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Gag grouper and sex change: how spatial management and life history traits affect male abundance

This article is a summary of the following publication:

Lowerre-Barbieri S, Menendez H, Bickford J, Switzer TS, Barbieri L, Koenig C (2020) Testing assumptions about sex change and spatial management in the protogynous gag grouper, Mycteroperca microlepis. Mar Ecol Prog Ser 639:199-214. https://doi.org/10.3354/meps13273

Article Highlights

  • In this study, we integrated large spatial-scale data with high-resolution data from a 3-year targeted study sampling gag at deep-water sites with varying spatial management (a marine protected area [MPA], a seasonally closed area, and an ‘Open area’).
  • Gag exhibited complex spatial ecology; females formed pre-spawning aggregations before migrating to deep-water spawning sites, which overlapped with locations where males were sampled year-round.
  • In the targeted study, the observed male sex ratio was 5% (in the MPA) compared to the expected 15%, and it was 0% in less protected areas (The Edges [seasonally closed] and an ‘Open area’) during spawning season.
  • Sex change occurred in only 0.48% of the samples taken, occasionally in small fish and before, during, and after the spawning season. In addition, sex change was observed in pre-spawning female-only aggregations as well on the spawning grounds, indicating male social cues are not requisite.
  • Our results indicate that overall gag abundance is low, MPAs do not protect all recruiting males (as previously assumed), and current regulations are not sufficient for the male population to recover to historic levels (~17% male).

Their research was published in the April 2020 issue of the scientific journal Marine Ecology Progress Series and is summarized below with the full content available through the FWRI library:

Testing assumptions about sex change and spatial management in the protogynous gag grouper, Mycteroperca microlepis

Introduction

Gag grouper (Mycteroperca microlepis) are an iconic Florida fish that may be in trouble. All fish begin as females in estuarine nursery grounds, but as they age gag move further offshore, with the oldest, largest fish turning into males. The gag’s unique life history and spatial ecology pattern makes it difficult to understand the best way to measure stock productivity based off reproductive parameters. Based on females-only, the last stock assessment in 2014 found gag to not be over-fished or undergoing over-fishing. But the same assessment predicted only ~ 2-3% of the population was male. Since then, commercial fishermen have not been meeting quota, leaving fishermen and scientists concerned that this stock may not be as healthy as assumed.

We conducted sampling primarily during gag spawning season, December to May, from 2015 to 2018 in three areas off the Florida Panhandle: (1) Madison Swanson, a marine protected area (MPA), closed all year round to bottom fishing; (2) The Edges, open half the year to fishing; and (3) an Open area (Figure 1). We integrated our directed sampling data with gag data from FWRI programs Fisheries Independent Monitoring and Fisheries Dependent Monitoring and also from Captain Ed Walker, a local commercial fisherman, who kept a portion of his catch for biological sampling prior to their sale. A large, integrated data set gave more power to test the following hypothesis about where and when sex change occurs and the effectiveness of spawning reserves to protect male gag.

Hypotheses

  • Females form pre-spawning aggregations in December, January, and February and then undergo spawning migrations to deep-water spawning aggregation sites, where males remain year-round and females move only to spawn.
  • Male abundance and male sex ratios will have increased since the 1990s, and within the MPA the male sex ratio will be ~15% based on the predicted efficacy of this management measure.
  • Sex change occurs only on the spawning grounds and is cued by a fish’s internal clock or occurs above a minimum size threshold, 800 mm/31.5 in total length (TL) and is cued by male sex ratios on the spawning grounds.

Results

The integrated data set was made up of 1,657 gag and included location and depth sampled for all but the samples from FDM (Figure 2).  Fish were sampled along the west coast of Florida from depths ranging from 5-122 meters/16-400 feet.  Gonadal tissue was assessed histologically for sex and reproductive development. Histology is the science of producing stained sections of preserved tissue on glass slides that can be examined under a microscope.

 

Spatial ecology, how fish were distributed over space
We hypothesized that female gag would form pre-spawning aggregations prior to migrating to deep-water spawning sites, where males remain year-round. Our results supported these hypotheses and showed that gag exhibit clear depth preferences with life stage, sex, and spawning (Figure 3). However, we did not find strong evidence of spawning aggregations, nor that all females leave deep-water spawning sites after the spawning season.

While behavior and migrations associated with spawning accompanied by changes in reproductive organs (gonads) in gag extends from December through May, we found that actual spawning only occurred at our study sites from February 1st through April 18th. Males and females were found at deep-water sites. Although previous gag research reported spawning aggregations of 50-100 fish dating from 1977-1997, this study did not see large numbers of gag on video data nor have large catches (maximum caught during the spawning season in the MPA was 17 gag). Sex-specific movement was evident based on the depths at which fish were captured as average depth at capture differed significantly with sex (Figure 4). Females displayed a minimum capture depth of 4.6 meters/15 feet whereas males started at 49.1 meters/161 feet. Pre-spawning aggregating behavior consistently occurred at the shallow sites that Captain Ed Walker targeted, where he captured fish in November and as late as mid-February. The maximum catch per day at these shallower sites was ~100 fish, and of the 21 fish sampled, 100% of those were female, and 50% had developing or spawning capable ovaries (ramping up to spawn).

Immature females, fish that had never spawned and were not mature enough to spawn at the time of capture, ranged from 1-4 years old and occurred in shallower waters compared to other reproductive phases (Figure 5). Developing females, fish which had received the signal to begin gonadal development for the upcoming spawning season, were as young as 2 years old and sampled over a wide range of depths. Spawning capable females ranged from 3 to 15 years old. Regenerating females, fish that had spawned previously but were not spawning any more this season or skipped spawning that season, had the widest range of ages (2-17 years old). The assumption that females migrate to deep-water spawning sites was supported by the presence of only mature females at these sites, as well as increased abundance during the spawning season (Figure 6). However, not all females left the spawning site after the spawning season ended. Females captured outside of the spawning season during opportunistic sampling – conducted in June, July, October, and November – in these deep-water sites ranged in age from 2 to 10 years old with an average age of 5 years old.

Sex ratio
We hypothesized within the MPA, that male abundance would have increased to 15%, as indicated by previous modelling efforts. We also hypothesized that the age at 50% male (A50) would increase in this protected environment and thus be greater than that seen in the 1990’s (10.9 years).

For all months with samples taken in the Madison Swanson MPA (December to May) there was an 11% male sex ratio.  However, during the spawning season sex ratios were only 5% male. During spawning season is when most mature males and females are in the same location, so a 5% male sex ratio is what we concluded to be a more accurate representation of the population compared to outside of the spawning season, when some females migrate back to shallower water. During the spawning season we had 0% male in the Edges (seasonally closed) as well as our Open area. Outside the spawning season only 1 male was captured at each of these locations. Although we do not have the data to estimate the optimal gag male sex ratio, several lines of evidence suggest that the current low male sex ratio (5% within the MPA and 0% in the Edges and Open area) is of concern.

We found an A50 of 13 years in Madison Swanson. This suggests the male population in the MPA may be aging with limited recent recruitment of younger males rather than indicating a recovering stock, highlighting our need to better assess male recruitment and the processes driving it. The mating function (relationship between sex ratio and fertilization success) plays an important role in the productivity of protogynous species (fish that begin life as females and transition to males) but is poorly understood. Males displayed low milt (sperm) reserves during the spawning season which is a pattern associated with pair spawners. Because gag are pair spawners and female gag are multiple batch spawners (meaning they produce multiple batches of eggs throughout the spawning season), males would have to spawn with multiple females per day, every day of the ~78-day spawning season. Although male spawning frequencies are unknown, given the low milt reserve gag displayed, this seems unlikely to be accomplished.

With the current low observed sex ratios being close to those seen in the 1990s when gag were considered overfished and undergoing overfishing, the above evidence suggests that male abundance is well below what would be expected in a healthy stock.

Sex Change
To answer if sex change in gag grouper is cued by male sex ratios on the spawning grounds and if there is a minimum size threshold that gag must reach to receive the signal to change sex we examined the occurrence and timing of transition Transitioning fish were very rare – 0.48% of the total samples – and observed from December through May. If the duration of gag sex change (i.e. the time it takes to become a functional male after receiving the cue to change sex) is similar to that of rock hind or black sea bass, approximately 2 months, then if female gag do not receive their sex change cue by December or January, which is when the females form pre-spawning aggregations, they will not be able to contribute as males in the upcoming spawning season, February through April. Male sex ratios are not a requisite cue for sex change, based on our observations that transitionals occur before, during, and after the spawning season and at both all-female pre-spawning aggregation sites and on the spawning grounds. These findings contradict the assumption that sex change occurs only on the spawning grounds and that spawning reserve MPAs will thus protect male recruitment.  However, further research is needed to fully understand the proportion of fish transitioning prior to arriving on the spawning grounds. 

Sex change was not associated with a minimum size, although males (average TL=1034 mm/40.7 inches) were significantly larger than females (average TL=793mm/31.2 inches) (Figure 7). Males had a larger average TL in the MPA compared to other areas, and the size and age of the transitional sampled in the MPA (14 years and 1107 mm/43.6 inches) was considerably larger and older than observed in the seasonally closed area (6 years old and 845mm/33.3 inches). Sex-specific ages overlapped, with the youngest male being 7 years old and the oldest female aged 17 years. Our results of males and transitionals smaller than 800 mm indicates there is not a minimum size threshold for a gag to change sex. The actual cue which initiates sex change remains unknown. However, the range in sizes and the processes seen in other species suggest that there is a social context to the cue.

We propose a new conceptual model for gag sex change: Presumably, the largest, most aggressive females in a pre-spawning aggregation will transition. On the spawning grounds these female-to-female interactions will be moderated by male abundance and size dominance. However, when male abundance is low, female-to-female interactions will be less influenced by males and/or spawning and result in higher numbers of transitionals both during and after the spawning season on the spawning grounds.

Conclusions

In gag grouper, the spatial distribution of their life cycle, their gender system, and their mating strategy impacts sex change, male recruitment, and the spatio-temporal level of fishing mortality they can sustain.

Given that both gag populations and fishing pressure is greatest in shallow waters, we hypothesize that shallow-water, pre-spawning aggregations are a key spatio-temporal bottleneck to gag productivity because of the potential to remove both fish undergoing transition and females cued to change (but without identifiable gonad restructuring) before they can contribute to gag productivity as males on the spawning grounds.

Gag have an especially complex lifecycle, with the two sexes exhibiting different size and spatial distributions, and this appears to have contributed to the low observed male sex ratios. The very low levels of males seen in this study suggests that all eggs may not get fertilized, decreasing the stocks productivity. This low male abundance and low catches, even in the MPA, suggest gag grouper in Florida may be in trouble. 

Figures

Figure 1

Distribution of gag Mycteroperca microlepis samples with location data by data source: (1) targeted study sites (teal squares, A, B) sampled from December through May; (2) samples from the fisheries-independent reef survey (blue triangles) and (3) samples from a Ed Walker a collaborative fisherman (C). Insets include sampling zones in (A) Madison Swanson and (B) the Edges. Note that comparable spatial information was not available for fisheries-dependent samples collected.

Figure 2

Pie chart showing the four sources of biological samples for this study.

The four sources of gag biological samples: (1) 3-year targeted study (blue, 37.5%), (2) FIM (orange, 21%), (3) FDM (gray, 37.9%) and (4) Ed Walker a collaborative fisherman (yellow, 3.5%).

Figure 3

Conceptual model of the spatial ecology of gag. The model shows pelagic gag larvae drift inshore and settle out in estuarine seagrass beds as nursery habitat where they continue to grow into juveniles from 5-7 months old and then move to nearshore hard bottom (in about 22 meters depth) as immature females, typically between 1-4 years old). As female gag mature, they begin to move offshore (in depths ranging from 15 to 121 meters) and form pre-spawning aggregations from November to February and most females migrate further offshore to the shelf in depths greater than 50 meters during spawning season (February-March) where males are thought to remain all year. Seasonal information is in parentheses, y=years, mths=months.

Model showing distribution of male and female gag grouper throughout the estuary, inshore and offshore.

Figure 4

Spatial distribution of gag samples used in this study by (A) females and (B) males. Red triangles denote fish sampled in the spawning season (1 February through 18 April), and black diamonds are fish sampled outside that time period. Green circles denote actively spawning females and the 10, 30, and 50 m depth contours are noted.

Two maps of Florida and Gulf of Mexico showing distribution of males and females during spawning season and outside of spawning season.

Figure 5

Chart showing reproductive phases and depth of capture of female gag in this study.

Depth of female gag at capture by reproductive phase from fishery independent sampling (i.e. 3 year study and survey). Immature females were found in depths below 50 meters whereas developing females had a larger depth range of 20 to 100 meters. Fully-yolked females were found in depths of 20 to 125 meters and active spawning took place in a smaller depth range of 70 to 100 meters. Regressing females occurred 70 to 125 meters and regenerating or resting females ranged from 10 to 130 meters. ‘Fully-yolked’ corresponds to spawning capable and ‘spawning’ designates active spawners. Boxes represent the 25th to 75th quantiles, and whiskers are the range. Diamonds represent the means, and horizontal lines are the medians. Those groups which significantly differed from each other, based on the Dwass, Steel, Critchlow-Fligner method, are indicated by different letters

Figure 6

Bar graphs showing that during the spawning season there was an increase in female abundance in depths greater than 40 meters compared to outside of spawning season.

Bar graphs showing that during the spawning season there was an increase in female abundance in depths greater than 40 meters compared to outside of spawning season, supporting the  hypothesis that females undergo spawning migrations to deep-water spawning aggregation sites. Sex-specific percentages of gag by depth bin and spawning season (red: males, blue: females) for all sampling areas. (A) Sampled during the spawning season from 1 February through 18 April; (B) sampled outside this time period. Sample sizes for each 20 m depth bin and season are noted above each bar

Figure 7

Bar graph showing that males were significantly larger than females.

Size distribution of gag by sex compared to expected normal (blue) and kernel (red) distributions. Although size approximated the normal distribution, it did not pass the Wilcoxon Mann-Whitney test, and differences were tested with non-parametric statistics. In the boxplots, mean is denoted by a diamond and median with a vertical line. The ends of the boxes represent the 25th and 75th percentiles, whiskers represent expected range, and dots show data points outside of this range