and post-flexion larval graysby were collected farther offshore than were preflexion larvae of the species (Fig. 3). At least two scenarios could explain this pattern in distribution. The offshore flexion and postflexion larvae collected in the straits could have been carried by the Florida Current into the sampling area from spawning sites as far away as the Gulf of Mexico or Caribbean Sea. Transport from upstream spawning locations explains the high diversity of grouper species collected in the area and is corroborated by genetic analysis of Gulf of Mexico and southeast United States populations (Zatcoff et al., 2004; Cushman et al., 2009). The fate of larvae carried away from coastal and estuarine habitat in the Loop-Florida-Gulf Stream currents is variable (Hare and Walsh, 2007; Richardson et al., 2009). Some individuals arrive at suitable habitat along the U.S. east coast far from spawning sites (e.g., bluefish [Pomatomus saltatrix]; Hare and Cowen, 1996), but many are carried too far north for survival (e.g., gray snapper [Lutjanus griseus]; Denit and Sponaugle, 2004) or never reach the coast (Hare and Walsh, 2007). Similarly, these later-stage larvae may have been advected offshore from nearby spawning sites and rely on regularly occurring oceanic events (e.g., gyres and meanders: Porch, 1998; frontal eddies: Sponaugle et al., 2005) or periodic events (e.g., wind storms: Shenker et al., 1993) to move them onshore toward nursery habitat. This second scenario would provide for some degree of self-recruitment. These scenarios may apply to other species of grouper; however, most species were collected too infrequently or in too narrow a size range to detect differences in distribution patterns between early life history stages. Further research is needed to determine the most likely processes driving the distribution patterns observed among Straits of Florida

grouper larvae. The results of such an analysis, the identification of recruitment pathways and survival rates, would have major implications for the management of populations spawning in the area.

Specimens identified as either E. itajara or Mycteroperca spp. were collected during spring (majority) and fall surveys (Fig. 4E). The fall contingent was collected on the southwest Florida and Louisiana shelves and represents evidence of fall-spawning Mycteroperca spp. or a previously undocumented spawning location for E. itajara. Most species of Mycteroperca are known to spawn in the winter and spring months in the Gulf of Mexico and Caribbean (Hood and Schlieder, 1992; Bullock and Murphy, 1994; Brule et al., 2003; Fitzhugh et al., 2005), and there were no large Mycteroperca spp. larvae collected in the fall survey to confirm a fall spawning population (Fig. 4F). However, the spawning seasons of many species of Mycteroperca are unknown, and at least one species (M. bonaci) is believed to spawn year-round (Brule et al., 2003), and therefore fall-spawned Mycteroperca spp. are possible. E. itajara are known to spawn in fall (Sadovy and Eklund, 1999). Although they are believed to occur throughout the coastal Gulf of Mexico (Heemstra and Randall, 1993), no E. itajara spawning sites have been recorded in the northwestern Gulf of Mexico (Sadovy and Eklund, 1999). These specimens could indicate an undocumented spawning site for E. itajara in the northwestern Gulf of Mexico, but targeted sampling in the area and molecular identification of larvae would be needed to verify and locate a new spawning site. Genetic confirmation of a northwest Gulf of Mexico population may be possible because Brazilian, Belizian, and Florida populations of E. itajara are genetically highly separated (Craig et al., 2009).

Influence of environmental factors

Interannual variability in the occurrence of grouper larvae was influenced by hydrography. The variables involved and the extent of that involvement varied by subregion and season (Figs. 5 and 6). Surface temperature and salinity were significant factors in the fall west Florida shelf model, which together with year and water depth, explained over 90% of the deviance in the data. Surface salinity was also significant in the Spring MS--AL--nFL subregion model and, along with year and water depth, explained over 80% of the deviance. These two models describe the importance of shelf-edge habitat. Low occurrence of grouper larvae in SEAMAP collections made it difficult to analyze fine spatial (within subregion) or temporal (within year) scale interactions with environment. Targeted sampling within subregions would be needed to better describe the relationship between the physical environment and larval occurrence.

Change in occurrence over time

The data presented here represent the best existing data set for examining long-term trends of larval grouper abundance in the southeast United States. We attempted to control for inconsistencies in sampling, but the results from this study cannot be fully separated from sampling bias, consistently low catches, nonspecies-level identifications, and missed peak spawning season for many commercially relevant species. However, our results provide evidence of a shift in grouper species composition toward fall-spawning populations over the SEAMAP time frame (Figs. 5-7). Spring-spawned larvae dominated collections before 1995, but in the more recent decade, fall-spawned larvae have come to dominate or have gone from nonexistent to present in larval collections. The relative increase in occurrence of fall-spawned larvae was best illustrated by the rapid rise in the number of larval graysby collected. In addition, a clear increase in the collection of fall-spawned members of a morphologically indistinguishable group of species (with small spinelets and standard tail pigment), including several commercially important species (namely, small H. flavolimbatus [<4.5 mm BL], E. itajara, H. niveatus, and possibly preflexion Mycteroperca spp. lacking pigment at the cleithral symphysis), was also observed (Fig. 7).

A shift in larval occurrence could result from a shift in abundance at the adult population level (e.g., changes in population size or spawning stock biomass), changes in the survivability of larvae (e.g., changes to maternal condition, fecundity, food availability, environmental regime, etc.), or a change in distribution. There is some evidence of changes in adult grouper population dynamics. For example, graysby larvae were one of the most abundant grouper species in our Straits of Florida collections and have become common in SEAMAP collections since 1995. Similarly, the occurrence of adult graysby increased off the coast of North Carolina between 1975 and 1992 (Parker and Dixon, 1998). Similar data on the abundance of adult graysby from the Florida Shelf is limited, but adult graysby are one of only three species of grouper that were not being overfished in the Florida Keys before 1996 (Ault et al., 1998) and were a dominant species on Florida Keys reefs in the early 1990s (Sluka et al., 1998). In addition, a decline in the abundance of larger grouper since the early 1990s (Bohnsack et al., 1994) could result in an increase in the abundance of smaller grouper species, like graysby (Sluka et al., 1998; Chiappone et al., 2000). However, increases in larval occurrence could also be the result of a shift in adult habitat use without an increase in population size. In the southern Caribbean, a significant shift in graysby distribution to deeper habitat coinciding with a reduction in coral cover has been observed (Nagelkerken et al., 2005). A similar shift in adult distribution on the west Florida shelf could explain the increase in larval occurrence observed in our study. Further examination of the potential causes of a shift in species dominance at the adult level and additional targeted investigations into larval survivability are needed to corroborate our findings of a shift in dominance in the northern Gulf of Mexico. However, the larval data here indicate that shifts in grouper abundance and species composition occurred over the last three decades.


Analysis of larval grouper distribution patterns provided a means of independently corroborating location and seasonality of spawning, but also allowed us to identify new patterns in grouper distribution and species composition in the Straits of Florida and northern Gulf of Mexico. The timing of larval occurrence, and thus the timing of spawning, for most species fell into one of two seasons, confirming what was already documented on spawning season for many species. However, two species, Cephalopholis cruentatus (graysby) and Epinephelus morio (red grouper), were collected during longer seasons than previously reported. Grouper larvae were collected in three distinct subregions of the Gulf of Mexico and along the shelf edge in both the gulf and Straits of Florida. Analysis of larval occurrence by sub-regional mean water depth, surface temperature, and surface salinity further corroborated the importance of shelf-edge habitat, particularly on the west Florida shelf in fall and the Mississippi-Alabama-north Florida shelf in spring. The species composition of grouper larvae in the Gulf of Mexico may have changed over the course of SEAMAP sampling. The frequency of occurrence of fall-spawned species has increased in relation to spring-spawned species since 1995. In the Straits of Florida, preflexion graysby were collected along the shelf edge, but flexion and postflexion larvae of the species were collected farther offshore. The distribution of later-stage graysby larvae could be evidence of processes directing self-recruitment or loss to the population. These data provided a first-time look at larval grouper distribution patterns over a large spatial and time scale and provided evidence of several topics needing further research.


We would like to thank the following people for their significant contributions to this research: L. Bulloc, J. Llopiz, C. Guigand, A. Exum, J. VanWye, K. Shulzitski, K. Williams, The SEAMAP Plankton Team, and the staff at the Sea Fisheries Institute, Plankton Sorting and Identification Center. This research would not have been possible without the resourcefulness and skilled assistance of the crews of the NOAA research vessels Chapman, Oregon II and Gordon Gunter and the dedication of biologists and volunteers who participated in SEAMAP plankton surveys sampling. N. Bachelor and J. Hare provided statistical expertise. This project was funded through the OAR Cooperative Institute Program Office and is part of the research program of the Northern Gulf Institute, a NOAA Cooperative Institute. Funding for the Florida Straits sampling was provided by grants from the National Science Foundation (OCE-0136132) and the Gulf States Marine Fisheries Commission (Billfish-2005-017).

Manuscript submitted 28 March 2011.

Manuscript accepted 16 August 2011.

Fish. Bull. 110:1-20(2012).

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Katrin E. Marancik (contact author) (1,2,3)

David E. Richardson (1)

Joanne Lyczkowski-Shultz (2)

Robert K. Cowen (4)

Malgorzata Konieczna (5)

Email address for contact author:

(1) Narragansett Laboratory Northeast Fisheries Science Center National Marine Fisheries Service, NOAA 28 Tarzwell Drive Narragansett, Rhode Island 02882

(2) Mississippi Laboratory Southeast Fisheries Science Center National Marine Fisheries Service, NOAA 3209 Frederic Street Pascagoula, Mississippi 39567

(3) IAP World Services, Inc. 3209 Frederic Street Pascagoula, Mississippi 39567

(4) Rosenstiel School of Marine and Atmospheric Science University of Miami 4600 Rickenbacker Causeway Miami, Florida 33149

(5) Sea Fisheries Institute Plankton Sorting and Identification Center u1, Kazimierza Krolewicza 4-E 71-550 Szczecin, Poland
Table 1
Percent frequency of occurrence (%FO) of total larvae and
number of total larvae and preflexion larvae collected, size
range, and monthly occurrence of specimens of each grouper
species or species group collected during Southeast Area
Monitoring and Assessment Program (SEAMAP) surveys from 1982
through 2005 (Marancik et al., 2010). The "*" symbol
denotes the total seasonal occurrence of any larvae; the "+"
symbol denotes presence of preflexion larvae collected.
Species complexes are listed as subdivisions of the
species-groups (small spinelets+standard pigment, and long
curved spinelets+standard pigment) were included with the
species group in analyses (e.g., 50 individuals were
included in the long curved spinelets+standard pigment

                                 %FO                          n

Species or group            Bongo   Neuston   Total   Preflexion

Cephalopholis cruentata      0.29      0.09      44           27
Cephalopholis fulva          0.01      0.02       3            1
Gonioplectrus hispanus       0.03      0.03       5
Hyporthodus mystacinus       0.01      0.01       2
Paranthias furcifer          0.06      0.01      12
Epinephelus striatus/
  Mycteroperca venenosa      0.01      0.02       3            3
Small epinephelini +         1.02      0.04     162          162
  standard pigment
Small spinelets +             0.9      0.41     199          121
  standard pigment
Epinephelus adscensionis/    0.01      0.01       2
E. morioldrummondhayi/       0.01      0.01       2
A. aferlE. adscensionis/     0.06      0.00       5
  D. inermis
Long curved spinelets        0.24      0.05      26            4
  + standard pigment
E. itajaralHyporthodus       0.15      0.01      24
Mycteroperca spp.
Small: Dorsal-
  ventral tail pigment       0.13      0.02      12           11
Medium: E. itajara/
  Mycteroperca               0.11      0.07      15            4
Large: Mycteroperca spp.     0.14      0.05      19
Long straight spinlelets     0.04      0.00       3            1
Specimens with
  broken spines              0.04      0.02       6            4
Total number of
  larvae collected
in bongos (neuston)                             544
% FO of larvae
  collected in bongo
  (neuston)                  3.29      0.89
Total number of
  plankton samples
collected: bongo                               7848
Neuston                                        9102

                                         Month collected
Species or group            range (mm)    Jan        Feb      Mar

Cephalopholis cruentata      2.2-6.4
Cephalopholis fulva          4.2-4.8
Gonioplectrus hispanus       2.9-10.6
Hyporthodus mystacinus       5.3-6.0
Paranthias furcifer          4.7-10.9
Epinephelus striatus/
  Mycteroperca venenosa      2.3-2.6
Small epinephelini +         1.2-4.8       +          +
  standard pigment
Small spinelets +            2.2-6.5                  +
  standard pigment
Epinephelus adscensionis/    6.6-8.0
E. morioldrummondhayi/       5.5-6.5
A. aferlE. adscensionis/     6.2-8.1       *
  D. inermis
Long curved spinelets        3.0-5.6
  + standard pigment
E. itajaralHyporthodus       4.9-24.3
Mycteroperca spp.
Small: Dorsal-
  ventral tail pigment       2.0-4.7
Medium: E. itajara/
  Mycteroperca               2.7-10.1                 *
Large: Mycteroperca spp.     5.5-19.5      *          *
Long straight spinlelets     3.3-4.4                  +
Specimens with
  broken spines              2.6-5.0
Total number of
  larvae collected
in bongos (neuston)                       5(0)      6(2)      0(0)
% FO of larvae
  collected in bongo
  (neuston)                              3.8(0)   12.2(5.0)   0(0)
Total number of
  plankton samples
collected: bongo                          133        41       178
Neuston                                   162        40        50

                                        Month collected

Species or group              Apr        May       Jun      Jul

Cephalopholis cruentata        +          +         *        *
Cephalopholis fulva            *          *
Gonioplectrus hispanus
Hyporthodus mystacinus                    *
Paranthias furcifer            *          *
Epinephelus striatus/
  Mycteroperca venenosa
Small epinephelini +           +          +         +        +
  standard pigment
Small spinelets +              +          +         +
  standard pigment
Epinephelus adscensionis/                 *
E. morioldrummondhayi/                    *
A. aferlE. adscensionis/       *          *
  D. inermis
Long curved spinelets          +          +
  + standard pigment
E. itajaralHyporthodus                    *
Mycteroperca spp.
Small: Dorsal-
  ventral tail pigment         +          +         +
Medium: E. itajara/
  Mycteroperca                 +          +         *
Large: Mycteroperca spp.       *          *         *
Long straight spinlelets                  *
Specimens with
  broken spines                           +
Total number of
  larvae collected
in bongos (neuston)          20(13)    160(44)     6(1)     3(0)
% FO of larvae
  collected in bongo
  (neuston)                 2.8(1.2)   5.2(1.4)   0.841)   0.4(0)
Total number of
  plankton samples
collected: bongo              639        1529      767      671
Neuston                       978        2419      835      635
                            Month collected

Species or group             Aug       Sep       Oct       Nov

Cephalopholis cruentata       +         +         +
Cephalopholis fulva                     +
Gonioplectrus hispanus        *         *
Hyporthodus mystacinus                            *
Paranthias furcifer                     *
Epinephelus striatus/
  Mycteroperca venenosa                 *         *
Small epinephelini +                    +         +         +
  standard pigment
Small spinelets +                       +         +         +
  standard pigment
Epinephelus adscensionis/
E. morioldrummondhayi/
A. aferlE. adscensionis/
  D. inermis
Long curved spinelets                   *         *
  + standard pigment
E. itajaralHyporthodus        *         *         *         *
Mycteroperca spp.
Small: Dorsal-
  ventral tail pigment                  +                   +
Medium: E. itajara/
  Mycteroperca                          *         +         +
Large: Mycteroperca spp.
Long straight spinlelets                *
Specimens with
  broken spines                         +
Total number of
  larvae collected
in bongos (neuston)          5(0)    147(31)    71(19)    10(1)
% FO of larvae
  collected in bongo
  (neuston)                 1.4(0)   4.449)    5.3(1.5)   1.542)
Total number of
  plankton samples
collected: bongo             360      1904       830       547
Neuston                      339      2167       795       482

Species or group            Dec

Cephalopholis cruentata
Cephalopholis fulva
Gonioplectrus hispanus
Hyporthodus mystacinus
Paranthias furcifer
Epinephelus striatus/
  Mycteroperca venenosa
Small epinephelini +
  standard pigment
Small spinelets +
  standard pigment
Epinephelus adscensionis/
E. morioldrummondhayi/
A. aferlE. adscensionis/
  D. inermis
Long curved spinelets
  + standard pigment
E. itajaralHyporthodus
Mycteroperca spp.
Small: Dorsal-
  ventral tail pigment
Medium: E. itajara/
Large: Mycteroperca spp.
Long straight spinlelets
Specimens with
  broken spines
Total number of
  larvae collected
in bongos (neuston)         0(0)
% FO of larvae
  collected in bongo
  (neuston)                 0(0)
Total number of
  plankton samples
collected: bongo            249
Neuston                     200

Table 2
Mean percent sampling coverage (% Coverage; number of grid
cells sampled-number of grid cells in subregionx100) and
range of latitudes and longitudes sampled in each Gulf of
Mexico subregion (a-e, see Fig. 2) during the spring or fall
Southeast Area Monitoring and Assessment Program (SEAMAP)
plankton surveys over the time intervals 1986-95 and 1996-

              a: Texas-Mexico shelf.
              to 90 deg. Longitude

                 %         Range       Range
Region        Coverage   latitude    longitude

  1986-1995     42.4     26.0-27.4   94.7-90.6
  1996-2005     54.8     26.0-27.5   95.9-90.7

  1986-1995     44.5     26.0-27.5   97.0-95.9
  1996-2005     66.5     26.0-27.5   97.0-92.8

              b: Texas-Louisiana shelf

                 %         Range       Range
Region        Coverage   latitude    longitude

  1986-1995     37.7     28.0-28.3   94.0-90.5
  1996-2005     50.0       28.0      95.9-90.5

  1986-1995     96.4     28.0-29.5   96.5-90.5
  1996-2005     86.0     28.0-29.5   96.5-90.5

              c: Mississippi-Alabama-
              north Florida shelf

                 17        Range       Range
Region        Coverage   latitude    longitude

  1986-1995     47.8     28.0-29.8   89.9-85.0
  1996-2005     47.1     28.0-29.9   90.0-85.1

  1986-1995     59.8     28.0-30.5   90.0-85.0
  1996-2005     58.0     28.1-30.4   90.0-85.1

              d: west Florida shelf

                 %%        Range       Range
Region        Coverage   latitude    longitude

  1986-1995     27.8     24.4-27.2   84.5-83.6
  1996-2005     22.0     24.1-26.0   84.5-83.6

  1986-1995     58.7     25.3-29.8   84.5-81.8
  1996-2005     45.7     25.7-29.6   84.5-82.2

              e: offshore southwest Florida
              to 90 deg. Longitude

                 %         Range       Range
Region        Coverage   latitude    longitude

  1986-1995     53.2     24.5-27.4   90.0-85.0
  1996-2005     58.7     24.5-27.5   90.0-85.0

  1986-1995     1.4        27.5        85.0
  1996-2005     5.7      26.0-27.5     85.0

Table 3
Gulf of Mexico plankton sampling data from 1982 through 2005
by month and Southeast Area Monitoring and Assessment
Program (SEAMAP) survey type showing the number and
occurrence (number of stations with grouper present, "Occ.
grouper") of grouper larvae in neuston, bongo, and
nonstandard sampling gear, and ranges in latitude and
longitude of the sampling surveys. WP=winter plankton
surveys, **=sampling outside of established SEAMAP surveys,
SP=spring plankton surveys, SQ=squid-butterfish surveys,
AS=Alabama summer plankton surveys, SG=summer groundfish
trawl surveys, FP=fall plankton surveys, AF=Alabama fall
plankton surveys, FG=fall groundfish trawl surveys, and
FS=fall pelagic fish surveys.


            Survey      No.      Occ.       No.
Month        type     grouper   grouper   samples

January       WP            0         0       162
February      **          na          0         0
February      WP            2         2        40
March         **            0         0        13
March         SP            0         0        37
April         **            0         0         5
April         SP           13        12       973
May           **            3         3        84
May           SP           40        30      2321
May           SQ            1         1        14
June          **            0         0        72
June          AS            0         0         4
June          SG            0         0       510
June          SP            1         1       249
July          **            0         0        21
July          SG            0         0       611
July          SQ            0         0         3
August        **            0         0        13
August        FP            0         0       258
August        SQ            0         0        68
September     AF            0         0       134
September     FP           31        19      2033
October       **            0         0        38
October       AF            0         0        18
October       FG            3         3       454
October       FP           16         9       276
October       FS            0         0         9
November      **            0         0        32
November      FG            1         1       436
November      FS            0         0        11
November      WP            0         0         3
December      FG            0         0         4
December      WP            0         0       196


              No.      Occ.       No.
Month       grouper   grouper   samples

January           5         5       133
February          0         0         5
February          6         5        36
March             0         0       130
March             0         0        48
April           na          0         0
April            20        18       639
May             na          0         0
May             160        80      1513
May               0         0        16
June              0         0        50
June              0         0         2
June              2         2       568
June              4         4       147
July              0         0        22
July              3         3       646
July              0         0         3
August            0         0        13
August            4         4       278
August            1         1        69
September         0         0         6
September       147        84      1898
October           2         2        41
October         na          0         0
October          20        15       488
October          44        23       290
October           5         4        11
November          1         1        32
November          7         5       504
November          2         2        11
November          0         0         3
December          0         0         7
December          0         0       242

             Non-standard gear        Latitude

              No.       No.
Month       grouper   samples    South     North

January           0         5     18.50     30.00
February        na          0     29.92     30.10
February          0         3     22.00     29.51
March           na          0     28.18     30.20
March           na          0     28.46     29.19
April           na          0     29.00     29.01
April           na          0     23.15     30.01
May             na          0     28.97     29.09
May               0        42     23.50     30.01
May             na          0     28.55     29.53
June            na          0     25.00     30.00
June            na          0     30.00     30.23
June            na          0     26.00     30.22
June            na          0     24.50     30.00
July            na          0     25.00     28.82
July            na          0     26.00     30.05
July            na          0     28.00     28.03
August          na          0     27.53     29.16
August          na          0     24.00     30.25
August          na          0     26.49     30.07
September       na          0     30.00     30.32
September       na          0     24.00     31.50
October         na          0     28.48     29.82
October         na          0     30.12     30.28
October         na          0     25.99     30.18
October         na          0     24.00     30.01
October         na          0     27.06     29.12
November        na          0     26.49     30.08
November        na          0     26.02     30.17
November        na          0     25.03     29.16
November        na          0     29.00     29.00
December        na          0     28.50     29.00
December          0         9     25.00     30.00


Month        West      East

January      -97.50    -87.00
February     -88.68    -88.40
February     -95.88    -87.83
March        -91.50    -86.50
March        -91.50    -89.48
April        -88.83    -88.83
April        -96.00    -83.20
May          -88.85    -88.14
May          -96.04    -82.00
May          -90.08    -87.93
June         -89.50    -83.00
June         -88.31    -87.50
June         -97.20    -86.00
June         -96.00    -83.50
July         -88.48    -82.00
July         -97.04    -87.00
July         -84.88    -84.21
August       -91.27    -87.63
August       -97.25    -82.00
August       -96.81    -85.03
September    -88.17    -87.97
September    -97.25    -79.67
October      -90.73    -84.99
October      -88.13    -87.98
October      -97.22    -85.01
October      -91.50    -81.49
October      -96.06    -86.09
November     -86.08    -82.49
November     -96.98    -84.45
November     -89.02    -84.01
November     -91.50    -90.50
December     -91.50    -90.50
December     -96.00    -85.00

Table 4
Percent frequency of occurrence (%FO) of total larvae, total
number of larvae and preflexion larvae collected, assemblage
location (assigned based on quotient analysis), and monthly
are listed occurrence of larvae of each species of grouper
collected along the Straits of Florida transect (see Fig.
1A). The order in which the species reflects month of first
capture. The "(a)" symbol indicates months with only later
stage larvae collected. The "(b)" symbol indicates when
preflexion larvae were collected. The "(c)" symbol indicates
when preflexion larvae were collected significantly more
frequently than would be expected if larvae were evenly
dispersed (based on quotient analysis).

                                                        No. of

Species                    Common name           %FO     Total

Mycteroperca bonaci        Black grouper         1.82         8
Cephalopholis fulva        Coney                 1.56        27
Epinephelus guttatus       Red hind              1.30       199
Epinephelus striatus       Nassau grouper        1.04        11
Mycteroperca venenosa      Yellowfin grouper     1.30        20
Paranthias furcifer        Atlantic creolefish   1.56        13
Mycteroperca phenax        Scamp                 1.04         4
Epinephelus morio          Red grouper           1.82         9
Hyporthodus nigritus       Warsaw grouper        0.26         1
Hyporthodus niveatus       Snowy grouper         1.82         7
Epinephelus drummondhayi   Speckled hind         0.52         2
Cephalopholis cruentata    Graysby               9.64       141
Alphestes afer             Mutton hamlet         0.26         1
Hyporthodus favolimbatus   Yellowedge grouper    4.95        73
Hyporthodus mystacinus     Misty grouper         0.78         4
Gonioplectrus hispanus     Spanish flag          0.26         1

                           Number of species                 16

Species                    Preflexion   Assemblage   Jan   Feb   Mar

Mycteroperca bonaci                 2      West      (c)
Cephalopholis fulva                13      East            (c)   (c)
Epinephelus guttatus              183      East            (c)   (c)
Epinephelus striatus                6      East            (b)   (a)
Mycteroperca venenosa               6      East            (b)   (c)
Paranthias furcifer                 8                      (a)   (c)
Mycteroperca phenax                 2                            (c)
Epinephelus morio                   2      West                  (a)
Hyporthodus nigritus
Hyporthodus niveatus                6      West
Epinephelus drummondhayi
Cephalopholis cruentata            17      East
Alphestes afer
Hyporthodus favolimbatus            6      West
Hyporthodus mystacinus
Gonioplectrus hispanus

                                   11                  1     5     7

                                       Month collected

Species                    Apr   May   Jun   Jul   Aug   Sep

Mycteroperca bonaci        (a)   (a)   (a)
Cephalopholis fulva        (a)               (a)
Epinephelus guttatus
Epinephelus striatus
Mycteroperca venenosa      (b)
Paranthias furcifer        (a)
Mycteroperca phenax        (c)
Epinephelus morio                (c)
Hyporthodus nigritus       (a)
Hyporthodus niveatus             (b)                     (c)
Epinephelus drummondhayi         (a)
Cephalopholis cruentata                (b)   (c)   (c)   (a)
Alphestes afer                         (a)
Hyporthodus favolimbatus                           (a)   (a)
Hyporthodus mystacinus                                   (a)
Gonioplectrus hispanus

                             6     4     3     2     2     4

                           Month collected

Species                    Oct   Nov   Dec

Mycteroperca bonaci
Cephalopholis fulva
Epinephelus guttatus
Epinephelus striatus
Mycteroperca venenosa
Paranthias furcifer
Mycteroperca phenax
Epinephelus morio
Hyporthodus nigritus
Hyporthodus niveatus       (c)
Epinephelus drummondhayi   (a)
Cephalopholis cruentata    (a)   (b)
Alphestes afer
Hyporthodus favolimbatus   (c)   (a)
Hyporthodus mystacinus     (a)
Gonioplectrus hispanus     (a)

                             6     3     1

Table 5
Results of best generalized additive models (GAMs)
predicting percent frequency of occurrence for each
subregion and season. TX-LA=Texas-Louisiana shelf, MS-AL
nFL=Mississippi-Alabama-northern Florida Shelf, and wFL =
west Florida Shelf. **** P-value <0.001, *** P-value <.01
** P-value < 0.05 and P-value <0.1. Covariates that were not
included in the model are marked with "na." The percentage
of the deviance from the null model explained by this model
is labeled "% Dev. exp." Generalized cross-validation (GCV)
and Akaike's information criterion ([AIC.sub.c] were used to
determine the best model from all combinations of covariates
(year, surface temperature, surface salinity, and water
depth). [r.sup.2]=the adjusted coefficient of determination.
AIC, weight is a measure of the likelihood that the model is
the best representation of the data (values range from 0 to 1).

Region      Season   Intercept     Year         temperature

TX-LA       Fall     **** 2.719    na           * 1.0
MS-AL-nFL   Fall     **** 6.0257   ** 1.0       na
wFL         Fall     **** 6.5939   *** 2.920    ** 2.436
M           Spring   **** 3.7240   **** 2.942   na

            Surface     Water                % Dev.
Region      salinity    depth       rz       exp.     GCV

TX-LA       na          na          0.0958   14.3     3.7348
MS-AL-nFL   na          na          0.244    28.4     21.453
wFL         *** 2.195   *** 2.076   0.874    94.5     12.247
M           ** 2.141    ** 1.0      0.764    84       5.6079

Region      AICc       weight

TX-LA       84.89725   0.162
MS-AL-nFL   119.8604   0.383
wFL         87.30072   0.998
M           89.9197    0.523
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