Marine protected areas (MPAs), which prohibit all fishing activity, are beginning to be recognized as alternative marine conservation management tools implemented to attain sustainable fish populations by maintaining ecosystem biodiversity, conserving genetic diversity, enhancing spawning stock, increasing productivity and reproductive output and protecting habitat structure (reviews by Allison et al. 1998, Bohnsack 1998, Appeldoorn & Lindeman 2003). Most MPAs, regardless of size, seem to have a relatively rapid (1 to 3 yr) and positive effect on the density, biomass, size and diversity of organisms within the closed area compared to outside or after reserve formation versus before (Halpern & Warner 2002, review). Although these reviews showed the positive effects of MPA’s on various biological measures inside reserves, most existing reserves may be too small to benefit regional fisheries (i.e. beyond the area immediately adjacent to reserve boundaries) and have a limited ability to permanently protect populations such as groupers and snappers that engage in long-distance migrations (McClanahan & Kaunda-Arara 1996, Bohnsack 1998, McClanahan & Mangi 2000, Roberts et al. 2001). However, well-placed MPAs can protect particularly vulnerable periods during a species life history such as temporary residence in nursery, feeding and spawning habitats (Kramer & Chapman 1999).

The life-history characteristics of groupers forming spawning aggregations render them particularly vulnerable to even moderate fishing mortality. For example, most species of Caribbean groupers are protogynous hermaphrodites that form size-structured spawning aggregations comprised of small females and large terminal-phase males (Domeier & Colin 1997). Intensive fishing pressure on grouper spawning aggregations can severely reduce overall biomass (Alcala 1988, Roberts 1995), decrease size and age at sexual maturity due to selective removal of the large reproductive males (PDT 1990), and drastically alter the sex ratio and disrupt the social structure necessary for successful reproduction (Colin et al. 1987, Shapiro et al. 1994, Beets & Friedlander 1999). Seasonal and permanent closures have been enacted to protect the biological integrity of single-species fish spawning aggregations (Sadovy 1994, Bohnsack 1996, Domeier & Colin 1997). Unfortunately, area closures can take years to establish and, when finally implemented, overfishing has usually caused serious damage to the spawning populations and either collapse of the aggregation has already occurred or recovery is very slow (Olsen & LaPlace 1978, Claro et al. 2001).

Negative impacts of fishing on grouper and snapper spawning aggregations have been documented throughout the Caribbean, e.g. Belize (Heyman et al. 2001, Sala et al. 2001), Bermuda (Luckhurst 1996), Cuba (Claro & Lindeman 2003), Florida Keys (Lindeman et al. 2000), Mexico (Aguilar-Perera & Aguilar-Davila 1996), Puerto Rico (Shapiro et al. 1993, Sadovy et al. 1994a,b), and the US Virgin Islands (Olsen & LaPlace 1978). Few empirical examples exist, however, of a permanent marine protected area facilitating the recovery of a spawning aggregation. The primary objective of this paper was to report on the population response of a red hind spawning aggregation following establishment of a MPA.

In the United States Virgin Islands, intensive fishing throughout the 1970s and early 1980s eliminated several Nassau Epinephelus striatus and yellow-fin Mycteroperca venenosa grouper spawning aggregations (Olsen & LaPlace 1978). After the population collapse of these 2 species, commercial fishermen began targeting the red hind E. guttatus, a smaller serranid that also forms spawning aggregations (Beets & Friedlander 1999). Red hind contributed 70 to 99% of the total catch of fin fish landed in the Virgin Islands between 1987 and 1992 (Cummings et al. 1997). By the late 1980s an evaluation of the red hind stock around St. Thomas showed dramatic decreases in average length and an extremely skewed female-to-male sex ratio (15:1) of the spawning population (Beets & Friedlander 1992), suggesting a disproportional harvest of large males (Sadovy & Figuerola 1992). In an effort to avert another fishery collapse, a 3 mo seasonal closure, which encompassed the December through February spawning season, was implemented in November 1990 on the island of St. Thomas to protect the annual spawning aggregation of red hind. This spawning aggregation site, known locally as the Red Hind Bank, is located along the shelf edge 12 km south of St. Thomas and includes the site of an extirpated Nassau grouper spawning aggregation (Beets & Friedlander 1999).

After several years of seasonal protection the red hind spawning population on St. Thomas began to show signs of recovery. By 1997 the average size of spawning adults had increased by 7 cm in length and the sex ratio had shifted to 4 females per male (Beets & Friedlander 1999). The potential value of this site to the local fishery led the Caribbean Fisheries Management Council, with the support of local fishermen, to recommend the Red Hind Bank as a permanent ‘Marine Conservation District’ (MCD). In December 1999 the Red Hind Bank MCD was established as the first no-take fishery reserve in the USVI, and protected 41 km² of deep coral reefs (33 to 45 m) along the southern shelf of the insular platform. The creation of the MCD, which represents approximately 1.5% of the fishing grounds within the Virgin Islands (Bohnsack 2000), reflected a shift in management from a single-species approach (seasonal closure) to an ecosystem-level approach that protected not only key species of commercial importance but also provided protection of a large area of critical fish habitat (Allison et al. 1998).

Since these management measures were implemented, the red hind spawning aggregation has shown positive trends in several population characteristics. Beets & Friedlander (1999) first collected density data on this red hind spawning aggregation in 1997, 7 yr after seasonal closure. During the last 3 yr of the seasonal closure, from 1997 to 2000, the density of the spawning population increased by over 200% (4.7 to 15.0 fish 100 m⁻²) or about 66% yr⁻¹. Following the establishment of the MCD, density and biomass of red hind increased 60% on average, whereas peak spawning densities more than doubled during a 3 yr period (Years 2000 to 2003). These values were supported by the fish trap catch rates which more than doubled after the MCD was established. Annual fluctuations in density were also apparent. The density of red hind peaked in both 2001 and 2003 but declined in the intervening years 2002 and 2004 (Fig. 3). Olsen & LaPlace (1978) and Sylvester et al. (1978) recorded a similar phenomenon, whereby the St. Thomas red hind spawning aggregation showed high abundances based on catch rates in both 1975 and 1977 spawning seasons, extremely low abundance during the 1976 spawning season and moderate abundance in the 1978 season. Olsen & LaPlace (1978) suggested that these changes in abundance were the result of both fishing mortality and the relocation of the spawning aggregation due to heavy fishing pressure and possibly subsequent predation pressure by sharks. The drop in density in 2002 and 2004 also followed increased catch-and-release fishing activity from my research in 2001 and 2003, but diver surveys and catch rates verified that the primary site of the spawning aggregation still had the highest densities and did not shift to a different location. Alternatively, this pattern may suggest a biannual difference in spawning cohort strength (odd years being the strong cohort), a phenomenon that is well-documented for some species of Pacific salmon (Bond 1996). The density of red hind during these peak spawning seasons in 2001 (January = 23.8 fish 100 m⁻² and February = 28.9 fish 100 m⁻²) and 2003 (January = 39.72 fish 100 m⁻²) were the highest densities ever documented for a red hind spawning aggregation in the Caribbean. The average density of spawning red hind over the entire spawning area was 11.88, 14.91, 10.00, 27.08 and 19.31 red hind 100 m⁻² for January 2000, 2001, 2002, 2003 and 2004, respectively. In 1984, Shapiro et al. (1993) recorded a peak density of 7.6 fish 100 m⁻² with a mean of 3.8 fish 100 m⁻² from a small red hind aggregation in SW Puerto Rico. The mean value for the Puerto Rico site is similar to the 4.7 fish 100 m⁻² reported from the St. Thomas MCD in 1997 (Beets & Friedlander 1999). However, the average density from the unprotected spawning aggregation in Puerto Rico dropped to 0.88 fish 100 m⁻² 2 yr later (Shapiro et al. 1993), whereas the average density of the St. Thomas MCD had increased to 11.88 fish 100 m⁻² 3 yr later. This suggests that the heavily overfished St. Thomas spawning population was still in a state of recovery in 1997 and that continued protection from fishing mortality had been extremely beneficial to the population.

During the last 3 yr of seasonal closure, from 1997 (Beets & Friedlander 1999) to 2000, the average length of the spawning population showed a significant increase from 36.6 to 38.8 cm, or about 0.73 cm yr⁻¹. Although Beets & Friedlander (1999) used traps with smaller mesh (3.8 cm² vs. 5.1 cm²), it probably did not influence the results, since red hind caught in both studies were all greater than 25 cm in total length. Most red hind smaller than 25 cm are not yet reproductively active (Sadovy et al. 1992) and would not have entered the spawning aggregation. In the years following the MCD closure, the average size of red hind actually decreased by 0.9 cm (from 38.8 to 37.9 cm) relative to the first year of sampling (Fig. 5). The decrease in average fish length may have been an artifact of sampling or a real change in the spawning population. Fish collected by hand line were 0.8 cm larger than fish caught with traps. Since the proportion of red hind caught by hand line decreased from 78.5% in 2000 to 11.5% in 2003 (Table 1) this size-related gear bias may have contributed to the 0.9 cm decline in average fish length during this period (Fig. 5). Alternatively, the decrease in fish length could have been effected by recruitment of small young females into the spawning population in 2003 (Fig. 8). A final alternative is that both gear bias and recruitment could have contributed to the slight decline in fish size from 2000 to 2003.

Beets & Friedlander (1999) calculated that the area utilized by the red hind aggregation in 1997 was between 0.1 to 0.24 km², the latter being comparable to the area calculated by the surveys in January 2000 and 2001 (0.24 km²). Based on these calculations, total spawning population size ranged between 4700 to 11 280 fish in 1997 compared to 26 229 red hind in 2000, 38 143 in 2001 and an astonishing 84 000 in 2003. The dramatic increase in the estimated population size of the red hind aggregation in 2003 resulted from both a westward expansion of the spawning aggregation and an increase in red hind density throughout this area. Prior to this study, most red hind spawning aggregations were thought to be small, ranging in size from 750 to 3000 fish (Shapiro 1987, Shapiro et al. 1993, Levin & Grimes 2002) and occupying a spawning area of 0.01 km². These early estimates were based on heavily fished aggregations in Puerto Rico. The population size estimates documented for the marine protected area in St. Thomas far exceed these values and begin to rival species such as Nassau grouper, for which up to 30 000 individuals have been reported in a single aggregation (Smith 1972).

One explanation for the dramatic increase in red hind density after establishment of the MCD is that the efficiency of the fishery to catch red hind had been substantially decreased. Prior to the year-round closure in December 1999, fishermen could begin fishing within the MCD immediately following the closed spawning season which lasted from December through February. Based on the telemetry data, fish departing the spawning site most probably follow the relatively narrow (<200 m) coral reef ridges to the west and east, which afford groupers shelter from predation, before dispersing to their home sites. Strategic placement of traps along these migratory pathways may have had a significant impact on the spawning population as they departed the spawning site (Johannes 1981). Once fish dispersed from the spawning aggregation, the efficiency of fishing gear to capture large numbers of red hind was reduced, resulting in greater escapement from the commercial fishery. The year-round closure and the relatively large size of the MCD eliminated a potential fishing mortality bottleneck by allowing red hind to depart the aggregation in relative safety before dispersing to areas outside the reserve boundaries. Based on the tag-recapture data, the majority of red hind traveled about 15 km northwest to a rocky reef area around Sail Rock, St. Thomas (Fig. 1). Other fish were recaptured from 6 km to at least 33 km from the aggregation site, creating a source population area of at least 500 km². These migration distances are comparable, if slightly higher, than those reported for red hind in SW Puerto Rico which dispersed 10 to 18 km from the spawning aggregation (Colin et al. 1987, Sadovy et al. 1992).

Another alternative is that the spawning aggregation may be composed largely of fish resident in the closed area, which now offers continued protection of red hind that remain on the shelf-edge reefs. Several studies in Puerto Rico found that red hind females migrate to shallower inshore areas, while males remain on the deeper offshore reefs (Shapiro 1987, Sadovy et al. 1994b). Commercial fishing on the deep offshore reefs after the seasonal closure ended may have had a proportionally greater impact on male red hind relative to females, which dispersed over wider areas. However, Nemeth & Quandt (2004) found that, between the months of March and September, red hind densities on coral reef sites within the MCD (n = 8) were lower than at non-MCD (n = 8) sites (0.24 vs. 0.42 red hind 100 m², respectively). At this time it is unknown what proportion of the spawning population remains in non-coral reef habitats within the boundaries of the MCD. However, it is interesting that many tagged red hind were caught in a coral reef area within 6 km of the northwestern edge of the MCD. Of these fish, 3 were recaptured only 1.5 km outside the northwest corner of the MCD. This coral reef area extends into the MCD and may provide suitable habitat for red hind departing the spawning aggregation.

A final alternative to explain the significant increase in density, especially in 2003, is that a large cohort of young females recruited into the spawning population (Fig. 8). Sadovy et al. (1992) estimated that red hind from the St. Thomas region can grow to nearly 20 cm within 12 to 15 mo post-settlement and that up to 50% of red hind females within a population can reach sexual maturity within 3 yr. Growth rates in this study (1.2 to 4.8 cm yr⁻¹) were similar to rates for red hind in Puerto Rico (1.2 to 9.6 cm yr⁻¹, Sadovy et al. 1992). A cohort of young females could theoretically have been the result of increased reproductive output of the St. Thomas red hind aggregation during the Year 2000 spawning season. The larger size and number of red hind within this spawning population represents a substantial increase in fecundity over previous years. The estimated egg production for red hind females at 36 cm (i.e. mean size of females in St. Thomas) could produce over 500 000 eggs female⁻¹, and older, larger females that reach 40 cm in length can produce over 1 000 000 eggs (Olsen & LaPlace 1978, Thompson & Munro 1978, Sadovy et al. 1992, Whiteman et al. 2005). With the greatly increased reproductive output of females, subsequent larval recruitment and rapid growth rates of juveniles, one could expect larger cohorts of young females to enter the St. Thomas spawning aggregation in future years if self-recruiting occurs. Substantial increases in reproductive output is a major benefit of protected spawning populations of fish and invertebrates (Bohnsack 1992, Palsson & Pacunski 1995, Kelly et al. 2000, Roberts et al. 2001, Gell & Roberts 2003, Willis et al. 2003).

Protection of the St. Thomas red hind spawning aggregation seems to have had positive effects on the red hind population around St. Thomas. Based on a review of the literature and biostatistical data from port landings, the average length of red hind from the commercial catch has steadily increased and tracked the average length of the spawning population (Fig. 5). The lengths of red hind from commercial landings were typically smaller than catches from the spawning aggregation, since the commercial catch includes subadult fish from inshore waters which tend to be smaller (Olsen & LaPlace 1978, Shapiro et al. 1993). The predominant factor affecting the size and abundance of groupers among diverse areas in the Caribbean is fishing pressure (Sluka et al. 1997, Chiappone et al. 2000). Thompson & Munro (1978) reported that the mean size of red hind in intensely fished nearshore areas of Jamaica versus offshore oceanic banks was 26 and 33 cm TL, respectively. With a reduction in fishing pressure of the red hind spawning aggregation in St. Thomas, the average size of red hind at the spawning aggregation steadily increased from a low of 29.5 cm in 1988 (Beets & Friedlander 1999) to nearly 39 cm 12 yr later (this study, Fig. 5). A concurrent increase in length of the red hind population outside the aggregation was clearly evident and increased significantly after the MCD was established (Fig. 5). Interviews with commercial and recreational fishermen around St. Thomas by the author during the past several years highlighted a general perception that the red hind being caught now are larger than before the MCD was established.

The results reported in this paper indicate that seasonal protection of the red hind spawning aggregation allowed the spawning population to rebound relatively rapidly from overfishing in terms of size, density and sex ratios. Permanent protection of large areas surrounding the spawning habitat provided additional benefits toward increasing spawning stock density and biomass as well as maintaining sex ratios between 3 and 5 females per male (Whiteman et al. 2005). Other factors which may have contributed to these changes include change in fishing effort or gear and the implementation of other fishery regulations. The number of licensed commercial fishermen in the Virgin Islands has been stable for over 15 yr (Tobias 1997, B. Kojis pers. comm.), whereas effort in trap-fishing doubled in St. Thomas from 1985 to 1996 (unpubl. data from NMFS biostatistical database). This increase in effort has apparently not influenced the red hind population. Between 1997 and 1999 fish traps with 3.8 cm² (1.5 inch²) square mesh were phased-out in St. Thomas (but not St. Croix) and replaced by traps with 5.1 cm² (2.0 inch²) square mesh. This change may have increased escapement of smaller red hind, but the effect on the larger sized fish comprising the spawning population was probably minor, as evidenced by the lack of difference in minimum-sized fish caught by traps used in Beets & Friedlander (1999) and this study. St. Croix also has a red hind spawning aggregation that has been seasonally protected since 1995. The sizes of red hind in the spawning aggregation and in the commercial catch have been declining and are considerably smaller (32.3 and 27.6 cm, respectively) than red hind in the St. Thomas region (Nemeth unpubl. data). These factors suggest that the establishment of the MCD has been the primary stimulant for maintaining and improving the St. Thomas red hind spawning population, a finding which corroborates many studies on the benefits of using marine fishery reserves (MFR) as a management strategy (Pauly 1979, Roberts & Polunin 1991, 1993, Russ 1991, Roberts 1995, Bohnsack 1996, Gell & Roberts 2003).

Because red hind spawn in smaller social groups (3 to 5 fish⁻¹ group) than the large social groups of 1000s to 10 000s of fish formed by other species like Nassau groupers Epinephelus striatus (Smith 1972, Olsen & LaPlace 1978), it is likely that red hind spawning populations are impacted less by short-term fishing pressure (Colin et al. 1987) and may show more rapid recovery once fishing is reduced. After the collapse of the Nassau grouper fishery in Virgin Islands (Olsen & LaPlace 1978) the red hind became the dominant grouper in the local fishery (Cummings et al. 1997). The change in catch composition from larger to smaller individuals and/or larger species being replaced by smaller species is well-documented (Luckhurst 1996, Chiappone et al. 2000). While Nassau grouper reach 850 to 950 mm (Olsen & LaPlace 1978, Colin et al. 1987, Colin 1992), red hind reach maximum lengths around 500 to 550 mm (Olsen & LaPlace 1978, Thompson & Munro 1978, Colin et al. 1987, Sadovy et al. 1992), although specimens from 620 to 720 mm have been recorded (Smith 1971, Randall 1983, Luckhurst et al. 1992). Whether the Nassau grouper will be able to reclaim its historical spawning site within the MCD (Olsen & LaPlace 1978) will require long-term monitoring efforts.

Other behavioral aspects of fish within spawning aggregations may also influence effects of differential fishing mortality. For example, males of many grouper species, including red hind, remain higher in the water column defending spawning territories or displaying to potential mates (Colin et al. 1987, Gillmore & Jones 1992). Sex and/or size-selective fishing mortality in spawning aggregations will occur when these more behaviorally dominant males take baited hooks more frequently than females (Gillmore & Jones 1992, Levin & Grimes 2002). Moreover, Levin & Grimes (2002) suggested that sex-changing female groupers of exploited populations may adopt stereotypical male behavior during the spawning season, making them more vulnerable to fishing and further disrupting reproduction.

Another example of the influence of behavior includes gender-biased small-scale movement patterns of aggregating groupers during the spawning season. My data suggest that male red hind arrive early at the spawning aggregation site (i.e. December) and stay on-site between spawning peaks. Thus, short-term seasonal closures, from 1 to 2 mo, that protect only the primary spawning month may make a large portion of the spawning population, especially males, vulnerable to fishing mortality. Between spawning peaks, a substantial portion (50 to 80%) of red hind disperses short distances (at least 100 m) into adjacent habitats (see Fig. 9). Size-frequency analysis suggests that most of these fish are probably females (fish < 40 cm TL). However, it is unknown what proportion of these fish seen in adjacent habitats were from the same group of spawning individuals that dispersed temporarily between full moon spawning events versus new arrivals waiting for the next full moon spawning event. If red hind and other larger grouper species disperse considerable distances between spawning peaks, then the size and placement of MPA boundaries may not provide sufficient protection from fishing if fish disperse beyond MPA boundaries during the spawning season. These findings suggest that the design of marine fishery reserves must take into account not only critical fish habitats but also the important life-history attributes that may exacerbate fishing mortality effects on protogynous species.