Bull Mar Sci. 91(4):399–418. 2015 research paper http://dx.doi.org/10.5343/bms.2015.1001
Reef relief and volume are predictors of Atlantic goliath grouper presence and abundance in the eastern Gulf of Mexico
1 Florida Fish and Wildlife AB Collins 1, 2 * Conservation Commission, Fish LR Barbieri 1 and Wildlife Research Institute, 3 100 8th Avenue SE, Saint RS McBride Petersburg, Florida 33701. ED McCoy 4 2 Current address: Florida Sea PJ Motta 4 Grant Agent, University of Florida IFAS Extension, Manatee County Government, 1303 17th Street West, Palmetto, Florida ABSTRACT.—Atlantic goliath grouper, Epinephelus 34221. itajara (Lichtenstein, 1822), presence, abundance, and size 3 National Marine Fisheries distribution were assessed during monthly underwater visual Service, Northeast Fisheries surveys at natural and artificial reefs in the central eastern Science Center, 166 Water Gulf of Mexico (7–50 m depth). Atlantic goliath grouper were Street, Woods Hole, more likely to be present, and to occur in greater abundance, Massachusetts 02543. at artificial reefs. Abundance was positively related to vertical 4 University of South Florida, relief and structural volume, and the largest numbers of Department of Integrative individuals were observed at high volume artificial reefs (e.g., Biology, 4202 East Fowler shipwrecks). This was likely due to greater refuge availability Avenue, Tampa, Florida 33620. provided by artificial reefs within the study region, where * Corresponding author email: structurally comparable natural habitats are rare. Atlantic
The spatial distribution of marine fish populations is rarely uniform. Whether or not a species is present within a given area is influenced by an extensive suite of factors, including habitat suitability, individual movement, and the presence of con- specifics (Sinclair 1988, MacCall 1990). Numerous studies have demonstrated the influence of habitat features upon fish presence and abundance, especially for reef fishes (e.g., Sale and Douglas 1984, Jones 1991, Hixon and Beets 1993, Sale et al. 1994, Nagelkerken et al. 2000, Wilson et al. 2010, Heyman and Wright 2011), and assess- ments of populations and stock status are better informed when measures of habitat association and suitability are well defined (Jones and Syms 1998). In the case of exploited or protected species, identification of the parameters that influence habitat
Bulletin of Marine Science 399 © 2015 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 400 Bulletin of Marine Science. Vol 91, No 4. 2015 selection is critical to ensure management of important areas and to efficiently target monitoring efforts during attempts to assess recovery or disturbance (MacCall 1990, Jones and Syms 1998). Atlantic goliath grouper [Epinephelus itajara (Lichtenstein, 1822); hereafter “go- liath grouper”] may attain 2.5 m in total length (TL), weigh up to 400 kg, and live at least 37 yrs (Bullock et al. 1992, Craig et al. 2011). The species historically oc- curred throughout subtropical and tropical waters of the Atlantic Ocean and Gulf of Mexico (Bullock et al. 1992, Craig et al. 2011), but a significant population decline was observed through the latter part of the 20th century after intense fishing pressure (Sadovy and Eklund 1999). Goliath grouper were protected from harvest in US wa- ters in 1990 (GMFMC 1990, SAFMC 1990) and in 1994 the species was listed as criti- cally endangered on the IUCN World Conservation Union’s Red List of Threatened Species (Pusack and Graham 2009). The species remains protected in US waters at this time and is also protected in other parts of the Atlantic Ocean and Caribbean region (Craig et al. 2011), but fisheries persist in some areas and the status of goliath grouper throughout the geographic range of the species remains uncertain. Within US waters, goliath grouper have responded well to protection and are show- ing signs of recovery (Cass-Calay and Schmidt 2009, Koenig et al. 2011). However, their life history characteristics make them especially susceptible to overfishing (e.g., long lived, late maturation, aggregate to spawn; Bullock et al. 1992, Musick 1999, Sadovy and Eklund 1999, Musick et al. 2000). Juvenile goliath grouper settle in shallow, nearshore estuaries, commonly near mangroves (Eklund and Schull 2001, Koenig et al. 2007, Lara et al. 2009), and display an ontogenetic shift to offshore ma- rine habitats with growth (Smith 1976, Koenig et al. 2007). Adults are reef associated, and typically occur at depths <50 m (Bullock et al. 1992, Heemstra and Randall 1993, Colin 1994, Gerhardinger et al. 2006, Koenig et al. 2011). Individuals are sedentary and display high site fidelity through most of the year, except during reproductive periods (August–September), when they may travel hundreds of kilometers to reach spawning aggregations (Sadovy and Eklund 1999, Koenig et al. 2011, Koenig and Coleman 2013, Collins 2014). This predictable and continuous association with reef habitats which are relatively close to shore, further increases goliath grouper vulner- ability to exploitation (Huntsman et al. 1999, Koenig et al. 2011). Future success of the goliath grouper population depends upon responsible man- agement as well as the availability of suitable habitat and resources throughout on- togeny. The southeastern Gulf of Mexico has historically been a center of abundance for goliath grouper (Bullock and Smith 1991), and this region is also the area where recovery has been most evident (Koenig et al. 2011). Using visual survey data at reef habitats from volunteer and scientific divers collected from 1994 through 2008, Koenig et al. (2011) performed a comprehensive assessment of goliath grouper re- covery in waters off the state of Florida. They documented the greatest numbers of goliath grouper at high relief artificial and rocky reefs, and greatest densities were observed off the southwest coast of Florida (between Charlotte Harbor and the Florida Keys). We aimed to build on this work by providing a detailed quantitative assessment of relative abundance and size distribution of goliath grouper as associ- ated with specific habitat features off the central west coast of Florida. The study area is just north of the species’ historical center of abundance, and provides data for a region where relatively few quantitative surveys have been performed. Collins et al.: Predictors of goliath grouper presence and abundance 401
Based on what is known regarding the life history of this species and their pref- erence for high-relief habitat that provides shelter (Bullock et al. 1992, Sadovy and Eklund 1999, Koenig et al. 2011), we predicted that goliath grouper relative abun- dance would exhibit a positive relationship with habitat relief and volume. Further, we expected that there would be a positive relationship between fish size and depth, since they settle in estuaries and are expected to move offshore as they approach maturity. In the absence of landings data and the associated life history informa- tion (e.g., length and age composition), quantification of size structure can provide a proxy for age distribution. Therefore, the present study aimed to: (1) describe the presence and abundance of goliath grouper as related to specific habitat features (ar- tificial vs natural, depth, relief, volume) within a region where high relief natural reefs are rare; and (2) provide detailed information regarding size distribution of the species within the study area. This information should advance the ability to monitor population changes through time, and assist with predictions of population dynam- ics for a species currently in a period of stock recovery.
Methods
Selection and Evaluation of Survey Sites.—Visual surveys and underwater video were used to quantify the abundance and size distribution of goliath grou- per within the study area between October 2007 and May 2010. Surveys (n = 379) were conducted during daylight hours in all months of the year, and survey sites (n = 80) were distributed across a range of depths to 50 m to include both artificial and natural reefs (Fig. 1). Artificial reefs n( = 36 sites, 268 surveys) included mostly shipwrecks, but also incorporated other anthropogenic structures (concrete pilings or concrete rubble fields). Natural reefs n( = 44 sites, 111 surveys) included lime- stone ledges, pinnacles, and offshore freshwater spring openings, which comprise the typical hard-bottom habitat within the study area (Smith 1976, Simmons et al. 2014). Sites were selected to ensure that the full spectrum of available reef types within the region were included, and effort was made to survey a diverse distribution of habitat types with varying levels of structural complexity and relief. Sites were chosen based upon published locations of reef habitat (Florida Fish and Wildlife Conservation Commission, available from http://ocean.floridamarine.org/mrgis/) and upon rec- ommendations by local veteran divers who served as the cooperative research part- ners for the duration of this research [Saint Petersburg Underwater Club (SPUC), pers comm]. Although goliath grouper are protected from harvest, there remains a targeted catch-and-release fishery and the species is often caught incidentally by anglers tar- geting other reef fish. Sites were therefore classified as “shallow” (≤20 m) or “deep” (>20 m), based on the depth at which pressure related fishing trauma (Wilde 2009, Sumpton et al. 2010) becomes more likely to occur for this species (approximately 20 m; Collins 2014; C Koenig, Florida State University, pers comm). Seasonal differ- ences were assessed through quarterly sampling of designated sites (Fig. 1). To better define seasonal patterns in the size distribution of fish, a greater number of artificial reefs than natural reefs (12 vs 6) were targeted for quarterly surveys because artificial reefs presented an increased opportunity to observe and measure goliath grouper (A Collins, pers obs). These 18 sites were surveyed at least once per season, defined as winter (January–March), spring (April–June), summer (July–September), and fall 402 Bulletin of Marine Science. Vol 91, No 4. 2015
Figure 1. Study area within the central eastern Gulf of Mexico. Between November 2007 and May 2010, 379 surveys were performed at 80 different sites classified either as artificialn ( = 36) or natural (n = 44) reefs. Sites visited at least quarterly (n = 18) are circled. Offshore bathymetry contours are displayed by 10 m intervals; sites were designated as “shallow” (≤ 20 m) or “deep” (>20 m), as indicated by the bold contour.
(October–December). An additional 62 sites (24 artificial and 38 natural reefs; Fig. 1) surrounding the designated 18 quarterly sites were surveyed opportunistically throughout the study period. Site relief was recorded as the maximum height of the site (straight vertical dis- tance from the seafloor to the top of the habitat structure). Relief was arbitrarily characterized as “low” (<1.5 m) or “high” (>1.5 m), based on knowledge of veter- an divers regarding available hard bottom reefs within the study area (SPUC, pers comm) and a qualitative assessment of the vertical space needed for multiple adult goliath grouper to easily take refuge within a structure. Site volume was estimated for artificial habitats by separating the site into manageable, measurable units, and summing unit volumes (length × width × height) to obtain a total volume of the structure. Volume was characterized as “low” (<1000 m3), “moderate” (1000–10,000 m3), or “high” (>10,000 m3) and categorized post-hoc based on the range of artificial reef volumes recorded during the present study. The structure was also assessed for internal cavities and the presence of openings >1 m2. For natural habitats, site volume was not calculated, but the vertical relief, presence of undercuts, and length of the ledge were recorded. Assessing Goliath Grouper Abundance and Size Distribution.—Goliath grouper presence and abundance were assessed through underwater video surveys performed while swimming in a single direction from one end of the site to the other. All crevices and holes were visually inspected, and the process was then repeated in reverse so that all sites were surveyed in their entirety at least twice during each Collins et al.: Predictors of goliath grouper presence and abundance 403
Figure 2. A goliath grouper, Epinephelus itajara, fitted with an external ID tag. Large print assists divers with resighting and individual identification, and a telephone number directs anglers to report tagged fish to the Florida Fish and Wildlife Conservation Commission tagged fish hotline. survey. Total survey time was positively related to the total area of the site; all sur- veys lasted a minimum of 15 min. Due to the large size and high visibility of goli- ath grouper, all individuals observed were counted and restrictive underwater visual survey methods were not applied (e.g., counting only individuals within 5 m of the midline of a transect tape or within a defined cylinder; Colvocoresses and Acosta 2007). Surveys performed in visibilities <5 m or lasting <15 min were excluded from statistical analyses. Surface and bottom water temperatures were recorded prior to each survey using a multi-probe meter (Yellow Springs Instruments, Model 85). Goliath grouper were considered present if at least one individual was observed during the survey. Abundance values were minimum estimates defined as the num- ber of goliath grouper recorded by the diver during a one-way survey of the site to re- duce the potential of double-counting individuals. During each survey, all attempts were made to identify characteristic marks of individual fish to further avoid over- estimating abundance. Surveys were recorded on a digital video camera (Sony HDR- CX550V) in an underwater housing (Light and Motion Bluefin) with a wide angle lens. A custom made laser apparatus fitted to the video camera projected two equi- distant laser points (20 cm apart) onto the body of the fish and permitted total length (TL) estimates (to the nearest cm) for fish filmed perpendicular to the optical axis of the camera. These still frames were removed from survey videos and processed using image analysis software (Image Pro Plus) to calculate TL. Conventional Tagging of Goliath Grouper.—Following the visual survey, goliath grouper were tagged in situ using a modified speargun to shoot the tag into the musculature directly beneath the dorsal fin (Koenig et al. 2011). Tagging was per- formed opportunistically to provide additional data regarding site fidelity, recapture events, and potential movement patterns. External tags were constructed of a nylon dart (Floy BFIM96 Billfish tag) modified to display an oversized plastic ID tag (6.5 × 3 cm) with enlarged text (2 cm font height) (Fig. 2). A telephone number on the tag encouraged anglers and divers to report fish. Prior to deployment, tags were sprayed 404 Bulletin of Marine Science. Vol 91, No 4. 2015 with clear anti-fouling paint (Aquagard Alumi-Koat, Flexdel Corp., NJ) to inhibit biofouling. Goliath grouper <100 cm TL were not tagged to reduce the potential for injury. Statistics.—The unbalanced survey design and correlated nature of these data dictated the use of statistical analyses that could account for these condi- tions. Therefore, a generalized linear model (Proc GENMOD; SAS version 9.2, SAS Institute, Inc., Cary, NC, USA) was used to identify relationships between goliath grouper presence and abundance and the following fixed parameters: habitat (artifi- cial or natural); depth zone (deep, > 20 m; or shallow, ≤ 20 m); season (winter, spring, summer, or fall), site relief (low, < 1.5m; or high, > 1.5 m); and site volume (low, < 1000 m3; moderate, 1000–10,000 m3; or high, > 10,000 m3). Volume was calculated for artificial habitats only. Presence was modeled as a binomial distribution; abundance was modeled as a negative binomial distribution. Each model considered interac- tion effects between each of the fixed parameters, and non-significant interaction terms were removed to find the “best” model. To address the confounding effects of reef type and vertical relief, a subset of the data containing only those reefs that overlapped in vertical relief (1.2–5.5 m, n = 44 sites) was examined in the same man- ner. In addition, the relationship between site relief and the mean number of goliath grouper present was also modeled using site relief as a continuous variable. A Mann- Whitney Rank sum test was used to determine if fish size was related to habitat type (artificial vs natural). To examine the correlation between size distribution and site parameters (depth, relief, and season), a general additive model (GAM) was applied (using the gamm4 package in R), where site parameters were fixed effects and site ID was a random effect to account for repeated measures of individuals over time. Finally, an analysis of variance (ANOVA) was used to test the relationship between reef relief and site depth.
Results
Surveys.—Research dives performed in adequate visibility (survey n = 349) result- ed in an assessment of 80 sites, including 44 natural reefs (total survey n = 104) and 36 artificial reefs (total survey n = 245) (Fig. 1). Site depth ranged 7–45 m for artificial reefs and 10–50 m for natural reefs. Natural reefs ranged in relief from 0.5–5.5 m (median = 1.2 m). Artificial reefs ranged in relief from 1.2 to 11.8 m (median = 3.7) and in volume from 10 to 13,716 m3. All natural reefs surveyed had undercuts that were restricted in height by the vertical relief of the outcropping. All artificial reefs surveyed had multiple openings of at least 1 m2. Survey time was positively related to the area of the site, and ranged 15–125 min (mean = 36 min). Bottom temperature during the study period ranged 14.1–31.7 °C. The frequency of surveys for each site was dependent upon environmental conditions, and ranged 1–29 surveys per site. Presence.—Goliath grouper were present during 90% of surveys at artificial reefs (221 of 245 surveys; 34 of 36 sites), but during only 40% of surveys at natural reefs (35 of 104 surveys; 17 of 44 sites) (Fig. 3). Presence was significantly less at natural reefs during all seasons and across all depths sampled (Proc GENMOD: P < 0.0001, Table 1). Presence decreased during the winter (Table 1, Fig. 3). Presence was more likely at sites with high relief (Proc GENMOD: P = 0.031), but presence was not affected by Collins et al.: Predictors of goliath grouper presence and abundance 405
Table 1. Results of PROC GENMOD test for effects of habitat type (artificial vs natural), depth zone (deep vs shallow), relief (high vs low), seasonal quarter (winter: Jan–Mar, spring: Apr– Jun, summer: Jul–Sep, fall: Oct–Dec), and volume (low, moderate or high) on the presence and abundance of goliath grouper, Epinephelus itajara, observed during underwater visual surveys within the central eastern Gulf of Mexico. Presence was modeled as a binomial distribution; abundance was modeled as a negative binomial distribution. Significant differences (P < 0.05) are indicated in bold. Values for difference (Diff) of least squares (LS) means are P values.
Presence Abundance Diff of LS Diff of LS Variable df F P means F P means Habitat 1/342 17.23 <0.0001 38.12 <0.0001 Depth zone 1/342 1.47 0.2268 9.10 0.0027 Relief 1/342 4.67 0.0314 8.10 0.0047 Season 3/342 3.17 0.0244 2.32 0.0748 Winter vs spring 0.0056 0.3521 Winter vs summer 0.0146 0.0255 Winter vs fall 0.0127 0.7468 Spring vs summer 0.7513 0.1062 Spring vs fall 0.9625 0.5231 Summer vs fall 0.7576 0.0382 Volume 2/215 0.08 0.9273 16.09 <0.0001 site depth (P = 0.227) or site volume (P = 0.927; volume was calculated for artificial sites only) (Table 1). Abundance.—Greatest numbers of goliath grouper were observed at artificial reefs (range 0–24 individuals; mean = 4.77). Artificial reefs in deep water (>20 m) had larger numbers of goliath grouper than those in shallow water (Proc GENMOD: P < 0.0001, Table 1), and this pattern was evident through all seasons (Fig. 4), with the highest numbers observed during the summer (Fig. 4, Table 1). High relief artificial reefs had up to 24 individuals (mean: approximately 5), while low relief artificial reefs typically had only 1 individual present (Fig. 5). Abundance was positively related to artificial reef relief and volume (Figs. 5, 6). It is important to note that the artificial reefs with the highest relief and greatest volume were also in deeper water (>20 m), and there was a positive relationship between site relief and site depth (ANOVA: r2 = 0.14, P = 0.03). Natural reefs had consistently low abundances of goliath grouper throughout the study area and across all seasons (range 0–3 individuals; mean = 0.43; Fig. 4). Similar to artificial reefs, abundance at natural reefs was positively related to reef relief (Table 1, Figs. 5A, 6A). An evaluation of a subset of data that contained natural and artificial reefs of comparable vertical relief (1.2–5.5 m, n = 44 sites) demonstrated that goliath grouper were still less likely to be present and occur in lower abundances at natural reefs (Proc GENMOD: P < 0.0001, Fig. 6B). Size Distribution.—Underwater videography and subsequent image analyses yielded total length measurements for 65% (823 of 1270) of goliath grouper that were filmed during surveys. Lengths verified through image analysis ranged from 36 to 214 cm TL. Throughout the study, the majority of individuals observed were 80–160 cm TL. There were no significant differences in size frequencies across years, or be- tween fish size and depth (Proc GENMOD: P = 0.8171). Individuals as small as 67 cm 406 Bulletin of Marine Science. Vol 91, No 4. 2015
Figure 3. The proportion of surveys performed where at least one goliath grouper Epinephelus itajara was present. Data are grouped by (A) reef type, (B) depth zone (shallow, ≤20 m; or deep, >20 m) and (C) season (winter, January–March; spring, April–June; summer, July–September; and fall, October–December). The total number of surveys performed for each group is displayed within each bar. Statistical differences (Proc GENMOD: P < 0.05) are indicted by letters above each bar. Surveys were performed off western Florida between November 2007 and May 2010.
TL were verified from sites as far as 80 km from shore and as deep as 36 m (Fig. 7A). The size of fish observed in shallow (≤20 m) water ranged 36–204 cm TL (mean = 120 cm), and fish measured in deep (>20 m) water ranged 54–214 cm TL (mean = 121 cm). Only 18 individuals were measured at natural sites, but they were significantly smaller (mean TL = 99 cm) than those observed at artificial sites (mean TL = 121 cm) (Mann-Whitney rank sum test: P = 0.002). The GAM model with repeated measures indicated no relationship between fish TL and site depth P( = 0.790) or site relief (P = 0.227), but there was a significant effect of seasonP ( < 0.01), where larger fish were observed during the summer (Fig. 7B). Site Fidelity and Movement Based on Conventional Tags.—In total, 172 goliath grouper were identified by unique markings or tagged in situ with exter- nal identification tags during surveys. The majority of fish were tagged at artificial habitats (166 of 172 tagged fish), and all resightings occurred at artificial habitats. Collins et al.: Predictors of goliath grouper presence and abundance 407
Figure 4. Abundance of goliath grouper, Epinephelus itajara, per season during surveys of natural (top graph) and artificial (bottom graph) reefs within shallow (≤20 m) and deep (>20 m) water. The mean of each data set is represented by the bold solid line, the median by the thin line, the boxes indicate the interquartile range, and 95% confidence intervals are contained within the er- ror bars. The bold dots indicate observations that fall outside the confidence intervals. Surveys were performed off western Florida between November 2007 and May 2010.
Resightings were verified for 27 of 172 (16%) tagged fish (Table 2). Most resightings were witnessed by one of us (ABC), with four recaptures reported by anglers or rec- reational divers. Time at large ranged from 1 to 958 d, and eight individuals were resighted multiple times (2–5 resightings per fish). One recapture was reported 203 km away from the initial tagging site, but most (83%) resightings or recaptures oc- curred at the same location as the initial tagging event. Six individuals were verified at nearby artificial reefs other than their initial tagging site, which provided evidence for movement between artificial reefs within the study area (Table 2).
Discussion
Before the harvest moratorium (GMFMC 1990, SAFMC 1990), the majority of commercially harvested goliath grouper were landed along Florida’s southwest coast (Bullock et al. 1992). This area is believed to be the center of abundance for this species due to the extensive mangrove nursery habitat that exists south of Naples 408 Bulletin of Marine Science. Vol 91, No 4. 2015
Figure 5. (A) The number of goliath grouper, Epinephelus itajara, observed during surveys of artificial (survey n = 245) and natural (survey n = 104) reefs with high (≥1.5 m) or low (<1.5 m) relief. (B) The number of goliath grouper observed by artificial reef volume for deep (>20 m) and shallow (≤20 m) artificial reefs. Volume was characterized post-hoc as low (<1000 m3), medium (1000–10,000 m3), or high (>10,000 m3). There were no high volume artificial reefs surveyed in shallow water (na). The mean of each data set is represented by the bold solid line, the median by the thin line, the boxes indicate the interquartile range, and 95% confidence intervals are con- tained within the error bars. The bold dots indicate observations that fall outside the confidence intervals. Letters denote significant differences among groups (PROC GENMOD: P < 0.05). Surveys were performed off western Florida between November 2007 and May 2010. (Bullock and Smith 1991, Sadovy and Eklund 1999, Koenig et al. 2007), and it is also where recovery has been most evident (Cass-Calay and Schmidt 2009, Koenig et al. 2011). As the population rebounds, it is expected that greater numbers of individuals will occur at increasing distances from the population center of abundance and ori- gin of recovery (Rosenzweig 1981, MacCall 1990). Continued survey efforts to docu- ment changes in the relative abundance of goliath grouper throughout their range are therefore useful in determining stock status (Fretwell and Lucas 1969, Rose and Kulka 1999, Jennings et al. 2001). Collins et al.: Predictors of goliath grouper presence and abundance 409
Figure 6. (A) The relationship between reef relief and mean number of goliath grouper, Epinephelus itajara, observed during visual surveys off western Florida between November 2007 and May 2010. Abundance was positively associated with site relief at both artificial r( 2 = 0.15, P = 0.019, df = 35) and natural (r2 = 0.23, P = 0.001, df = 43) reefs. (B) The number of goliath grouper ob- served during surveys at reef habitats with comparable vertical relief (between 1.2 and 5.5 m; n = 44 sites). The mean of each data set is represented by the bold solid line, the median by the thin line, the boxes indicate the interquartile range, and 95% confidence intervals are contained within the error bars. Presence and Abundance.—Goliath grouper were present during almost all surveys at artificial reefs, but were observed at natural reefs only sporadically. This is consistent with the findings of Koenig et al. (2011), whose surveys also documented largest numbers of goliath grouper at artificial habitats within this region. On the west Florida shelf, artificial reefs typically provide greater relief and structural com- plexity than natural reefs (Smith 1976, Parker et al. 1983, Simmons et al. 2014). It is suspected that the positive relationship between goliath grouper abundance and reef relief and volume is associated, at least in part, with ample refuge opportunities for large fishes. This has been observed for other groupers, which exhibit a positive -re lationship between abundance and size of artificial reefs [e.g., gag, Mycteroperca mi- crolepis (Goode and Bean, 1879); Lindberg et al. 2006], as well as the vertical height of 410 Bulletin of Marine Science. Vol 91, No 4. 2015
Figure 7. (A) Size distribution of goliath grouper, Epinephelus itajara, observed at each site sur- veyed between November 2007 and May 2010. Sites are arranged in order of depth (7–48 m) and include all sites for which goliath grouper were observed and measured. The shaded horizontal bar represents the size range at which goliath grouper mature (110–135 cm TL; Bullock et al. 1992). The vertical dotted line separates shallow (<20 m) from deep sites. Sites that only show the mean value (bold solid line) indicate that fewer than three fish were measured. (B) Size dis- tribution of goliath grouper observed by season. Numbers of measured fish during each season are denoted inside each box. Letters denote significant differences in size among seasons and/or depth zones (GAM: P < 0.05). The mean of each data set is represented by the bold solid line, the median by the thin line, the boxes indicate the interquartile range, and 95% confidence intervals are contained within the error bars. ledges [e.g., gag and scamp, Mycteroperca phenax (Jordan and Swain, 1884); Kendall et al. 2008]. Structural complexity may provide refuge from predation (Piko and Szedlmayer 2007, White 2007), increase foraging success (Helfman 1981, Horinouchi et al. 2009), or serve to concentrate prey (Jones 1991, Almany 2004, Arena et al. 2007). Artificial reefs likely provide considerable refuge and foraging opportunities (e.g., Bohnsack 1989, Hackradt et al. 2011), where the availability of comparable natural habitat is limited. There are more than 2400 artificial reefs documented off of the Florida coast, and more than 600 are known within the study area (FWC artificial reef program: http://myfwc.com/conservation/saltwater/artificial-reefs/). The role Collins et al.: Predictors of goliath grouper presence and abundance 411
Table 2. Tag/recapture data for goliath grouper, Epinephelus itajara, that have been resighted since their initial tagging date. Days at large indicates number of days between sightings (* = recaptured and reported by angler; ** = caught by one of us (AC) via hook and line as part of another study). Distance moved is the straight line distance between sites of tagging and resighting. Individual IDs correspond to their tag ID; individuals HK and YS were not tagged but had distinctive features that allowed for easy recognition. Depth is that of site at tagging, or depth at resighting (m), if different.
Days at Distance moved Size at tagging ID Tag date Resighting date large (km) (TL, cm) Depth 1 11/9/2007 11/29/2007 20 0 152 26 11 12/1/2007 6/22/2008* 204 203 122 19, 9 18 12/29/2007 7/20/2008 204 29 140 28, 34 31 2/4/2008 5/30/2008 116 0 100 18 55 4/2/2008 4/3/2008 1 0 181 28 57 4/2/2008 4/3/2008 1 0 178 28 67 4/18/2008 6/3/2008 46 0 133 19 87 6/3/2008 7/10/2008 37 0 142 19 90 6/3/2008 6/11/2008* 8 16 153 34, 26 7/10/2008 37 16 93 6/4/2008 7/4/2008 30 0 155 9 103 7/10/2008 7/23/2008 13 0 135 25 107 7/18/2008 7/27/2008 9 0 143 29 112 7/20/2008 7/23/2008 3 0 118 34 113 7/20/2008 7/23/2008 3 0 135 34 136 8/8/2008 9/4/2008 27 0 100 21 9/28/2008 51 0 137 8/8/2008 7/22/2010* 713 10 170 21, 19 159 10/10/2008 8/28/2009 322 28 129 31, 30 184 5/8/2009 5/9/2009 1 0 139 32 6/1/2009 24 0 188 5/11/2009 8/11/2009 92 0 110 19 HK 5/15/2009 5/25/2009 10 0 190 21 6/25/2009 41 0 190 6/8/2009 6/20/2009 12 0 137 30 7/10/2009 32 0 7/21/2009 43 0 8/28/2009 81 0 10/7/2009 121 0 194 6/9/2009 8/4/2009 56 0 114 26 9/1/2009 84 0 10/13/2009 126 0 YS 6/17/2009 6/25/2009 8 0 80 19 197 7/3/2009 7/10/2009 7 0 179 19, 26 8/15/2009 43 15 200 6/1/2009 6/25/2009 24 0 149 19 7/9/2009 38 0 8/11/2009 71 0 10/1/2009 122 0 206 11/17/2009 11/24/2010* 372 0 150 26 208 11/17/2009 4/14/2011** 513 0 182 26 7/2/2012** 958 0 190 412 Bulletin of Marine Science. Vol 91, No 4. 2015 that these reefs—especially large, high volume structures such as shipwrecks—play in the distribution of goliath grouper is becoming evident as the population recovers. The results reported herein are consistent with reports of stock recovery, with mean values of 4–5 individuals recorded at artificial reefs [in comparison to Koenig et al. (2011), who recorded a mean of 1–2 individuals at high relief artificial and rocky reefs within the study region]. Low abundances at nearby natural reefs suggest a behavior- al preference for the higher relief, higher volume habitat that artificial reefs provide. Whether or not these artificial reefs are a benefit to the population by facilitating production, or are simply aggregating fish that would normally be more dispersed under natural conditions (i.e., “source” vs “sink”), is unknown. Whether the density of goliath grouper at a particular reef is constrained by refuge space, prey availability, or current population levels is not known. It has been demon- strated that in some cases the availability of shelter may be more important in habitat selection than competition for food. For example, gag grouper (M. microlepis) have been demonstrated to sacrifice growth for shelter at artificial reefs in the northern Gulf of Mexico (Lindberg et al. 2006). Data regarding the metabolic needs of goliath grouper in the wild are not available, but an adult goliath grouper in an aquarium was observed to consume only 4%–6% of its total body weight per month (Kittell and Ratte 2008). Consistent numbers of goliath grouper observed at sites surveyed sea- sonally suggest that these areas provided sufficient resources to maintain approxi- mately the same number of individuals throughout the year. The northern range of goliath grouper should remain restricted by the thermal tolerance of the species (mortality typically occurs at sustained temperatures of <15 °C; Gilmore et al. 1978, FWC, unpubl data). Although individuals have been reported in the Gulf of Mexico as far north as the Florida panhandle and the mouth of the Mississippi River (Franks 2005, Koenig et al. 2011), these individuals are likely pres- ent only seasonally and probably move south or to deeper water during the colder months of the year when bottom water temperatures in the northern Gulf of Mexico are regularly <15 °C. Within the present study area, fewer fish were observed at shal- low sites during the winter, which may have been a result of fish moving out of the area in response to lower water temperatures, or simply an artifact of lower detection capability by divers since goliath grouper become less active when the water is cold (A Collins, pers obs). Even so, multiple fish were still recorded at most sites through- out the year and acoustic monitoring of individuals (Collins 2014) further supports year round residence of goliath grouper within the study region. Size Distribution.—Length (and by proxy, age) composition of a stock can be correlated with population size and indicate stock status (Ricker 1963, Jennings et al. 2001); thus, quantifying size distribution of individuals can assist assessments of population recovery. Most goliath grouper recorded during visual surveys for the present study were between 80 and 160 cm TL (range 36–214 TL, median = 121 cm TL; n = 823), which corresponds with an age distribution of approximately 5–15 yrs (Bullock et al. 1992). This is generally consistent with Koenig et al. (2011), who sur- veyed 17 sites within the study area between 2004 and 2008, and reported a median TL of approximately 130 cm (n = 32 individuals). For a fish that can live to at least 37 yrs and exceed 200 cm TL, the majority of fish observed during our study were rela- tively young and many were likely immature (length at maturity = 110–135 cm TL) (Bullock et al. 1992). Life history theory predicts the size and age distribution of most Collins et al.: Predictors of goliath grouper presence and abundance 413 marine fish populations will be typically skewed to the left (older fish are ultimately less numerous than younger ones; Walters and Martell 2004), so the size distribu- tion reported herein is not surprising. Unfortunately, there is no existing “healthy” baseline for goliath grouper with which to compare current population parameters, since the most comprehensive life history study to date (Bullock et al. 1992) was performed after the population had already suffered significant size and age trunca- tion (e.g., McClenachan 2009). Any change in fishing regulations (e.g., Shideler et al. 2015) should therefore be approached cautiously, since the removal of the largest and oldest individuals has the potential to increase population fluctuation and volatility (Anderson et al. 2008). It was initially expected that the largest goliath grouper would be observed the farthest from shore, based on the fact that juveniles settle within estuaries and move to deeper water as they approach maturity (Bullock et al. 1992, Gerhardinger et al. 2006, Koenig et al. 2007) and because other reef fish species in the Gulf of Mexico have been observed to display this pattern [i.e., hogfish Lachnolaimus maxi- mus (Walbaum, 1792), Collins and McBride 2011; gag M. microlepis, Coleman et al. 1996]. Size-based offshore migration of goliath grouper did not appear to be obliga- tory, however, as large adults (>150 cm) were observed throughout the depth range sampled and there was no relationship between fish size and depth or distance from shore. Interestingly, smaller (<100 cm TL), presumably sub-adult fish, were observed at sites as far as 80 km from shore, suggesting that individuals may disperse offshore at earlier ages than previously believed. It is also possible that a proportion of the population has always displayed this strategy and simply went unnoticed due to re- duced numbers and the absence of directed research activities. A peak in the size distribution and the abundance of goliath grouper was noted at deep artificial reefs during the summer. Goliath grouper in Florida aggregate to spawn July through September (Bullock et al. 1992, Sadovy and Eklund 1999) and will migrate long distances to reach spawning aggregation sites (Eklund and Schull 2001, Koenig et al. 2011, Koenig and Coleman 2013, Collins 2014). Previously doc- umented spawning aggregations in the southeastern Gulf of Mexico were at deep artificial reefs (35–45 m; Porch and Eklund 2004, Sadovy and Eklund 1999, Mann et al. 2009; D DeMaria, pers comm), but there have been no confirmed spawning ag- gregations identified within the study area to date. It is possible that the peak in large individuals during the summer at the deepest artificial reefs was related to spawning, but this was not verified and requires additional investigation. Site Fidelity and Movement Based on Conventional Tags.—Multiple studies have reported that goliath grouper maintain a high degree of site fidelity, both as juveniles (Frias-Torres et al. 2007, Koenig et al. 2007) and adults (Eklund and Schull 2001, Pina-Amargós and Gonzalez-Sanson 2009, Koenig et al. 2011). Site fi- delity of goliath grouper was therefore expected and almost all individuals resighted during the present study were in fact reported at their initial location up to 958 d after tagging. The recapture data herein also demonstrated long distance movements of up to 203 km from the initial site of tagging. Similar findings were reported by Koenig et al. (2011) who confirmed goliath grouper movements exceeding 200 km. These observations are important when implementing management plans and pro- viding guidelines for conservation, because areas of vulnerability range temporally 414 Bulletin of Marine Science. Vol 91, No 4. 2015 from relatively small daily activity spaces to lifetime ranges that have the potential to encompass hundreds of kilometers. In summary, goliath grouper were most abundant at high relief, high volume arti- ficial reefs within the study area on the west Florida shelf. Individuals were present during almost all surveys at artificial reefs, where average abundances were typi- cally between four and five individuals, but increased with site relief and site volume. Individuals were less common at natural reefs (mean abundance <1), and this is likely due to the fact that most of the natural hard bottom in the study region consists of low relief limestone outcroppings that offer minimal cover for large-bodied fish. The availability of artificial reefs appears to modify goliath grouper habitat choice (and therefore, distribution)—either by providing additional resources that allow the study area to support greater numbers of individuals overall or by simply aggregating individuals into greater densities than would be expected under natural conditions. Goliath grouper ranged in size from 36 to 214 cm TL, demonstrating the occurrence of both juveniles and large adults at offshore habitat. The existence of larger, presum- ably reproductively active (>135 cm) adults is an encouraging sign for continued pop- ulation recovery; additionally, the large number of younger, sub-adult fish indicates successful recruitment since the moratorium was implemented in 1990. Continued monitoring of the abundance and size distribution of goliath grouper within the study area as well as elsewhere (e.g., Cass-Calay and Schmidt 2009, Koenig et al. 2011) will assist in assessing stock status and population recovery. Advances in technology (e.g., GPS, side-scan sonar) continue to increase human ability to locate marine hard bottom habitats. These tools greatly assist monitoring and management efforts, but also increase fish susceptibility to harvest by making them easier to find. Site fidelity and the tendency for goliath grouper to gather pre- dictably around high relief structure that is relatively close to shore amplifies the interaction between goliath grouper and anglers. The life history traits of this spe- cies make it especially vulnerable to overharvest, so as the population recovers and pressure to reopen a fishery escalates (Frias-Torres 2013, Shideler et al. 2015), any changes in management should be considered with caution. The findings reported herein provide information regarding spatial and temporal habitat associations and size distribution of goliath grouper in the central eastern Gulf of Mexico, and should inform future management efforts.
Acknowledgments
This work could not have been completed without the efforts and dedication of the mem- bers of the St. Petersburg Underwater Club (SPUC). We would like to thank all of the partici- pating divers, specifically S Bratic, W Butts, J DeLaCruz, C Gardinal, C Grauer, B Hardman, S Hooker, I Lathrop, S Lucas, K Ludwig, M Joswig, D O’Hern, D Palmer, H Scarboro, R Taylor, and E Walker. We would also like to thank FWRI’s Fisheries-Independent Monitoring and Fish Biology programs for sampling assistance. M Murphy and E Leone provided statistical assistance. T Kellison served as the NOAA/NMFS partner and provided useful comments throughout the project. We would like to extend our gratitude to L Bullock, D DeMaria, and C Koenig for comments throughout this research, and three anonymous reviewers who provided insightful comments on previous versions of this manuscript. The majority of the work described herein was funded by a NOAA/NMFS Cooperative Research Program grant awarded to the Fish and Wildlife Research Institute (NOAA grant NA07NMF4540085). The views, statements, conclusions, and recommendations expressed herein are those of the au- thor and do not necessarily reflect the views of the US Department of Commerce or any of its subagencies. Collins et al.: Predictors of goliath grouper presence and abundance 415
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