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Revista de Biología Tropical
versión On-line ISSN 0034-7744versión impresa ISSN 0034-7744
Rev. biol. trop vol.62 supl.3 San José sep. 2014
Is the Queen conch Strombus gigas (Mesogastropoda: Strombidae) a species with Allee effect?
Es el caracol marino Strombus gigas (Mesogastropoda: Strombidae) una especie con efecto Alle?
Es el caracol marino Strombus gigas (Mesogastropoda: Strombidae) una especie con efecto Alle?
Abstract
The marine park of Xel-Há has a population of Strombus gigas which breeds in the area. We determined the relationship between reproductive activity, conch density and environmental parameters. Samples were collected from February to December 2012, using the transect method, at four sites of Marine Park Xel-Ha, Quintana Roo, Mexico. Sediment samples were analyzed and classified using Folk & Ward’s method. Temperature, salinity and dissolved oxygen were also recorded. Density had a small correlation with sediment (Pearson r=0.29 with very coarse and r=0.26 with coarse sand), while mating and spawning had a correlation of r=0.54 and 0.62 with medium sand, respectively. Density was high in the four sites and was not associated with mating and spawning (r=0.08 and 0.03, respectively). For reproduction, S. gigas requires specific substrate conditions (sandy effect) and not just a density of 56 Conch Ha–1 (Allee effect).
Key words: Strombus gigas, Allee effect, reproductive behavior, sandy effect.
Resumen
El parque marino de Xel -Há tiene una población de Strombus gigas que se cría en la zona. Determinamos la relación entre la actividad reproductiva, la densidad de la concha de S. gigas y los parámetros ambientales. Las muestras fueron recolectadas de febrero a diciembre de 2012, utilizando el método de transecto, en cuatro sitios del Parque Marino de Xel -Ha, Quintana Roo, México. Fueron analizados y clasificados utilizando la metodología de Folk & Ward. También se registraron temperaturas, salinidad y oxígeno disuelto. La densidad de concha mostró una baja correlación en la categoría de sedimentos (r = 0.29 , con muy gruesos y r = 0.26 con arena gruesa ), mientras que el apareamiento y desove con arena media mostraron una correlación de r = 0.54 y 0.62, respectivamente. Las densidades en cuatro sitios fueron altas y no se asociaron con el número de apareamientos y desove (r = 0.08 y 0.03, respectivamente). Para la reproducción, S. gigas requiere condiciones específicas de sustrato (efecto arenoso) y no sólo una densidad de 56 Conch Ha-1 (efecto Allee ).
Palabras clave: Strombus gigas, efecto Allee, comportamiento reproductivo, efecto Sandy
The queen conch Strombus gigas is distributed from Brazil and Venezuela in the south up to Florida and the Bahamas in the north, including all the lesser and greater Antilles. S. gigas is now a luxury food. It represents one of the most valuable resources in the region, and was considered as second most valuable fishery with incomes of 6 US$ millions/year, exceeded only by the spiny lobster Panulirus argus (Brownell & Stevely, 1981; Pérez-Pérez & Aldana-Aranda, 2000). Now S. gigas is an overfished species protected by CITES who is regulated by the international commerce of this resource (de Jesús Navarrete, 2001; Brito-Manzano, Aldana-Aranda, de la Cruz-Lázaro & Estrada-Botello, 2006). However, illegal catch is practiced in all countries of the Caribbean region.
This organism has internal fertilization, it produces an egg mass and its development is indirect (Randall, 1964). Given the regional importance of queen conch in the Caribbean, and the critical status of most populations, the reproductive biology of this species has been studied in several Caribbean countries (Aldana Aranda et al., 2003a to 2003e; Delgado et al., 2004; Aldana-Aranda, 2006; Castro, Frenkiel, Baqueiro & Aldana-Aranda, 2007; Bissada-Gooding & Oxeford, 2010). Stoner, Sandt& Boidron-Metairon (1992) related S. gigas reproduction with temperature, photoperiod and density of adult conchs.
Stoner & Ray-Culp (2000) observed that mating and spawning in the Bahamas never occurred at a density <48 Conch∙Ha-1. These authors mention that the “Allee effect” (or “depensation”) (Gascoigne & Lipcius, 2004) has an influence in the reproductive activity of S. gigas, concluding that the overfishing of this resource affects in the recovering and reproduction rates. de Jesús-Navarrete and Valencia-Beltrán (2003) reported a migration for reproduction to sandy areas, associating the reproduction with density but not with sediment, based on these observations, the principal goal of this research was to evaluate the effect of the sediment, physicochemical and population parameters on the reproductive activity of S. gigas from February to December 2012.
Materials and Methods
Study area: The study was carried in four sites of Xel-Há inlet (Bocana, Centro, Brazo Norte and Cueva) located in Quintana Roo, México, in the geographical coordinates 20°18’50”-20°19’17”N y 87°21’45.5”-87°21’02.5”W (Fig. 1). This site has a total water surface of 14Ha, where the average depth is 3.0m, showing a gradient in the physicochemical parameters (due to the underground river effluents).
Sample collection: In each site we placed three linear transects of 100 x 2m of length, giving an area of 200m-2 by transect. Weekly from February to December 2012, using scuba diving we registered the number of adult conch and the reproductive activity. Figures 2A-2C show mating, spawning and free egg masses of S. gigas. Monthly in each site siphonal length (mm) and thickness lip (mm) in adult conchs were measured. Temperature (°C), salinity (ppt), dissolved oxygen (mg∙L-1) were measured and sediment samples were taken. The sediment samples were dried and classified with the Folk & Ward methodology (1957). The Infostat software was used to calculated means, standard deviation, one-way Anova and Pearson’s correlation among reproductive, physicochemical and granulometrics parameters.
Results
Environmental parameters: Mean and standard deviation (S.D.) of temperature were 27.44±0.97°C. Brazo Norte showed the lowest records, while Centro recorded the highest (27.25±1.10 and 27.70±0.75°C, respectively). There was no significant variation between sites (p=0.2033). Bocana and Cueva showed mean salinities of 33.76±0.87 and 13.64±1.83ppt, respectively. Salinity showed significant variation between sites (p≤0.0001). Mean of dissolved oxygen was 4.73±0.97mg.l-1, with the highest concentration in Bocana and minor in Cueva (5.45±1.28 and 4.01±1.15 mg.l-1, respectively), showing significant variation among sites (p≤0.0001). In relation to the sediments composition, Bocana showed 62% of coarse to medium to sands; Centro and Cueva, 60% to fine and very fine sands and Brazo Norte, 73.5% of fine to very fine sands (Fig. 3). The substrate composition among sites showed significant difference (p≤0.0001).
Sizes population: Bocana had a density of 665.58±585.38 Conch.Ha-1, followed by Cueva, Brazo Norte and Centro (647.17±487.17, 596.92±333.10 and 404.58±454.21 Conch.Ha-1) (Fig. 4A). Density was ≥10 times than density suggested by Stoner to have mating and spawning. There was significant variation among sites (p≤0.0001). The size structure in the four locations was very similar, with values of 203.68±23.73mm of shell length in Bocana, to 187.61±27.15mm in Cueva (Fig. 4B). Shell length did not change significantly among locations (p=0.3080). Using lip thickness (6mm) as an indicator of reproductive activity in conch (Aldana-Aranda & Frenkiel, 2007), we observed that conch of three sites have a lip thickness corresponding to adults: Bocana, Centro and Cueva with 15.25±6.7, 11.66±7.48 and 6.03±5.47mm, respectively (Fig. 4C). However, lip thickness of conch showed significant variation among sites (p=0.0198).
Pearson correlation analysis showed a high association between mating and medium sands (r=0.54) and spawning with medium sand (r=0.62). Temperature was associated with spawning (r=0.40), while density conch exhibited a low association with mating and spawning (r=0.08 and r=0.03, respectively) (Table 1).
Discussion
Stoner & Ray-Culp (2000) observed that mating never occurred when density was <56 Conch.Ha-1, and spawning never occurred at <48 Conch.Ha-1, demonstrating the operation of depensatory mechanisms. In this study mean density was >400 Conch.Ha-1 in four sites, however only the Bocana site showed mating and spawning behaviors. Peel and Aldana-Aranda (2012) reported a spatial segregation of juveniles and adults in Xel-Ha, pointing that the sites in the interior of the Inlet probably function as nurseries while Bocana could be associated with reproductive activity. It was observed in the present study that adults are placed in all the sites, which indicate that reproduction occurs in this inlet, but only at Bocana site. Stoner, Sandt and Boidron-Metairon (1992) and de Jesús Navarrete (1999) associated temperature with reproduction of S. gigas. In this study reproductive behavior was associated with temperature and dissolved oxygen, but conch presented mating and spawning only when sediments present ≥60 % of medium to coarse sands (Table 2).
Four sites exhibited a density suggested by Stoner & Ray-Culp (2000) to be related to reproduction, and had reproductive adults present at all times. Given that the physicochemical parameters were similar at all four sites, we suggest that S. gigas needs for mating and spawning a minimal density and a reproductive migration pattern related with sediment category (medium sand). Our theory is that S. gigas for reproduction is a species with a specific sandy habitat, having two effects: “Allee” and “Sandy” effects.
Acknowledgments
This research was supported by project Sistema de Información Geográfica para la Conservación del Patrimonio del Caribe y el Desarrollo Sustentable del Parque Xel-Há (Innovatec-Conacyt: 183724). We would like to thank Alejandro Aldana Moreno for photography support, scholarships from Conacyt and staff of Laboratory of Biology and Aquaculture of Mollusks (Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional) for assistance in samplings.
References
Aldana-Aranda, D., & Frenkiel, L. (2007). Lip thickness of Strombus gigas versus maturity: a management measure. Proceedings of the Gulf and Caribbean Fisheries Institute, 58, 431-442. [ Links ]
Aldana-Aranda, D. (2006). Overview of reproductive patterns of the queen conch Strombus gigas from different reef systems in the Caribbean. Proceedings of the Gulf and Caribbean Fisheries Institute, 57, 771-790. [ Links ]
Aldana-Aranda, D., Baqueiro-Cárdenas, E., & Manzanilla-Naim, S. (2003a). Mexican marine parks as a fishery management tool for the queen conch Strombus gigas. In Aldana-Aranda, D. (ed.). El caracol rosa Strombus gigas: conocimiento integral para su manejo sustentable en el Caribe. México: CYTED-Press. [ Links ]
Aldana Aranda, D., Cardenas, E.B., Morales, I.M., Ochoa, R.I., & Brule, T. (2003b). Reproductive patterns of Strombus gigas from Alacranes Reef versus Chinchorro Bank of Mexico. Proceedings of the Gulf and Caribbean Fisheries Institute, 54, 202-225. [ Links ]
Aldana-Aranda, D., Cardenas, E. B., Morales, I. M., Ochoa, R. I., Brule, T., & Baez, R. I. O. (2003c). Gonad behavior during peak reproduction period of Strombus gigas from Banco Chinchorro. Bulletin of Marine Science, 73(1), 241-248. [ Links ]
Aldana-Aranda, D., Sánchez-Crespo, M., Reynaga-Álvarez, P., Patiño-Suarez, V., George-Zamora, A., & Baqueiro-Cárdenas, E.R. (2003d). Crecimiento y temporada reproductiva del caracol rosa Strombus gigas en el Parque Xel-Ha, Mexico. Proceedings of the Gulf and Caribbean Fisheries Institute, 56, 741-754. [ Links ]
Aldana-Aranda, D., Sánchez-Crespo, M., Patino-Suarez, V., George-Zamora, A., Baqueiro-Cárdenas, E., Carillo, E., & Pérez, S. (2003e). Abundancia, frecuencia de tallas y distribucion especial del caracol Strombus gigas en el Parque Xel-Ha, Mexico. In Aldana-Aranda, D. (Ed.). El caracol rosa Strombus gigas: conocimiento integral para su manejo sustentable en el Caribe. México: CYTED-Press. [ Links ]
Bissada-Gooding, C. E., & Oxeford, H. A. (2010). Estimating Home Range and Density of a Queen Conch Aggregation using Acoustic Telemetry and Conventional Tagging. Proceedings of the Gulf and Caribbean Fisheries Institute, 62, 384-389. [ Links ]
Brito Manzano, N., Aldana Aranda, D., de la Cruz Lázaro, E., & Estrada Botello, M. A. (2006). Organogénesis larvaria de Strombus gigas (Mesogastropoda: Strombidae) en el Arrecife Alacranes durante el período máximo de su época reproductiva. Redalyc, Universidad y Ciencia, 22(1), 75-82. [ Links ]
Brownell, W. N., & Stevely, J. M. (1981). The biology, fisheries and management of the Queen conch Strombus gigas. Marine Fisheries Review, US Department of Commerce, 43(7), 1-12. [ Links ]
Castro-Gonzalez, E. R., Frenkiel, L., Baqueiro-Cardenas, E., & Aldana-Aranda, D. (2007). Atypical reproductive cycle of the queen conch Strombus gigas (Mollusca: gastropoda). Proceedings of the Gulf and Caribbean Fisheries Institute, 58, 443-450. [ Links ]
de Jesús Navarrete, A. (1999). Distribución y abundancia de larvas velígeras de Strombus gigas en Banco Chinchorro Quintana Roo, México. Tesis doctoral, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, México. [ Links ]
de Jesús-Navarrete, A., & Valencia-Beltrán, V. (2003). Abundance of Strombus gigas zero-year class juveniles at Banco Chinchorro Biosphere Reserve, Quintana Roo, Mexico. Bulletin of Marine Science, 73, 232-240. [ Links ]
de Jesús-Navarrete, A. (2001). Crecimiento del caracolStrombus gigas (Gastropoda: Strombidae) en cuatroambientes de Quintana Roo, México. Revista de Biologia Tropical, 49, 85-91. [ Links ]
Delgado, G. A., Bartels, C. T., Glazer, R. A., Brown-Petersen, N. J., & McCarthy, K. J. (2004). Translocation as a strategy to rehabilitate the queen conch (Strombus gigas) population in the Florida Keys. Fishery Bulletin, (2), 278-288. [ Links ]
Folk R. L., & Ward, W. C. (1957). Brazos River bar: a study in the significance of grain size parameters. Journal of Sedimentary Petrology, 27, 3-26. [ Links ]
Gascoigne J. C., & Lipcius, R. N. (2004). Allee effects driven by predation. Journal of Applied Ecology, 41, 801-810. [ Links ]
Peel, J. R., & Aldana-Aranda, D. (2012). Growth and population assessment of the queen conch Strombus gigas (Mesogastropoda: Strombidae) by capture mark-recapture sampling in a natural protected area of the Mexican Caribbean. Revista de Biologia Tropical, 60(1), 127-137, [ Links ]
Pérez-Pérez, M., & Aldana-Aranda, D. (2000). Distribución abundancia, densidad y morfometría de Strombus gigas (Mesogastrópoda: Strombidae) en el arrecife Alacranes, Yucatán, México. Revista de Biologia Tropical, 48, 51-57. [ Links ]
Randall, J. E. (1964). Contributions to the biology of the queen conch, Strombus gigas. Bulletin of Marine Science, 14(2), 246-295. [ Links ]
Stoner, A. W., & Ray-Culp, M. (2000). Evidence for Allee effects in an over-harvested marine gastropod: density-dependent mating and egg production. Marine Ecology Progress Series, 202, 297-302. [ Links ]
Stoner, A. W., Sandt, V. J., & Boidron-Metairon, I. F. (1992). Seasonality of reprodutucive activity and abundance of veligers in queen conch, Strombus gigas. Fishery Bulletin, 90, 161-170. [ Links ]
Aldana-Aranda, D. (2006). Overview of reproductive patterns of the queen conch Strombus gigas from different reef systems in the Caribbean. Proceedings of the Gulf and Caribbean Fisheries Institute, 57, 771-790. [ Links ]
Aldana-Aranda, D., Baqueiro-Cárdenas, E., & Manzanilla-Naim, S. (2003a). Mexican marine parks as a fishery management tool for the queen conch Strombus gigas. In Aldana-Aranda, D. (ed.). El caracol rosa Strombus gigas: conocimiento integral para su manejo sustentable en el Caribe. México: CYTED-Press. [ Links ]
Aldana Aranda, D., Cardenas, E.B., Morales, I.M., Ochoa, R.I., & Brule, T. (2003b). Reproductive patterns of Strombus gigas from Alacranes Reef versus Chinchorro Bank of Mexico. Proceedings of the Gulf and Caribbean Fisheries Institute, 54, 202-225. [ Links ]
Aldana-Aranda, D., Cardenas, E. B., Morales, I. M., Ochoa, R. I., Brule, T., & Baez, R. I. O. (2003c). Gonad behavior during peak reproduction period of Strombus gigas from Banco Chinchorro. Bulletin of Marine Science, 73(1), 241-248. [ Links ]
Aldana-Aranda, D., Sánchez-Crespo, M., Reynaga-Álvarez, P., Patiño-Suarez, V., George-Zamora, A., & Baqueiro-Cárdenas, E.R. (2003d). Crecimiento y temporada reproductiva del caracol rosa Strombus gigas en el Parque Xel-Ha, Mexico. Proceedings of the Gulf and Caribbean Fisheries Institute, 56, 741-754. [ Links ]
Aldana-Aranda, D., Sánchez-Crespo, M., Patino-Suarez, V., George-Zamora, A., Baqueiro-Cárdenas, E., Carillo, E., & Pérez, S. (2003e). Abundancia, frecuencia de tallas y distribucion especial del caracol Strombus gigas en el Parque Xel-Ha, Mexico. In Aldana-Aranda, D. (Ed.). El caracol rosa Strombus gigas: conocimiento integral para su manejo sustentable en el Caribe. México: CYTED-Press. [ Links ]
Bissada-Gooding, C. E., & Oxeford, H. A. (2010). Estimating Home Range and Density of a Queen Conch Aggregation using Acoustic Telemetry and Conventional Tagging. Proceedings of the Gulf and Caribbean Fisheries Institute, 62, 384-389. [ Links ]
Brito Manzano, N., Aldana Aranda, D., de la Cruz Lázaro, E., & Estrada Botello, M. A. (2006). Organogénesis larvaria de Strombus gigas (Mesogastropoda: Strombidae) en el Arrecife Alacranes durante el período máximo de su época reproductiva. Redalyc, Universidad y Ciencia, 22(1), 75-82. [ Links ]
Brownell, W. N., & Stevely, J. M. (1981). The biology, fisheries and management of the Queen conch Strombus gigas. Marine Fisheries Review, US Department of Commerce, 43(7), 1-12. [ Links ]
Castro-Gonzalez, E. R., Frenkiel, L., Baqueiro-Cardenas, E., & Aldana-Aranda, D. (2007). Atypical reproductive cycle of the queen conch Strombus gigas (Mollusca: gastropoda). Proceedings of the Gulf and Caribbean Fisheries Institute, 58, 443-450. [ Links ]
de Jesús Navarrete, A. (1999). Distribución y abundancia de larvas velígeras de Strombus gigas en Banco Chinchorro Quintana Roo, México. Tesis doctoral, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, México. [ Links ]
de Jesús-Navarrete, A., & Valencia-Beltrán, V. (2003). Abundance of Strombus gigas zero-year class juveniles at Banco Chinchorro Biosphere Reserve, Quintana Roo, Mexico. Bulletin of Marine Science, 73, 232-240. [ Links ]
de Jesús-Navarrete, A. (2001). Crecimiento del caracolStrombus gigas (Gastropoda: Strombidae) en cuatroambientes de Quintana Roo, México. Revista de Biologia Tropical, 49, 85-91. [ Links ]
Delgado, G. A., Bartels, C. T., Glazer, R. A., Brown-Petersen, N. J., & McCarthy, K. J. (2004). Translocation as a strategy to rehabilitate the queen conch (Strombus gigas) population in the Florida Keys. Fishery Bulletin, (2), 278-288. [ Links ]
Folk R. L., & Ward, W. C. (1957). Brazos River bar: a study in the significance of grain size parameters. Journal of Sedimentary Petrology, 27, 3-26. [ Links ]
Gascoigne J. C., & Lipcius, R. N. (2004). Allee effects driven by predation. Journal of Applied Ecology, 41, 801-810. [ Links ]
Peel, J. R., & Aldana-Aranda, D. (2012). Growth and population assessment of the queen conch Strombus gigas (Mesogastropoda: Strombidae) by capture mark-recapture sampling in a natural protected area of the Mexican Caribbean. Revista de Biologia Tropical, 60(1), 127-137, [ Links ]
Pérez-Pérez, M., & Aldana-Aranda, D. (2000). Distribución abundancia, densidad y morfometría de Strombus gigas (Mesogastrópoda: Strombidae) en el arrecife Alacranes, Yucatán, México. Revista de Biologia Tropical, 48, 51-57. [ Links ]
Randall, J. E. (1964). Contributions to the biology of the queen conch, Strombus gigas. Bulletin of Marine Science, 14(2), 246-295. [ Links ]
Stoner, A. W., & Ray-Culp, M. (2000). Evidence for Allee effects in an over-harvested marine gastropod: density-dependent mating and egg production. Marine Ecology Progress Series, 202, 297-302. [ Links ]
Stoner, A. W., Sandt, V. J., & Boidron-Metairon, I. F. (1992). Seasonality of reprodutucive activity and abundance of veligers in queen conch, Strombus gigas. Fishery Bulletin, 90, 161-170. [ Links ]
1. Laboratorio de Biología y Cultivo de Moluscos. Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso, Km. 6, A.P. 73 Cordemex, C. P. 97310, Mérida, Yucatán, México; daldana@mda.cinvestav.mx
Received 1-VIII-2013 Corrected 14-II-2014 Accepted 24-III-2014
