Length-Based Spawning Potential Ratio (LB-SPR) for Red Grouper ( Epinephelus morio ) and Associated Species in the Commercial Fishery of the Yucatan Peninsula, Mexico

,


Introduction
Te reproductive output, i.e., the production of viable eggs, and subsequent recruitment processes, which are subject to environmental factors, leading to natural fuctuations in marine populations over time and space, constitutes crucial components in the dynamics of marine populations [1,2].Such fuctuations result from changes in both biotic and abiotic factors that afect growth and mortality rates during early life stages [2].
In marine populations, the frequency and timing of ofspring release are determined by temporal reproductive patterns, which exhibit high variability in marine fshes and play a crucial role in their reproductive success throughout their lifespan [3].Te reproductive biology of a species has a profound impact on its productivity and, consequently, its ability to withstand exploitation or any human disturbance [4].Te reproductive process is essential for ensuring the sustainability of fsheries, highlighting the importance of evaluating and managing marine fsheries to protect and conserve the spawning populations of specifc stocks [5].Terefore, it is of paramount importance to quantify productivity in relation to reproductive potential (RP) and recruitment [4].
Stock depletion, caused by overfshing of recruitment, results in a decline in marine populations, leading to signifcant economic losses [6][7][8].Furthermore, the increased fshing pressure on larger and older individuals, crucial for reproductive output, exacerbates the adverse impacts of overfshing [9,10].
Currently, over ffty percent of marine fsh stocks are actively being exploited up to their maximum sustainable yield, with approximately one-third of these stocks already experiencing overexploitation [8,11].Tis concerning trend is particularly evident in Mexican fshery resources, where more than a quarter of them are overfshed [12].Among these resources is the red grouper stock (Epinephelus morio, Epinephelidae) [13,14], and its associated species [15], which are the primary targets of the red grouper fshery-the largest commercial fshery in the Yucatan region [16,17].
Stock assessment is a complex and costly process [18,19].In fsheries where stock dynamics have not been evaluated, the negative efects of overfshing may not be immediately apparent.As a result, there is an imminent risk of collapse before these issues are recognized [8,10,18,20].
Small-scale or artisanal fsheries, distinguished by the use of traditional manual techniques, small vessels in shallow coastal waters, and relatively modest individual catches [21,22], encounter challenges in data collection, particularly regarding age data, due to limited resources and expertise.As a result, researchers and managers heavily depend on length composition data [23].Efectively assessing and managing them is a complex and challenging task, particularly when using traditional fshing models [12,24,25].Hence, assessment methods and management procedures must optimize the use of the limited data available to account for signifcant uncertainties [20].
Length-based methods have been developed for populations with limited data, which help assess stock status and provide valuable management information, including reference points like fsh growth and mortality rates.Tese methods enhance our understanding of fsh population dynamics [23,26,27].In this context, the length-based spawning potential ratio method (LB-SPR), an equilibrium-based model developed for assessing spawning potential in fsheries with limited data [18,19], represents a valuable tool with implications for the sustainable management of small-scale fsheries.
Te Spawning Potential Ratio (SPR) of a fsh stock represents the portion of unfshed reproductive capacity that remains under specifc levels of fshing pressure [23,[28][29][30].It helps predict whether a population will decline, remain stable, or increase based on its ability to sustain itself [31].
Spawning Potential Ratio (SPR) is widely recognized for its signifcance in the feld of sustainable fsheries management, as it plays a pivotal role in informing decisionmaking and conservation eforts.Tis metric is particularly relevant in the context of data-poor fsheries, providing valuable insights into the impact of fshing activities on stock productivity [23,28].Terefore, the aim of this study is to assess the Length-Based Spawning Potential Ratio (LB-SPR) of seven marine fsh species captured in the artisanal red grouper fshery in the Yucatan Peninsula.
Te red grouper fshery, which targets E. morio within the grouper-snapper complex, has signifcantly contributed to the growth and development of the Yucatan fshing industry since the 1970s, thanks to the substantial production and economic value of E. morio [16,17,25,34,35].Nevertheless, the depletion of red grouper biomass due to overfshing has precipitated the collapse of the fshery, leading to a reduction in its overall productivity [12,36].
In the Campeche Bank, the small-scale fshing feet employs various fshing methods, including handline, longline, nets, speargun, harpoon diving, and trolling with rod and lure [17].Te species targeted in the commercial red grouper fshery are primarily caught using bottom longline and handline methods that involve hooks and bait of various types and sizes [17,34,45].
Te handline, or cord, consists of a main line known as "reinal," carrying one to three straight hooks (size 7 to 10), either short or long-shanked.Monoflament thread (size 60 to 90) is used, accompanied by a lead weight to sink the bait quickly [17].Te bottom longlines typically consist of a mainline, gangions with hooks, buoyancy aids, and lead weights, operated anchored to the bottom using heavy objects as ballast, and can be manually or hydraulically retrieved [17,35,45].Te gear operates in the sea, fxed to the bottom at varying depths, with each longline carrying 150 to 500 curved hooks, also known as "guachinanguero" or "eagle claw" [17].

Growth Pattern
2.2.1.Groupers.Tose fsh are long-lived, slow-growing fsh that reach sizes greater than 100 cm and can live more than 20 years [46].In the CB region, groupers exhibit slow growth characterized by growth stanzas, distinct growth stages marked by abrupt changes in growth rate, due to variations in their ontogenetic development [47,48].Groupers in this 2 Journal of Applied Ichthyology  Yellowtail snapper (O.chrysurus) exhibits rapid growth during the frst two years, followed by a decline around the fve-year mark, and eventually stabilize over the next nine years, reaching lengths of up to 84 cm [50,53,54,[56][57][58][59].Gear selectivity and exploitation levels can impact growth rates, reducing the abundance of larger-sized fsh [50,54,56].In southern and southeastern regions of the GoM, the growth pattern exhibits negative allometry (b < 3) [48,60].Along the coasts of Veracruz, individuals can reach sizes of up to 60 cm [60].In the CB region, individuals grow slowly attaining sizes of up to 54 cm and a lifespan of up to 15 years [41,48,61].
Lane snapper (L.synagris) exhibit geographical and sexual diferences in their growth patterns.Growth pattern is characterized by growth stanzas, with rapid grow during the frst year but gradually slows down in the second year.Subsequently, growth progressively decreases each year until it reaches nearly asymptotic values at around age 9 [55].Generally, males display a faster growth rate and achieve larger sizes than females [51,52].In the western Atlantic Ocean individuals can reach sizes of up to 38 cm and have a lifespan of 19 years [55].Along the northern Gulf of Mexico and the coasts of Florida larger lane snappers can reach sizes of up to 51.2 cm [51].In the Caribbean populations individuals can reach sizes up to 71 cm, often showing an allometric negative growth pattern, and a lifespan of 14 years [52,[62][63][64].In CB region, individuals reach size up to 43 cm, females typically being larger than males [65].
2.2.3.Associated Species.Hogfsh (L.maximus) can grow to sizes of up to 84 cm and have a lifespan of up to 19 years [42,66].In the eastern Gulf of Mexico, they exhibit a bathymetric distribution pattern associated with size and age, likely infuenced by high fshing pressure nearshore (<30 m), where smaller individuals are more commonly found [66].In CB region, growth is also appearing to be infuenced by fshing pressure [67].Te pattern growth is allometric negative (b < 3).Individual can reach sizes up to 54 cm [48,67,68].
White grunt (H.plumierii) grows following a determinate (i.e., asymptotic) or indeterminate growth pattern [69,70].Individuals can reach sizes up to 41 cm and have a lifespan of up to 18 years [39,70,71].Typically, males exhibit larger sizes than females [40,70].In CB region, individuals can attain sizes of up to 40 cm and a potential lifespan of up to 17 years [39].

Reproductive Strategies.
Reproductive traits, such as size and age at maturity, sex ratio, fecundity, spawning time, and duration, display signifcant phenotypic plasticity across various fsh populations.Terefore, it is essential to understand the specifc reproductive strategies of each population.Tis knowledge is crucial for establishing local guidelines on sustainable fshing mortality thresholds, which may include measures such as closed areas and seasons, as well as enforcing minimum landing size regulations [4].
Te red grouper reproduces seasonally, with peak spawning occurring in late winter and early spring (January-March) [72].Females reach sexual maturity (50% maturity level, L 50 ) at a length of 50.9 cm fork length (FL), and sexual inversion or sex change typically occurs at a mean size of 59.7 cm FL [72].Te current fecundity pattern is unknown, and it is unclear whether it follows a determinate or indeterminate type [76].
Regarding the black grouper, mature females can be found from October to June, with a peak spawning period occurring from January to February [73].Females reach sexual maturity (L 50 ) at a length of 72.1 cm FL and sexual inversion typically occurs at an average size of 103.3 cm FL [73].
Gag groupers spawn from December to March, with the highest spawning activity observed between January and March [74].Females reach maturity (L 50 ) at 72.1 cm FL and sexual inversion occurs at 103 cm FL.Finally, spawning aggregation behavior is commonly observed in black grouper populations across various regions, including the Gulf of Mexico, the Caribbean Sea, and Bermuda.Similar behavior is also documented in gag grouper populations along the continental shelf on both the east and west coasts of Florida [73,74,[77][78][79]. [80].In the CB region, exhibit the reproductive strategy typical of continental populations.Te yellowtail snapper (O.chrysurus) displays an extended spawning period, primarily occurring during spring and autumn [61].Individuals reach maturity at a small size (L min = 14 cm FL), with an L 50 of 21.3 cm FL for females.Tis snapper exhibits multiple spawning events synchronized with the new moon phase throughout the 9-month spawning season [61].Lane snapper (L.synagris) primarily reproduces between March and July, with spawning peaks occurring in May and July.Larger size classes (36.0 cm FL) are predominantly composed of females that reach maturity at an L min of 15 cm FL and an L 50 of 17.8 cm FL [65].Both snappers exhibit asynchronous development of oocytes and batch fecundity; the yellowtail snapper can produce up to 160,000 oocytes, while the lane snapper can produce up to 200,000 oocytes [61,65].

Associated Species.
Te hogfsh (L.maximus Labridae) is identifed as a monandric protogynous hermaphrodite [81].Nevertheless, the presence of ovotestes exhibiting internal morphology similar to ovaries in larger individuals raises the possibility of diandric hermaphroditism [82].Females' hogfsh are batch spawners; the mating exhibits a harem structure [81,83].Reproductive seasonality varies considerably across its geographical distribution.In the CB region, it exhibits the longest annual spawning period, spanning 11 months, with peak spawning events occurring between February and May [84].Females reach maturity at an L 50 of 15 cm FL , with an L min of 13.9 cm FL.Sexual inversion occurs within a size range of 21 to 40 cm FL, at a P 50 of 32 cm FL [84].Oocyte development and batch spawning follow an asynchronous pattern, characterized by a homogeneous distribution of oocyte stages [38].
Te white grunt (H.plumierii Haemulidae) is a Gonochoric species with no evident sexual dimorphism [40].Te reproductive pattern of the white grunt varies across different populations within its geographical distribution [40,85].In the CB region, this Haemulidae species reproduces annually for seven months, from February to August, with the peak spawning event occurring in May [40].Females reach maturity (L 50 ) at 15.22 cm total length (TL) and exhibit asynchronous oocyte development.Tey have indeterminate fecundity, capable of producing batches of up to 40,000 oocytes [40].

Study Area.
Te Campeche Bank region consists of a shallow submarine plain with a large extension and a small slope (maximum depth: 200 m), located between the Tabasco-Campeche Basin and the Yucatan Strait, between 18 °and 24 °north latitude and 87 °and 93 °north longitude (Figure 1).Tis zone is valuable as a fshing area due to the presence of high-value species [86,87].
Te total length (TL) of each specimen was measured in centimeters (cm).Moreover, data on each species' length at sexual maturity (L 50 ), which represents the length at which 50% of females become sexually mature for the frst time [72], as well as their von Bertalanfy maximum length (L ∞ ), growth rate (K), and natural mortality rate (M), were collected from scientifc literature (Table 1).

Length-Based SPR Model
Overview.When addressing recruitment overfshing in fsh populations with lower resilience, an SPR (Spawning Potential Ratio) of 0.4 is commonly recognized as an indicator for the Maximum Sustainable Yield (MSY) [90].Te minimum acceptable levels of SPR to ensure stocks maintain satisfactory productivity range from 0.20 to 0.30 [28].A drop below 0.20 in SPR indicates a risk of decline, particularly in juvenile fsh supply.When SPR falls below 0.10, populations may rapidly decline and even face local extinction [31].
Te length-based SPR assessment method evaluates the impact of harvesting on a population's reproductive capacity.In unexploited or unfshed fsh stocks, the natural SPR is 100% or 1.0, but fshing activities can reduce it to a specifc proportion of the unfshed level, represented as SPR X% or <1.0.Harvesting fsh before they reach sexual maturity results in a 0% SPR, signifcantly diminishing their ability to reproduce [18,22,31].
To estimate the spawning potential ratio (SPR) of a fsh population using size composition data from an exploited stock, the LB-SPR model relies on key parameters (Table 2).Tese parameters include fsh length data, size classes, the von Bertalanfy asymptotic length, the length at which 50% maturity (L 50 ) is reached, and the length at which 95% maturity (L 95 ) is attained.
Additionally, the model takes into account the ratio of natural mortality to the von Bertalanfy K coefcient, which is denoted as the M/K ratio.According to Hordyk et al. [23,91], the M/K ratio reveals less variability than natural mortality (M) across diferent stocks and species.It combines catch size composition with an estimate of local size at maturity to determine a population's ability to replenish itself after fshing [23,91].Furthermore, exploitation parameters are taken into account.Tese include the length at 50% selectivity (SL 50 ), the length at 95% selectivity (SL 95 ), and the F/M ratio [19,30,92].

SPR Analysis.
Te LB-SPR analysis was conducted for each species using the LB-SPR package [93] on the R Core Team [94] platform.Te R script by Hordyk [92], was confgured with the biological and exploitation parameters from Table 2. Te LB-SPR package's default confguration applies the growth-type-groups (GTG) methodology as proposed by Walters and Martell [29]; as cited in [30].
Te GTG LB-SPR model assumes established life history parameters and utilizes an equilibrium per-recruit model to determine relative fshing mortality, selectivity-at-length, and the spawning potential ratio based on representative catch-at-length data [30].Furthermore, the GTG-LB-SPR model incorporates variable M in terms of size and utilizes the life history ratio M/K.Tis is done in conjunction with assessments of size-at-maturity and asymptotic size (L ∞ ), along with length composition data.
Tis comprehensive approach is used to evaluate the spawning potential ratio (SPR) of data-limited stocks that exhibit size-dependent selectivity patterns, allowing for the consideration of Lee's phenomenon [30].

Fish Length.
Te length of the fsh exhibited variability (Figure 3; Table 3).Among the caught species, groupers (red grouper, black grouper, and gag grouper), were the largest fsh, spanning from 29.0 to 87.0 cm TL.
Gag grouper show of the largest average length at 54.3 cm TL, with an individual range of 31.0 to 87.0 cm TL (±13.06);black grouper followed with an average length of 52.83 cm TL, ranging from 25.0 to 85.0 cm TL (±10.28),Snappers (yellowtail and lane snapper) along with associated species (hogfsh and white grunt) displayed smaller sizes compared to groupers.Among them, yellowtail snapper shows of the largest length in average at 33.0 cm TL, ranging from 21.0 to 47.0 cm TL (±6.49).Following this, lane snapper measured 28.0 cm TL on average, with an individual range of 20.0 to 45.0 cm TL (±3.73).
Te associated species showed some degree of similarity in size to the snappers.Hogfsh, at an average length of 30.0 cm TL, exhibited the largest size range, spanning from 20.0 to 40.5 cm TL (±3.22).On the other hand, white grunt, with an average length of 26.9 cm TL, represented the smallest fsh in terms of average length, ranging from 18.1 to 34.0 cm TL (±3.00).For snappers, yellowtail snapper (SL 50 � 33.0 cm TL, L 50 � 21.3 cm FL) and lane snapper (SL 50 � 27.5 cm TL, L 50 � 17.8 cm FL); and associated species, hogfsh (SL 50 � 30.7 cm TL, L 50 � 15.0 cm FL) and white grunt   2 for details).the size selectivity pattern difered from that of groupers, as the SL 50 values exceeded the respective L 50 .Tis suggests that 50% of the caught fsh were mature or adult individuals.

Spawning Potential Ratio. Te Length-Based Spawning Potential Ratio (LB-SPR) analysis indicated variable
Spawning Potential Ratio (SPR) values for the species of the red grouper fshery and associated species that were analyzed (Figure 5).Among them, groupers exhibited the lowest values of SPR, all of them under the reference value (0.40).Te values registered ranged from 0.05 to 0.26, with gag grouper recorded the highest SPR value (0.26), although it was so close to the minimum critical value (i.e., 0.20).In the other hand, red grouper and black grouper, recorded values of SPR below the critical minimum (0.10 and 0.05, respectively).In the snapper group, yellowtail snapper (0.44) recorded a value just slightly above the reference value (0.40), whereas lane snapper (0.28) recorded the lowest SPR among this group, falling under the reference value.On the other hand, the associated species, hogfsh and white grunt, recorded the best overall values (0.72 and 0.98, respectively), surpassing the reference for SPR.

Fishing Pressure (F/M
) and Relative Yield.Te fshing pressure (F/M) and Relative Yield values difered among groupers, snappers, and associated species (Figure 6).Te LB-SPR analysis indicated that the F/M was high for red grouper (2.85) and black grouper (3.21) (Figures 6(a    Regarding snappers (Figures 6(d) and 6(e)), the F/M was lower for yellowtail snapper (1.80) but highest for lane snapper (6.60).In relation to Relative Yield, the analysis indicates that the yellowtail snapper has reached its maximum level.At this point, the analysis also shows a decrease in SSB/SSB 0 .Similarly, for lane snapper, the maximum Relative Yield has been exceeded, resulting in a decrease in the SSB/SSB 0 as well.
For the associated species (Figures 6(f ) and 6(g)), the F/M ratio was higher for hogfsh (2.08) than for white grunt (1.91).In these species, the Relative Yield has not yet reached its maximum, and the levels of SSB/SSB 0 are at their best overall, particularly for white grunt.

Discussion and Conclusions
Tis study represents the frst assessment of the Spawning Potential Ratio for the red grouper fshery species in the coastal waters of the Yucatan Peninsula.Te following discussion presents the most relevant results and explores its implications for the sustainable management of the red grouper fshery.

Te LB-SPR Analysis.
Length-based stock assessment methods, such as LB-SPR, along with others like the lengthbased Tompson and Bell approach, length-based integrated mixed efects, and length-based risk analysis, are widely acknowledged for their consistency and accuracy [95].However, to ensure the accuracy and precision of evaluation results, it is crucial that the collection of length data accurately represents the length compositions of the entire population, taking into consideration the random spatial distribution of fsh and the scattered nature of the samples [95].
In this study, we could not observe specimens of the seven species below the recorded minimum length values due to sampling limitations.Nevertheless, our research provides a reasonably robust initial approximation, which has aided in assessing the spawning potential of both the target and associated species in the artisanal red grouper fshery of the Campeche Bank.

Spawning Potential Ratio of the Grouper-Snapper Complex
5.2.1.Groupers.Hordyk et al. [23] emphasize that capturing a substantial proportion of immature juvenile individuals signifcantly diminishes spawning and recruitment, even at low fshing mortality (F/M) levels.Tis phenomenon aligns with our fndings for groupers.Although groupers were larger in size among the captured fsh, they were found to be immature ( < L 50 ) and displayed low SPR values.Notably, both red grouper and black grouper fell below the critical minimum value for SPR (0.10 and 0.05, respectively).For both species, these results suggest a high risk of local extinction.As for gag grouper, while its SPR value (0.26) continues to ensure that stocks maintain satisfactory productivity (0.20-0.30), it remains dangerously close to the critical minimum value for SPR (i.e., 0.20), posing an imminent risk of population decline.
Groupers have been subjected to signifcant fshing exploitation, resulting in declines in their abundance, size, spawning aggregations, and species composition [96].Groupers from Campeche Bank are highly vulnerable to overfshing due to their extended lifespan, larger size-age thresholds for sexual maturity, and the low M and K indices [44,75,76].For instance, the red grouper reaches L 50 � 50.9 cm FL, P 50 � 9.3 years; the black grouper achieves L 50 � 72.1 cm FL, P 50 � 13.6 years; and the gag grouper attains L 50 � 72 cm FL, P 50 � 11.6 years [44,[72][73][74].Te red grouper population, particularly, has undergone a decline in biomass from 1986 to 2000.Tis decline is attributed to reduced size in both the spawning stock and recruitment of 1-2-year-olds.Te cause of this decline can be traced back to heightened fshing pressure on juvenile and preadult groupers, specifcally those in the 2-3 age group, which has recorded the highest fshing mortality rate at 0.37.Consequently, this has led to a reduction in commercial catches from 14,410 to 9,797 tons [36].Tis trend persists despite the established management scheme for the fshery, with catches further dropping to less than 4000 tons [14].
Te increased fshing pressure on juvenile red grouper primarily results from the activities of the small-scale artisanal feet.Tis feet predominantly targets juvenile red grouper due to their substantial abundance in the fshing areas along the shallow waters of the Yucatan coastline [13,36,37,72,97].Te heightened vulnerability of this age group to fshing gear, specifcally the bottom longline, commonly employed in the red grouper fshery by this feet [98], contributes to the increased capture.
Te distribution pattern and migrations across the Campeche Bank constitutes an additional contributing factor.Juvenile red grouper (i.e., 20 to 30 cm TL) are typically found in shallow coastal waters within the depth range of 15 to 25 meters.In contrast, sexually mature adults (measuring ≥51 cm TL) are commonly observed in deeper waters (>30 m) [36,72,99].During the reproductive season in winter-spring, juvenile groupers move to shallower waters in the central-eastern region, whereas adult fsh undertake migrations to deeper waters, typically at depths ranging from 35 to 60 meters.Subsequently, in spring-summer, juveniles shift their habitat to northern areas, while adults migrate westward, crossing the vicinity of Dzilam de Bravo and Rio Lagartos [100].
Te susceptibility of groupers from Campeche Bank to overfshing appears to be infuenced by various factors.Notably, their distinct biology, distribution patterns, and potential migrations across the Campeche Bank contribute signifcantly to this susceptibility.Tese specifc factors play a crucial role in the observed trend of overfshing, particularly in recruitment and growth.Tis trend has resulted in a decline in the ecological performance of the red grouper fshery, thereby impacting the economic and social sectors at the artisanal level as underscore by Rincón-Sandoval and López-Rocha [101] in their evaluation of the red grouper fshery's performance using the Fishery Performance Indicators (FPI) framework proposed by Anderson et al. [8].
Furthermore, climate change presents an added threat to groupers, particularly the red grouper, currently facing overexploitation, as indicated by recent analyses conducted by Brulé et al. [76].Te authors observed that increasing water temperatures may disrupt their reproductive cycles, sexual diferentiation, sex reversal, and sex ratio, potentially reducing fertility.

Snappers and Associated
Species.Te snappers, including yellowtail and lane snapper, were observed to be smaller in size.Nevertheless, they were primarily captured in the adult state, specifcally after reaching sexual maturity (i.e., SL 50 > L 50 ), along with associated species such as hogfsh and white grunt.Our fndings regarding the adult catch of snappers align with the results reported by Brulé et al. [37], who noted that adults of yellowtail and lane snapper are predominantly captured in the Campeche Bank.
Te results for lane snapper align with the fndings by Hordyk et al. [23].Te authors emphasized that, despite a high fshing mortality (F/M) ratio among mature individuals due to pronounced selectivity, the fshery remains sustainable, albeit with reduced yields.Tis phenomenon can be attributed to the fact that older fsh typically demonstrate higher annual fecundity and spawn over a more extended season [1].However, it should be noted that not all mature female fsh lay eggs during the spawning season, and females undergoing their initial spawning at the age of 1 year exhibit the least likelihood of reproduction, as exemplifed by the spotted seatrout (Cynoscion nebulosus) [5].
Trejo-Martínez et al. [65] verifed this pattern for lane snapper within the Campeche Bank, highlighting that female, typically larger than males, exhibit an extended spawning period of 120 days.Te researchers observed a signifcantly higher fecundity (>200,000 oocytes) among the largest females (46.0 cm), with no males being observed in the larger size classes (>36.0 cm FL).
Te skewed gender ratio towards larger females, as observed by Trejo-Martínez et al. [65], contrasts with the fndings of Luckhurst et al. [55] for lane snapper in Bermuda (western Atlantic Ocean).Te latter researchers documented a higher proportion of males in the largest size category (>33 cm), attributing this trend to selective processes and competition during the capture phase.Tey proposed that larger males exhibit greater aggressiveness, resulting in higher success rates compared to females in interactions with fshing gear.Furthermore, they highlighted the possibility that distinct movement patterns between sexes on the fshing grounds may contribute to this observed phenomenon.
In this context, it is plausible that the bias observed by Trejo-Martínez et al. [65] towards females larger than 36.0 cm may be attributed to a decrease in the number of males due to heightened pressure on the latter.In this situation, larger females with greater reproductive potential could be in a condition of increased vulnerability to capture, resulting in a reduction in the proportion of these females in the population.Tis, in turn, poses a risk to decline in the stock of lane snapper.
On the other hand, lane snapper is vulnerable, like to other long-lived species, even under minimal levels of overexploitation [62].Terefore, despite the heightened potential for spawning, it is imperative, in adherence to the precautionary principle, to alleviate the increased fshing pressure (F/M � 6.60) on adult lane snapper individuals on the Campeche Bank, to mitigate the risk of population decline (i.e., SPR <0.20).
For the associated species, hogfsh, and white grunt, our fndings align with the LB-SPR model, which produces high SPR for species whose captured individuals' sizes are close to L ∞ [19].Both species, particularly white grunt, exhibited the highest SPR values (0.72 and 0.98, respectively) among all studied species.Additionally, both species recorded maximum sizes (40.5 cm and 34.0 cm TL, respectively) that closely correspond to their respective L ∞ values (i.e., 42.8 and 33.8 cm, respectively; Tables 2 and 3, Figure 3).
Te observed SPR for hogfsh (0.78) and, particularly, white grunt (0.98), closely approaches the natural SPR of 1.0, which is a typical value for unexploited or unfshed fsh stocks [22,31].Tis outcome can be attributed to the relatively recent commercial exploitation of both species in this region, which has emerged in response to the decline of the red grouper in the southern Gulf of Mexico [38][39][40] and has not yet been fully exploited.

Management Implications.
Te present results underscore the urgent necessity to alleviate the fshing pressure trend from the small-scale feet targeting juvenile groupers fsh, particularly for red grouper and black grouper, to mitigate the risk of local extinction.
Te existing management framework involves measures aimed at preventing recruitment and growth overfshing, including fshing bans, minimum size limits (MSL), and restrictions on gear selectivity (i.e., size and type of hook and bait type).Tese management actions have been exclusively focused on the target species, red grouper (E.morio).However, this management approach has not proven entirely efective in controlling recruitment and growth overfshing, since the impact on juvenile red grouper persists, as indicated by several studies [97,98].
An illustrative example of inefciency in management of recruitment and growth overfshing is manifests in the MSL = 36.3cm TL [103], that is smaller than the size at frst maturity (L 50 = 50.9cm FL [72], for red grouper, as noted by Brulé et al. [97] and Renán et al. [44]).Tose authors noted that even capturing fsh above the MSL, >36.3 cm TL (considered as legal groupers), they still be individuals that have not reached sexual maturity (juveniles and preadults, <L 50 ).Nevertheless, adjusting the Minimum Size Limit (MSL) to match or exceed the L 50 could present ethical and logistical challenges related to small-scale fshermen's access to the grouper resource.Consequently, this adjustment may result in the exclusion of this sector from the red grouper fshery [44,97,98].
Our results underscore the immediate necessity to reorient the current management approach.Particularly, it is crucial to address the capture of sublegal groupers (<MSL) by implementing necessary regulatory modifcations.Achieving this objective requires precise modifcations to the regulations governing the fshing gear used in the red grouper fshery, especially regarding gear selectivity (i.e., hook size and bait size), to reduce catches of immature fsh.Tis recommendation aligns with prior suggestions by Brulé et al. [97] and Rincón-Sandoval et al. [98].Furthermore, Brulé et al. [104] emphasizes the necessity of updating the size at frst maturity for the red grouper (L 50 = 50.9cm FL; [72]) due to the intense fshing pressure on this resource over the past two decades.
Te challenge of sublegal fsh, identifed by Rincón-Sandoval et al. [98], due to their increased susceptibility to fshing gear lacking sufcient size selectivity, poses a threat to sustainable fshing practices since the use of nonselective gear is detrimental to fshery resources [97,[105][106][107].Efectively controlling and managing overfishing, which impacts both growth and recruitment, relies on the selectivity of gear infuenced by factors such as hook size, bait, lures, and minimum size limits (MSL).
Rincón-Sandoval and López-Rocha [101] highlight that revising selectivity regulations carries dual advantages, encompassing ecological benefts (reduced capture of juveniles) and economic gains.Tis modifcation is poised to enhance both the red grouper stock and the livelihoods of fshermen by fostering increased capture of larger groupers, which command higher value per kilogram in the local market [108][109][110].
Furthermore, employing no-take marine reserves and areas with less intensive fshing could help alleviate intense fshing pressure.Tese reserves have demonstrated efectiveness in safeguarding grouper resources [96].Tis approach enhances enforcement efciency compared to complex catch and efort regulations, potentially reducing the necessity for collecting fsheries-dependent data.Te positive outcome is attributed to a signifcant increase in the density and biomass of larger grouper species [96].Currently, collaborative initiatives involving the State of Yucatan government, the academic community, the fshing industry, and nongovernmental organizations (NGOs) are in progress to establish the Fishing Refuge Zone Network along the Yucatan coast.Tese eforts are guided by NOM-049-SAG/ PESC-2014 [103].Noteworthy accomplishments include the successful inauguration of the inaugural fshing refuge zone Journal of Applied Ichthyology in Celestun by the Ministry of Agriculture and Rural Development (SADER) and National Commission of Aquaculture and Fisheries (CONAPESCA) [111].
Additionally, adopting an ecosystem-based approach to manage the red grouper fshery could allow not only for the protection of the red grouper but also for safeguarding all the species within the grouper-snapper complex and preserving their respective habitats.
Te present study represents the initial assessment of the Spawning Potential Ratio for seven commercially signifcant species captured by the red grouper fshery of the coast of the Yucatan Peninsula.Te fndings shed light on the strategies needed to prevent the local extinction of grouper resources currently diminished and associated species.Moreover, they provide a path toward sustainability for the red grouper fshery, thereby safeguarding the food security of the region and ensuring the well-being of communities dependent on fsheries resources in this area.

Figure 1 :
Figure 1: Map of the study area in the Yucatan Peninsula, indicating the fshing ports where the length data of the captured fsh was recorded.

Figure 3 :
Figure 3: Boxplot illustrating the total length of red grouper (E.morio) and associated species.Te black horizontal lines represent the median total length (cm) for each species, the boxes indicate the interquartile range, and the whiskers denote the 95% confdence intervals.Te red dotted line signifes the Minimum Legal Size (MLS) for red grouper, set at 36.3 cm TL.Te dotted blue lines indicate the L ∞ for each species (For M. bonaci and M. microlepis, the respective L ∞ values exceed the range of the axis scale; refer to Table2for details).

Figure 5 :
Figure5: Bar plot illustrating the Spawning Potential Ratio (SPR) using the LB-SPR Model for the red grouper fshery and its associated species.Te black dotted line indicates the SPR reference value, while the red dotted line represents the critical minimum SPR value and whiskers denote the 95% confdence intervals.A SPR below 0.20 suggests an elevated risk of decline, particularly in the supply of juvenile fsh.

Table 1 :
Population parameters of species associated with the red grouper fshery from the literature.

Table 2 :
Biological and exploitation parameters analyzed in the LB-SPR model for the red grouper fshery and associated species.
while red grouper measured an average length of 41.2 cm TL, spanning from 29.0 to 69.5 cm TL (±5.86).

Table 3 :
Number of specimens and biometric data per species.