Reproduction of grey snapper (Teleostei: Lutjanidae) in the southern Gulf of Mexico

INTRODUCTION

Snappers (Lutjanidae) are mainly restricted to tropical and subtropical regions. They are commercially important fish species throughout their geographical range, especially for local artisanal fisheries (Allen 1985Allen G.R. 1985. FAO Species Catalogue. Vol. 6. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fish. Synop. 125: 208 p.). Snapper populations in the Gulf of Mexico are distributed over extensive continental platforms, while those of the Caribbean Sea are essentially insular (Allen 1985Allen G.R. 1985. FAO Species Catalogue. Vol. 6. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fish. Synop. 125: 208 p., Bannerot et al. 1987Bannerot S., Fox W.W., Powers J.E. 1987. Reproductive strategies and the management of snappers and groupers in the Gulf on Mexico and Caribbean. In: Polovina J. and Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado, pp. 561-603.). The grey snapper Lutjanus griseus (Linnaeus, 1758) is widely and continuously distributed from Massachusetts in the United States to the Caribbean coast of Venezuela (Lindeman et al. 2016Lindeman K. C., Anderson W., Carpenter K.E., et al. 2016. - Lutjanus griseus. The IUCN Red List of Threatened Species 2016: e.T192941A2180367.). It is one of the most abundant reef fish in many areas of the Caribbean Sea. In Florida, it represents a major portion of recreational snapper catches; indeed, the L. griseus recreational fishery in this region exceeds its commercial fishery in terms of catch (Allen 1985Allen G.R. 1985. FAO Species Catalogue. Vol. 6. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fish. Synop. 125: 208 p., Lindeman et al. 2016Lindeman K. C., Anderson W., Carpenter K.E., et al. 2016. - Lutjanus griseus. The IUCN Red List of Threatened Species 2016: e.T192941A2180367.). Although the International Union for Conservation of Nature (IUCN) Red List classifies L. griseus as of least concern, Lindeman et al. (2016)Lindeman K. C., Anderson W., Carpenter K.E., et al. 2016. - Lutjanus griseus. The IUCN Red List of Threatened Species 2016: e.T192941A2180367. argue that its populations in Cuba, Puerto Rico and along the US Atlantic coast show signs of decline. In the northern Gulf of Mexico, the US stock is not considered to be overfished but has exhibited signs of overfishing since 1976 (SEDAR 2018Southeast Data, Assessment, and Review (SEDAR). 2018. - SEDAR 51 Gulf of Mexico gray snapper Final Stock Assessment Report. SEDAR: North Charleston SC.). In the southern Gulf of Mexico, L. griseus is one of the main snapper species exploited by artisanal fishers in the state of Yucatan, Mexico (Monroy-García et al. 2019Monroy-García C., Gutiérrez-Pérez C., Medina-Quijano H., et al. 2019. La actividad pesquera de la flota ribereña en el estado de Yucatán: pesquería de escama. Primera edición, Instituto Nacional de Pesca y Acuacultura, Ciudad de México, México. 102 pp.). Snapper fisheries have become increasingly important in Yucatan in response to sharp declines in populations of red grouper Epinephelus morio (Valenciennes, 1828), the region’s main fishery. In addition, large decreases have been observed in the population of Mexican red snapper Lutjanus campechanus (Poey, 1860) since early 1990 (SAGARPA 2018Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA). 2018. Acuerdo por el que se da a conocer la actualización de la carta nacional pesquera. In López-González A. (ed), Diario Oficial de la Federación, Tomo DCCLXXVII 10 (segunda sección). Secretaría de Gobernación, Ciudad de México, pp. 1-112.). Both trends have helped make L. griseus one of the most exploited snappers in the waters of the Yucatan Peninsula (Monroy-García et al. 2019Monroy-García C., Gutiérrez-Pérez C., Medina-Quijano H., et al. 2019. La actividad pesquera de la flota ribereña en el estado de Yucatán: pesquería de escama. Primera edición, Instituto Nacional de Pesca y Acuacultura, Ciudad de México, México. 102 pp.).

In response to their distribution habitat, snappers generally show a certain plasticity in some of their reproductive traits. Following Grimes’ (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp. concept, reproductive seasonality and size at maturity in snappers are more dependent on habitat types than on latitude. Species or populations that inhabit continental shelves or shallow waters (<91 m) have a restricted spawning season centred in summer and a sexual maturity which occurs at 41% (continental shelves) or 43% (shallow waters) of species maximum size. Conversely, species or populations from insular regions or deep reef zones (>91 m) reproduce year-round with spawning pulses in spring and autumn, and experience sexual maturity at 51% (insular regions) or 49% (deep reef zones) of species maximum size (Grimes 1987Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp.). For example, the population of silk snapper Lutjanus vivanus (Cuvier, 1828) from North Carolina and South Carolina has a restricted spawning season (June to August) and matures at 36% (female) or 41% (male) of its maximum size, whereas in Jamaica the same species spawns year-round and matures at 85% (female) or 73% (male) of its maximum size. In the Antilles and the Bahamas, deepwater (120-180 m depth; Allen 1985Allen G.R. 1985. FAO Species Catalogue. Vol. 6. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fish. Synop. 125: 208 p.) black snapper Apsilus dentatus (Guichenot, 1853) mature at 74% (female) or 79% (male) of its maximum size (Grimes 1987Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp.). However, Grimes (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp. also mentions that in various snapper populations around the world, sexual maturity and/or reproductive season are not strictly dictated by habitat type. For example, populations of red snapper L. campechanus and yellowtail snapper Ocyurus chrysurus (Bloch, 1791) from the continental shelf of the Yucatan Peninsula are reported to have an extended seasonal reproductive pattern: February to November for L. campechanus (Brulé et al. 2010Brulé T., Colás-Marrufo T., Pérez-Díaz E., Sámano-Zapata J.C. 2010. Red Snapper reproductive biology in the southern Gulf of Mexico. Trans. Am. Fish. Soc. 139: 957-968. https://doi.org/10.1577/T09-125.1 ) and January to September for O. chrysurus (Trejo-Martínez et al. 2011Trejo-Martínez J., Brulé T., Mena-Loría A., et al. 2011. Reproductive aspects of the yellowtail snapper Ocyurus chrysurus from the southern Gulf of Mexico. J. Fish Biol. 79: 915-936. https://doi.org/10.1111/j.1095-8649.2011.03062.x ). This is more typical of insular snapper species and populations.

The reproductive biology of L. griseus has been investigated in populations in Florida (Starck 1971Starck W.A. II. 1971. Biology of the Gray Snapper, Lutjanus griseus (Linneaus), in the Florida Keys. In: Starck W.A., II, Schroeder R.E. (eds), Invstigations on the gray snapper, Lutjanus griseus. Stud. Trop. Oceanogr. Miami 10: 11-150. https://doi.org/10.2307/1442662 , Domeier et al. 1996Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201., Allman and Grimes 2002Allman R.J., Grimes C.B. 2002. Temporal and spatial dynamics of spawning, settlement and growth of gray snapper (Lutjanus griseus) from the west Florida shelf as determined from otolith microstructures. Fish. Bull. 100: 391-403.), Cuba (González et al. 1979González E., Damas T., Millares N., Borrero M. 1979. Desove inducido en el caballerote (Lutjanus griseus Linné, 1758), en condiciones de laboratorio. Rev. Cub. Investig. Pesq. 4: 43-64., Báez et al. 1982Báez M.I., Alvarez-Lajonchere L.S., Ojeda-Serrano E. 1982. Reproducción del caballerote, Lutjanus griseus (Linnaeus) en Tunas de Zaza, Cuba. Rev. Invest. Mar. 3: 43-86., Claro 1983Claro R. 1983. - Ecología y ciclo de vida del caballerote, Lutjanus griseus (Linnaeus), en la plataforma cubana. I. Identidad, distribución y hábitat, nutrición y reproducción. Rep. Invest. Inst. Oceanol., Acad. Cien. Cuba 7: 1-30.), Guatemala (Andrade and Santos 2019Andrade H., Santos J. 2019. Life history of the gray snapper at the warm edge of its distribution range in the Caribbean. Mar. Coast. Fish. 11: 315-327. https://doi.org/10.1002/mcf2.10087 ) and Venezuela (Guerra-Campos and Bashirullah 1975Guerra-Campos A., Bashirullah A.K.M. 1975. Biología del pargo Lutjanus griseus (Linn.) de la isla de Cubagua, Venezuela. II. Maduración sexual y Fecundidad. Bol. Inst. Oceanogr. Univ. Oriente 14: 109-116.), but not in the southern Gulf of Mexico. Therefore, the present study analysed the main reproductive characteristics (sex-size distribution, sex ratio, size at maturity and spawning seasonality) of L. griseus from the continental shelf of the Yucatan Peninsula (i.e. Campeche Bank). The objective was to assess whether this population exhibits the pattern of sexual maturity and reproductive seasonality typical of continental snapper species and populations.

MATERIALS AND METHODS

Study area

 ⌅

In the southern Gulf of Mexico, Campeche Bank corresponds to the northern extension of the Yucatan Peninsula continental shelf (Fig. 1). Bottoms are sandy, coral and limestone substrates and, to a lesser degree, mud (García and Gómez 1974García C., Gómez J.A. 1974. Carta preliminar de fondos del Banco de Campeche., Res. Invest., INP 1: 37-38.). Macrobenthos biomass estimates suggest Campeche Bank harbours a great abundance of zoobenthos that is likely to be the dietary basis of various demersal fish species, such as snappers (Spichak and Formoso 1974Spichak S.K., Formoso M. 1974. Distribución cuantitativa del zoobentos alimenticio en el banco de Campeche (primavera). INP/CIP Cuba, Res. Invest. 1: 88-92.). All continental freshwater outflows into the sea at Campeche Bank originate from the terrestrial aquifer in the form of point-specific submarine discharges along the Peninsula coast (Aranda-Cirerol et al. 2006Aranda-Cirerol A., Herrera-Silveira J.A., Comín F.A. 2006. Nutrient water quality in a tropical coastal zone with groundwater discharge, northwest Yucatán, Mexico. Estuar. Coast. Shelf Sci. 68: 445-454. https://doi.org/10.1016/j.ecss.2006.02.015 ). In the northeastern Campeche Bank, in spring and summer, there is a temporary massive upwelling of cold (22.5°C), nutrient-rich water from the depths of the Caribbean Sea which flows east-to-southwest across the continental slope of Campeche Bank (Merino 1997Merino M., 1997. Upwelling on the Yucatan Shelf: hydrographic evidence. J. Mar. Syst. 13: 101-121. https://doi.org/10.1016/S0924-7963(96)00123-6 ). During the autumn and winter, the region experiences atmospheric cold fronts from the northwest, while in the summer prevailing winds are from the south and southeast, with occasional cyclones during the summer and early autumn (Kornicker and Boyd 1962Kornicker L.S., Boyd D.W. 1962. Shallow-water geology and environments of Alacran reef complex, Campeche Bank, Mexico. Bull. Am. Assoc. Pet. Geol. 46: 640-673. https://doi.org/10.1306/BC743851-16BE-11D7-8645000102C1865D , Logan 1969Logan B.W. 1969. Coral reefs and banks, Yucatán shelf, Mexico. Bull. Am. Assoc. Pet. Geol. 11: 129-198.). Mean sea surface temperature during the study period fluctuated from 26.8°C in February to 29.3°C in September (Gutiérrez et al. 2021Gutiérrez J.M., Jones R.G., Narisma G.T., et al. (eds), Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press: Cambridge. Available online: http://interactive-atlas.ipcc.ch/ (accessed on 1 March 2022).).

Fig. 1.  Sample sites of Lutjanus griseus caught from Campeche Bank, southern Gulf of Mexico, between January 2018 and September 2019. Yellow dots indicate sampling sites where females in actively spawning or past-spawner reproductive subphases were captured.

Sexual cycle

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Sexual cycle was characterized by analysing monthly mean variations in the gonadosomatic index (GSI=100×[ gW/GW] ) and in the relative proportion of individuals in each reproductive phase or subphase. To run a calendar year analysis, individuals (excluding immatures) were grouped by month of capture.

Presumed L. griseus spawning sites on Campeche Bank were identified based on actively spawning female spatial distribution (i.e. ovaries showing oocyte maturation [ OM] ) or past-spawner subphases (i.e. ovaries showing vitellogenic oocytes and postovulatory follicles) (Fig. 2). The first subphase indicates that females are in an imminent spawning stage, while the second indicates recently past spawning (Brown-Peterson et al. 2011Brown-Peterson N.J., Wyansky D.M., Saborido-Rey F., et al. 2011. A Standardized terminology for describing reproductive development in fishes. Mar. Coast. Fish. 3: 52-72. https://doi.org/10.1080/19425120.2011.555724 ).

Fig. 2.  Histological sections of ovaries from female Lutjanus griseus caught from Campeche Bank, southern Gulf of Mexico, between January 2018 and September 2019. A, actively spawning females; B, past-spawner females. CA, cortico alveolar oocyte; GVBD, germinal vesicle breakdown; GVM, germinal vesicle migration; H, hydrated oocyte; PG, primary growth oocyte; POF, postovulatory follicle; Vtg1, primary vitellogenic oocyte; Vtg2, secondary vitellogenic oocyte; Vtg3, tertiary vitellogenic oocyte (haematoxylin-eosin staining).

Data for TL and SL from previous snapper reproduction studies were converted to FL using the equations FL=0.943´TL+0.157 (r²=0.984; n=1236) and FL=1.151´SL+0.957 (r²=0.993; n=1226), based on TL, FL and SL data from the present study.

All measurements are presented as mean±standard error (se), and all statistical analyses were run using an α level of 0.05.

RESULTS

Sexual maturity

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The L_min was 24.2 cm FL for sexually mature females (individual in regeneration phase), and 22.8 cm FL for sexually mature males (individual in regression phase). The L_max recorded for L. griseus on Campeche Bank was 63.9 cm FL for females and 63.2 cm FL for males; therefore, the percentage of maximum size at which females reached maturity was 38% and that for males was 36%. For females, L₅₀ was 32.2 cm FL (31.0-33.5 cm FL limits, 95% confidence interval) and for males it was 22.0 cm FL (20.0-23.6 cm FL limits, 95% confidence interval) (Fig. 3).

Fig. 3.  Percentage in relation to fork length of sexually mature female and male Lutjanus griseus caught from Campeche Bank in the southern Gulf of Mexico between January 2018 and September 2019. The proportion of sexually mature fish within each size class was plotted using a binary logistic regression. Vertical lines indicate the length at which 50% of individuals were mature (L₅₀). Numbers indicate sample size for each size class. Sexually mature fish are early developing, developing, spawning capable, actively spawning, past-spawner (only for females), regressing and regenerating individuals.

Median sizes of immature females (30.3 cm FL) were significantly lower than median sizes of regenerating females (36.6 cm FL) (Kruskal-Wallis test H=94.91, df=1, P<2.2e-16). The length-frequency distribution of immature females differed from that of regenerating females (Kolmogorov-Smirnov test KS=0.0617, P=0.0355) (Fig. 4). These results confirm the accuracy of discrimination between immature and regenerating females based on ovary histology in the present study.

Fig. 4.  Size-frequency distributions for immature (I) and regenerating (RGE) female Lutjanus griseus caught from Campeche Bank in the southern Gulf of Mexico between January 2018 and September 2019.

Sexual cycle

 ⌅

Monthly evolution of the GSI for females and males throughout a calendar year showed that reproductive activity in L. griseus begins in May and ends in September (Fig. 5). Maximum mean GSI values were observed in June for males (1.01±0.14%) and in August for females (1.38±0.34%). The low mean GSI values observed between October and April for both females (0.33±0.02% and 0.46±0.05%, respectively) and males (0.13±0.01% and 0.12±0.01%, respectively) indicate that they were reproductively inactive during this period.

Fig. 5.  Seasonal variation of the Gonadosomatic index (GSI; mean±se) for female and male Lutjanus griseus caught from Campeche Bank in the southern Gulf of Mexico between January 2018 and September 2019. Numbers indicate sample size for each pooled sampled month.

Annual monthly variation in the percentage of individuals in different reproductive phases and subphases confirmed the GSI analysis observations (Fig. 6). Reproductively active females (n=47; 15% of captured females) were observed between May and September and reached a maximum percentage of captures in July (36%; n=13). The highest percentage of spawning capable females was recorded in June (29%; n=12), that for actively spawning females in August (6%; n=2), and that for past-spawning females in July (14%; n=5). From May to September, regenerating females represented between 24% and 77% of females captured monthly. Few regressing females were observed in monthly captures (range: 2-9%; n=1-3). Between October and April, all or most (96% in November) captured females were in the regenerating phase. Although males were reproductively active during a slightly longer time than females (April to October), their seasonal peak in reproductive activity was very similar to that of females (Fig. 6). The highest percentages of spawning capable and actively spawning males were observed between May and August (range=47-89%; n=17-58). The highest percentages of actively spawning males were observed in June (34%; n=22) and July (38%; n=26). The percentages of regenerating males were lowest between May and August (range=0-28%; n=0-10) and highest ​​between December and March (range=57-93%; n=26-38).

Fig. 6.  Seasonal variation of the percent frequency of female and male Lutjanus griseus caught from Campeche Bank in the southern Gulf of Mexico between January 2018 and September 2019, classified according to reproductive phases and subphases over a single year (RGE, regenerating; ED, early developing; D, developing; SC, spawning capable; AS, actively spawning; PS, past-spawner; RGR, regressing). Numbers indicate sample size for each pooled sampled month.

DISCUSSION

The use of different fishing gears to capture L. griseus specimens on Campeche Bank generated a sample consisting of individuals distributed over a wide range of representative lengths (14.7-63.9 cm FL). This snapper species is reported to reach a maximum size of 89 cm TL (=84 cm FL), although the most frequent size is 40 cm TL (=38 cm FL) (Allen 1985Allen G.R. 1985. FAO Species Catalogue. Vol. 6. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fish. Synop. 125: 208 p.). However, in this study juveniles smaller than 14.0 cm FL were not collected, probably because the fishing area covered by ​​the artisanal fleet in Yucatan excludes estuaries, coastal lagoons and the coastal margin, which are nursery habitats for L. griseus (Starck 1971Starck W.A. II. 1971. Biology of the Gray Snapper, Lutjanus griseus (Linneaus), in the Florida Keys. In: Starck W.A., II, Schroeder R.E. (eds), Invstigations on the gray snapper, Lutjanus griseus. Stud. Trop. Oceanogr. Miami 10: 11-150. https://doi.org/10.2307/1442662 , Claro and Lindeman 2004Claro R., Lindeman K.C. 2004. Biología y manejo de los pargos (Lutjanidae) en el Atlántico occidental. CITMA, Cuba, 472 pp. En CD-ROM, ISBN 878-959-298-011-2. http://www.redciencia.cu/cdoceano , Faunce and Seafy 2007Faunce C.H., Seafy E.J. 2007. Nearshore habitat use by gray snapper (Lutjanus griseus) and bluestriped grunt (Haemulon sciurus): environmental gradients and ontogenetic shifts. Bull. Mar. Sci. 80: 473-495.). The median sizes and length-frequency distributions for both sexes on Campeche Bank were identical, as previously reported for L. griseus populations in Florida (Starck 1971Starck W.A. II. 1971. Biology of the Gray Snapper, Lutjanus griseus (Linneaus), in the Florida Keys. In: Starck W.A., II, Schroeder R.E. (eds), Invstigations on the gray snapper, Lutjanus griseus. Stud. Trop. Oceanogr. Miami 10: 11-150. https://doi.org/10.2307/1442662 , Domeier et al. 1996Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201.). According to Domeier et al. (1996)Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201., this demographic trait could result from this species’s gonochoric-type sexuality pattern.

Grimes (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp. states that snappers can exhibit a slightly female-biased sex ratio in larger size classes because of differences in growth and mortality between sexes. Moreover, the overall sex ratio in L. griseus populations frequently favours females, as reported in the west Florida Keys (Domeier et al. 1996Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201.), Cuba (Báez et al. 1982Báez M.I., Alvarez-Lajonchere L.S., Ojeda-Serrano E. 1982. Reproducción del caballerote, Lutjanus griseus (Linnaeus) en Tunas de Zaza, Cuba. Rev. Invest. Mar. 3: 43-86., Claro 1983Claro R. 1983. - Ecología y ciclo de vida del caballerote, Lutjanus griseus (Linnaeus), en la plataforma cubana. I. Identidad, distribución y hábitat, nutrición y reproducción. Rep. Invest. Inst. Oceanol., Acad. Cien. Cuba 7: 1-30.) and Venezuela (Guerra-Campos and Bashirullah 1975Guerra-Campos A., Bashirullah A.K.M. 1975. Biología del pargo Lutjanus griseus (Linn.) de la isla de Cubagua, Venezuela. II. Maduración sexual y Fecundidad. Bol. Inst. Oceanogr. Univ. Oriente 14: 109-116.) (Table 2). However, the sex ratio observed here in the Campeche Bank population was balanced, as previously observed in populations in the Everglades National Park and the Florida Keys (Croker 1962Croker R.A. 1962. Growth and food of the gray snapper, Lutjanus griseus, in Everglades National Park. Trans. Amer. Fish. Soc. 91: 379-383. https://doi.org/10.1577/1548-8659(1962)91[379:GAFOTG]2.0.CO;2, Starck 1971Starck W.A. II. 1971. Biology of the Gray Snapper, Lutjanus griseus (Linneaus), in the Florida Keys. In: Starck W.A., II, Schroeder R.E. (eds), Invstigations on the gray snapper, Lutjanus griseus. Stud. Trop. Oceanogr. Miami 10: 11-150. https://doi.org/10.2307/1442662 ), the west coast of Florida (Allman and Goetz 2009Allman R.J, Goetz L.A. 2009. Regional variation in the population structure of gray snapper, Lutjanus griseus, along the west Florida shelf. Bull. Mar. Sci. 84: 315-330.) and the coast of Guatemala (Andrade and Santos 2019Andrade H., Santos J. 2019. Life history of the gray snapper at the warm edge of its distribution range in the Caribbean. Mar. Coast. Fish. 11: 315-327. https://doi.org/10.1002/mcf2.10087 ) (Table 2). Interpopulational variation in sex ratio in L. griseus ​​may occur in response to certain spatial-temporal factors such as habitat type and climatic season (Claro and Lindeman 2004Claro R., Lindeman K.C. 2004. Biología y manejo de los pargos (Lutjanidae) en el Atlántico occidental. CITMA, Cuba, 472 pp. En CD-ROM, ISBN 878-959-298-011-2. http://www.redciencia.cu/cdoceano ).

On Campeche Bank, male L. griseus reach sexual maturity at a smaller size than females, as reported for other populations (Table 2). The percentages of maximum size at sexual maturity in females (38%) and males (36%) show that the Campeche Bank population exhibits a typical maturity pattern for snapper populations distributed on continental shelves or in shallow waters (mature at about 41% and 43% of maximum size, respectively), as defined by Grimes (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp.. Similar results have been reported for Florida continental shelf populations: 40% for females and 37% to 38% for males (Starck 1971Starck W.A. II. 1971. Biology of the Gray Snapper, Lutjanus griseus (Linneaus), in the Florida Keys. In: Starck W.A., II, Schroeder R.E. (eds), Invstigations on the gray snapper, Lutjanus griseus. Stud. Trop. Oceanogr. Miami 10: 11-150. https://doi.org/10.2307/1442662 , Domeier et al. 1996Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201.). On the Guatemalan coast, however, the maximum size at sexual maturity percentage for L. griseus was higher in females (50%) than in males (38%) (Table 2); the female value was similar to those established by Grimes (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp. for snapper populations in insular or deep-water regions (mature at about 51% and 49% of maximum size, respectively). In Cuba, by contrast, the maximum size at sexual maturity percentages reported for L. griseus females (41%-46%) and males (35%-43%) were more typical of species and populations distributed on continental shelves (Báez et al. 1982Báez M.I., Alvarez-Lajonchere L.S., Ojeda-Serrano E. 1982. Reproducción del caballerote, Lutjanus griseus (Linnaeus) en Tunas de Zaza, Cuba. Rev. Invest. Mar. 3: 43-86., Claro 1983Claro R. 1983. - Ecología y ciclo de vida del caballerote, Lutjanus griseus (Linnaeus), en la plataforma cubana. I. Identidad, distribución y hábitat, nutrición y reproducción. Rep. Invest. Inst. Oceanol., Acad. Cien. Cuba 7: 1-30.) (Table 2). Differences between observed values and those proposed by Grimes (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp. may be explained by errors in calculating L_min in females and males and/or L_max for the studied populations. For example, Báez et al. (1982)Báez M.I., Alvarez-Lajonchere L.S., Ojeda-Serrano E. 1982. Reproducción del caballerote, Lutjanus griseus (Linnaeus) en Tunas de Zaza, Cuba. Rev. Invest. Mar. 3: 43-86., Claro (1983)Claro R. 1983. - Ecología y ciclo de vida del caballerote, Lutjanus griseus (Linnaeus), en la plataforma cubana. I. Identidad, distribución y hábitat, nutrición y reproducción. Rep. Invest. Inst. Oceanol., Acad. Cien. Cuba 7: 1-30. and Andrade and Santos (2019)Andrade H., Santos J. 2019. Life history of the gray snapper at the warm edge of its distribution range in the Caribbean. Mar. Coast. Fish. 11: 315-327. https://doi.org/10.1002/mcf2.10087 calculated L_min for both sexes by macroscopic examination of gonads, which is considered the least accurate method (Murua et al. 2003Murua H., Kraus G., Saborido-Rey F., et al. 2003. Procedures to estimate fecundity of marine fish species in relation to their reproductive strategy. J. Northwest Atl. Fish. Sci. 33: 33-54. https://doi.org/10.2960/J.v33.a3 , Lowerre-Barbieri et al. 2011Lowerre-Barbieri S. K., Ganias K., Saborido-Rey F., et al. 2011. Reproductive timing in marine fishes: variability, temporal scales, and methods. Mar. Coast. Fish. 3: 71-91. https://doi.org/10.1080/19425120.2011.556932 ). The L_max values reported by these authors were lower (51-53 cm FL and 55 cm TL [ =52 cm FL] ) than the L_max observed in the present study. Another possible explanation for discrepancies is that Grimes’s (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp. proposed values are not generally applicable to all snapper species and populations. For example, populations of lane snapper Lutjanus synagris (Linnaeus, 1758) from Cuba, Puerto Rico, Jamaica and Trinidad have an atypical sexual maturity pattern characteristic of continental shelf areas, while the population off Venezuela has an atypical pattern characteristic of island regions (Trejo-Martínez et al. 2021Trejo-Martínez J., Brulé T., Morales-López N., et al. 2021. Reproductive strategy of a continental shelf lane snapper population from the Southern Gulf of Mexico. Mar. Coast. Fish. 13: 140-156. https://doi.org/10.1002/mcf2.10142 ).

Two previous reports containing L₅₀ data for L. griseus are for the populations of the northern Gulf of Mexico (SEDAR 2018Southeast Data, Assessment, and Review (SEDAR). 2018. - SEDAR 51 Gulf of Mexico gray snapper Final Stock Assessment Report. SEDAR: North Charleston SC.) and off the Guatemalan coast (Andrade and Santos 2019Andrade H., Santos J. 2019. Life history of the gray snapper at the warm edge of its distribution range in the Caribbean. Mar. Coast. Fish. 11: 315-327. https://doi.org/10.1002/mcf2.10087 ) (Table 2). For the northern Gulf of Mexico population, the more recent calculation of female length at 50% maturity is between 23.9 and 28.8 cm FL, with 90% of individuals being mature at 36.2 cm FL. However, if based on female GSI values, a significant contribution to the spawning stock is not achieved until 30.0 cm FL, a size considered a more accurate estimate of L₅₀ for L. griseus (SEDAR, 2018Southeast Data, Assessment, and Review (SEDAR). 2018. - SEDAR 51 Gulf of Mexico gray snapper Final Stock Assessment Report. SEDAR: North Charleston SC.). Combining data from both sexes, Andrade and Santos (2019)Andrade H., Santos J. 2019. Life history of the gray snapper at the warm edge of its distribution range in the Caribbean. Mar. Coast. Fish. 11: 315-327. https://doi.org/10.1002/mcf2.10087 estimated an L₅₀ of 31.1 cm TL (=29.5 cm FL) for the Guatemalan population. The values from both studies are between those observed for females and males in the present study. In contrast, a study of L. griseus off Florida over 25 years ago found that 90% of individuals (females and males combined) were mature at 20 cm SL (=24 cm FL) and 100% at 24 cm SL (=29 cm) (Domeier et al. 1996Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201.). Compared with the L₅₀ data values reported for the northern Gulf of Mexico (SEDAR 2018Southeast Data, Assessment, and Review (SEDAR). 2018. - SEDAR 51 Gulf of Mexico gray snapper Final Stock Assessment Report. SEDAR: North Charleston SC.) and Guatemala (Andrade and Santos 2019Andrade H., Santos J. 2019. Life history of the gray snapper at the warm edge of its distribution range in the Caribbean. Mar. Coast. Fish. 11: 315-327. https://doi.org/10.1002/mcf2.10087 ), and those in the present study, these values seem to be serious underestimates and are difficult to explain. Perhaps the number of specimens analysed by Domeier et al. (1996)Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201. by means of histological preparation of gonads was too small (n=122), and/or mistakes were made in identification of the microscopic stages of gonadal maturation.

Spawning season for the Campeche Bank L. griseus population occurs from May to September, with probable spawning pulses between June and August, which are typical of snapper species and populations from continental shelves (Grimes 1987Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp.). These results coincide with those for L. griseus populations from other continental shelf regions such as Florida (Starck 1971Starck W.A. II. 1971. Biology of the Gray Snapper, Lutjanus griseus (Linneaus), in the Florida Keys. In: Starck W.A., II, Schroeder R.E. (eds), Invstigations on the gray snapper, Lutjanus griseus. Stud. Trop. Oceanogr. Miami 10: 11-150. https://doi.org/10.2307/1442662 , Domeier et al. 1996Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201., Allman and Grimes 2002Allman R.J., Grimes C.B. 2002. Temporal and spatial dynamics of spawning, settlement and growth of gray snapper (Lutjanus griseus) from the west Florida shelf as determined from otolith microstructures. Fish. Bull. 100: 391-403.) and Guatemala (Andrade and Santos 2019Andrade H., Santos J. 2019. Life history of the gray snapper at the warm edge of its distribution range in the Caribbean. Mar. Coast. Fish. 11: 315-327. https://doi.org/10.1002/mcf2.10087 ) (Table 2). However, L. griseus populations from insular regions such as Cuba (Báez et al. 1982Báez M.I., Alvarez-Lajonchere L.S., Ojeda-Serrano E. 1982. Reproducción del caballerote, Lutjanus griseus (Linnaeus) en Tunas de Zaza, Cuba. Rev. Invest. Mar. 3: 43-86., Claro 1983Claro R. 1983. - Ecología y ciclo de vida del caballerote, Lutjanus griseus (Linnaeus), en la plataforma cubana. I. Identidad, distribución y hábitat, nutrición y reproducción. Rep. Invest. Inst. Oceanol., Acad. Cien. Cuba 7: 1-30.) and Cubagua Island in Venezuela (Guerra-Campos and Bashirullah 1975Guerra-Campos A., Bashirullah A.K.M. 1975. Biología del pargo Lutjanus griseus (Linn.) de la isla de Cubagua, Venezuela. II. Maduración sexual y Fecundidad. Bol. Inst. Oceanogr. Univ. Oriente 14: 109-116.) also display a restricted spawning season centred in summer, a spawning season pattern characteristic of continental shelf populations (Table 2). Thus, as previously noted by Grimes (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp., insular L. griseus populations do not always exhibit reproductive seasons strictly in accordance with their habitat type.

Collection sites for two of the actively spawning females (n_total=6) and three of the past-spawner females (n_total=10) analysed in the present study could not be placed confidently. But it is known that the others (four actively spawning and seven past-spawner females) were caught at three collection sites west of Celestún (range=29-44 m deep) and one north of Dzilam de Bravo (22 m deep), suggesting that these may be L. griseus spawning areas. Actively spawning and past-spawner females were captured within seven days before and two days after the full moon phase. Only one actively spawning female was caught five days after the new moon. This would coincide with a report that in Cuba L. griseus spawners migrate to waters 20 to 30 m deep to reproduce at night near the full moon (Claro 1983Claro R. 1983. - Ecología y ciclo de vida del caballerote, Lutjanus griseus (Linnaeus), en la plataforma cubana. I. Identidad, distribución y hábitat, nutrición y reproducción. Rep. Invest. Inst. Oceanol., Acad. Cien. Cuba 7: 1-30., Claro and Lindeman 2003Claro R., Lindeman K.C. 2003. Spawning aggregation sites of snapper and grouper species (Lutjanidae and serranidae) on the insular shelf of Cuba. Gulf Caribb. Res. 14: 91-106. https://doi.org/10.18785/gcr.1402.07 ). Larger movements by grey snapper are related to spawning migration and it is probable that this species aggregates at offshore spawning sites (SEDAR 2018Southeast Data, Assessment, and Review (SEDAR). 2018. - SEDAR 51 Gulf of Mexico gray snapper Final Stock Assessment Report. SEDAR: North Charleston SC.). However, L. griseus spawning aggregations have not yet been fully validated (Domeier and Colin 1997Domeier M.L., Colin P.L. 1997. Tropical reef fish spawning aggregations: defined and reviewed. Bull. Mar. Sci 60: 698-726., Lindeman et al. 2000Lindeman K.C., Pugliese R., Waugh G.T., Ault J.C. 2000. Developmental patterns within a multispecies reef fishery: management applications for essential fish habitats and protected areas. Bull. Mar. Sci. 66: 929-956.; Binder et al. 2021Binder B.M., Taylor J.C., Gregg K., Boswell K.M. 2021. Fish spawning aggregations in the southeast Florida Coral Reef Ecosystem Conservation Area: A case study synthesis of user reports, literature, and field validation efforts. Front. Mar. Sci. 8: 671477. https://doi.org/10.3389/fmars.2021.671477 ). The Campeche Bank L. griseus population exhibits an asynchronous ovarian organization and is a batch spawner (Macal-López et al. in pressMacal-López K.C., Brulé T., Torres-Villegas J.R., et al. In press. Oocyte distribution, ovarian organization, and spawning pattern in Lutjanus griseus. Cybium.). However, spawning frequency/spawning interval was not calculated in this study because there were insufficient numbers of reproductively active females in the sample. In the northern Gulf of Mexico, it has been estimated that the L. griseus spawning season is 137 days long and encompasses 37 spawns within that period (SEDAR 2018Southeast Data, Assessment, and Review (SEDAR). 2018. - SEDAR 51 Gulf of Mexico gray snapper Final Stock Assessment Report. SEDAR: North Charleston SC.). Using these values provides an estimated spawning interval of 3.7 days for this snapper.

Despite a paucity of reproductively active females, particularly those in the active spawning and past-spawner subphases, the present data were sufficient to characterize sexual maturity and spawning season for L. griseus on Campeche Bank. This is an ongoing challenge in the study of L. griseus (Starck 1971Starck W.A. II. 1971. Biology of the Gray Snapper, Lutjanus griseus (Linneaus), in the Florida Keys. In: Starck W.A., II, Schroeder R.E. (eds), Invstigations on the gray snapper, Lutjanus griseus. Stud. Trop. Oceanogr. Miami 10: 11-150. https://doi.org/10.2307/1442662 , Rutherford et al. 1983Rutherford E.S., Thue E.B., Buker D.G. 1983. Population structure, food habits, and spawning activity of gray snapper, Lutjanus griseus, in Everglades National Park. S. Fla. Res. Cent. Rep. SFRC-83/02. 41 pp., Domeier et al. 1996Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201.), because maturing adults migrate from shallow coastal waters to spawning grounds in deeper reef areas during the spawning season (Starck 1971Starck W.A. II. 1971. Biology of the Gray Snapper, Lutjanus griseus (Linneaus), in the Florida Keys. In: Starck W.A., II, Schroeder R.E. (eds), Invstigations on the gray snapper, Lutjanus griseus. Stud. Trop. Oceanogr. Miami 10: 11-150. https://doi.org/10.2307/1442662 , Domeier et al. 1996Domeier M.L., Koenig C., Coleman F.1996. Reproductive biology of the gray snapper (Lutjanus griseus), with notes on spawning for other western Atlantic snappers (Lutjanidae). In: Arreguin-Sanchez F., Munro J.L, Balgos M.C., Pauly D. (eds), Biology, fisheries and culture of tropical groupers and snappers. ICLARM, pp. 189-201., SEDAR 2018Southeast Data, Assessment, and Review (SEDAR). 2018. - SEDAR 51 Gulf of Mexico gray snapper Final Stock Assessment Report. SEDAR: North Charleston SC.). Collection for the present study was done mainly in shallow waters, which may have caused the scarcity of reproductively active females in the collections. However, high percentages of reproductively active males (range=19%-89%), including various in the actively spawning subphase (range=3%-38%), were caught every month of the spawning season (May-September). Mature L. griseus decrease feeding activity during the spawning season (Claro 1983Claro R. 1983. - Ecología y ciclo de vida del caballerote, Lutjanus griseus (Linnaeus), en la plataforma cubana. I. Identidad, distribución y hábitat, nutrición y reproducción. Rep. Invest. Inst. Oceanol., Acad. Cien. Cuba 7: 1-30.), and thus reproductively active females may have been less accessible than males to the fishing gear used during the spawning season, especially to passive techniques such as hook and line. Another possible explanation is that most reproductively active females start migrating to offshore spawning grounds earlier in the season than reproductively active males, and/or that most reproductively active males make continuous movements during the spawning season between offshore spawning sites and inshore feeding sites

The present results for the Campeche Bank L. griseus population corroborate Grimes’s (1987)Grimes C.B. 1987. Reproductive biology of the Lutjanidae: a review. In Polovina J.J., Ralston S. (eds), Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, Colorado. 239-294 pp. concept regarding continental reproductive pattern in snappers. For this continental population, sexual maturation occurred at a smaller size in males than in females, and between 36% and 38% of the maximum size for both sexes. The spawning season was centred around summer, with spawning peaks observed between June and August. This study generates new data on core aspects of the reproductive strategy of L. griseus, one of the least-studied snappers in the western Central Atlantic. It expands knowledge on the life history of a species vital to tropical marine ecosystem ecology and provides data fundamental to stock assessment and to defining the fisheries management policies most appropriate to specific snapper populations.