Keywords
controlled conditions
embryonic development
gasteropods
Gulf of California
reproductive strategy
condiciones controladas
conservación
desarrollo embrionario
estrategia reproductiva
gastrópodos
Golfo de California
How to Cite
Abstract
ABSTRACT
Introduction: The marine snail Hexaplex nigritus is a heavily exploited muricid in the Gulf of California for consumption and handcrafts. When they reproduce, adults aggregated in the form of artificial reefs facilitating their identification and extraction, situation that has reduced their population in that area. Objective: In order to investigate the spawning and intracapsular and larval development of this species as tools for its production in captivity for repopulation purposes. Methods: Eighteen brooders were collected and kept in a closed system with controlled parameters and feeding from April 2017 to September 2018. Growth of parents, spawning of ovigerous masses, number of capsules, and number of embryos and larvae within the capsules, were registered. The main morphological structures of embryos and larvae were documented according to their development. Results: Intracapsular embryonic development and veliger larva until its establishment lasted 14-15 and 31-32 days, respectively. Each 80-88 mm length female produced around 4 ovigerous masses, 627 capsules and 663 993 extracapsular veliger larvae per year. Conclusions: Easy adaptation and reproductive potential shown by H. nigritus in the laboratory are presented as promising strategies for its repopulation and conservation.
References
Barnes, R.S.K. (1990). Reproductive strategies in contrasting populations of the coastal gastropod Hydrobia ulvae. II. Longevity and life-time egg production. Journal of Experimental Marine Biology and Ecology, 138(3), 183-200. DOI: 10.1016/0022-0981(90)90166-A
Bayne, B.L. (1976). Aspects of reproduction in bivalve molluscs. Estuarine Processes. Uses, Stresses, and Adaptation to the Estuary. Massachusetts, United States of America: Academic Press.
Bayne, B.L., & Newell, R.C. (1983). 9. Physiological energetics of marine molluscs. The Mollusca. Physiology. Massachusetts, United States of America: Academic Press.
Benkendorff, K., Bremner, J.B., & Davis, A.R. (2000). Tyrian purple precursors in the egg masses of the Australian muricid, Dicathais orbita: A possible defensive role. Journal of Chemical Ecology, 26(4), 1037-1050. DOI: 10.1023/A:1005441116095
Benkendorff, K., Westley, C.B., & Gallardo, C.S. (2004). Observations on the production of purple pigments in the egg capsules, hypobranchial and reproductive glands from seven species of Muricidae (Gastropoda: Mollusca). Invertebrate Reproduction & Development, 46(2-3): 93-102. DOI: 10.1080/07924259.2004.9652612
Brokordt, K. (2003). Sex differences in reproductive investment: maternal care reduces escape response capacity in the whelk Buccinum undatum. Journal of Experimental Marine Biology and Ecology, 291, 161-180. DOI: 10.1016/S0022-0981(03)00119-9
Brusca, R.C., Kimrey, E., & Moore, W. (2004). A seashore guide to the northern Gulf of California. Tucson, United States of America: Arizona-Sonora Desert Museum.
Buckland-Nicks, J., & Chia, F.S. (1990). Egg capsule formation and hatching in the marine snail Littorina sitkana. Philosophical Transactions of the Royal Society of London B, 326, 159-176.
Camacho-Sánchez, F.Y. (2009). Efecto de la temperatura sobre el desarrollo embrionario del caracol burro Hexaplex (Muricanthus) nigritus (Philippi, 1845), en condiciones de laboratorio (Tesis de Licenciatura). Universidad de Occidente, Sinaloa, México.
Camacho-Sánchez, F.Y. (2012). Desarrollo embrionario y metamorfosis del caracol chino Hexaplex (Muricanthus) nigritus (Philipi, 1845) en condiciones de laboratorio (Tesis de Maestría). Instituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, México.
Cañete, J.I., Gallardo, C.S., Céspedes, T., Cárdenas, C.A., & Santana, M. (2012). Encapsulated development, spawning and early veliger of the ranellid snail Fusitriton magellanicus (Röding, 1798) in the cold waters of the Magellan Strait, Chile. Latin American Journal of Aquatic Research, 40(4), 914-928. DOI: 103856/vol40-issue4-fulltext-8
Chaparro, O.R., & Flores, M.L. (2002). Reproductive output of Crepidula fecunda females: distribution of energy in the production of gametes and capsules walls. New Zealand Journal of Marine and Freshwater Research, 36, 661-673. DOI: 10.1080/00288330.2002.9517122
Chatzinikolaou, E., & Richardson, C.A. (2010). Parental size and environmental conditions affect egg capsule production by Nassarius reticulatus (Linnaeus 1758) (Gastropoda: Nassariidae). Journal of Experimental Marine Biology and Ecology, 390, 14-21. DOI: 10.1016/j.jembe.2010.04.029
CITES. (2020). Convención sobre el Comercio Internacional de Especies Amenazadas de Fauna y Flora Silvestres. Recuperado de www.ckecklist.cites.org/#/es
CONAPESCA. (2020). Comisión Nacional de Acuacultura y Pesca. Recuperado de www.acuasesor.conapesca.gob.mx/anuario.php
Cudney-Bueno, R. (2007). Marine reserves, community-based management, and small-scale benthic fisheries in the Gulf of California, Mexico (Doctoral Dissertartion). University of Arizona, Arizona, United States of America.
Cudney-Bueno, R., & Rowell, K. (2008). The black murex snail, Hexaplex nigritus (Mollusca, Muricidae), in the Gulf of California, Mexico: II. Growth, longevity, and morphological variations with implications for management of a rapidly declining fishery. Bulletin of Marine Science, 83(2), 299-313.
Cudney-Bueno, R., Prescott, R., & Hinojosa-Huerta, O. (2008). The black murex snail, Hexaplex nigritus (Mollusca, Muricidae), in the Gulf of California, Mexico: I. Reproductive ecology and breeding aggregations. Bulletin of Marine Science, 83(2), 285-298.
Cumplido, M., Pappalardo, P., Fernández, M., Averjub, A., & Bigatti, G. (2011). Embryonic develoment, feeding and intracapsular availability in Thophon geversianus (Gastropods: Muricidae). Journal of Molluscan Studies, 77, 429-436. DOI: 10.1093/mollus/eyr025
Dame, R.F. (1996). Ecology of marine bivalves: an ecosystem approach. Boca Raton, United States of America: CRC Press.
D’Asaro, C.N. (1966). The egg capsules, embryogenesis, and early organogenesis of a common oyster predator, Thais haemastoma floridana (Gastropoda: Prosobranchia). Bulletin of Marine Sciences, 16(4), 884-914.
D’Asaro, C.N. (1970). Egg capsules of prosobranch mollusks from South Florida and The Bahamas and notes on spawning in the laboratory. Bulletin of Marine Sciences, 20(2), 414-440.
D’Asaro, C.N. (1992). Gunnar Thorson's world-wide collection of prosobranch egg capsules: Muricidae. Ophelia, 35(1), 1-101.
Fabioux, C., Huvet, A., Le Souchu, P., Le Pennec, M., & Pouvreau, S. (2005). Temperature and photoperiod drive Crassostrea gigas reproductive internal clock. Aquaculture, 250(1-2), 458-470. DOI: 10.1016/j.aquaculture.2005.02.038
Fu, T., Guerette, P.A., Tan, R.Y.T., Zhao, H., Schefer, L., Mezzenga, R., & Miserez, A. (2015). Biomimetic self-assambly of recombinant marine snail egg capsule proteins into structural coiled-coil units. Journal of Materials Chemistry B, 3, 2671-2684. DOI: 10.1039/c4tb01434k
Góngora, G.A. (1999). Efecto de la temperatura sobre el desarrollo embrionario del caracol marino Strombus pugilis (L.) (Tesis de Licenciatura). Universidad Autónoma de Yucatán, Yucatán, México.
Góngora-Gómez, A.M., Domínguez-Orozco, A.L., Muñoz-Sevilla, N.P., & Rodríguez-Gil, L.A. (2007). Obtención de masas ovígeras del caracol lancetilla, Strombus pugilis (Mesogastropoda: Strombidae) en condiciones de laboratorio. Revista de Biología Tropical, 55(1), 183-188.
Góngora-Gómez, A.M., García-Ulloa, M., & Domínguez, A. (2010). Desarrollo embrionario del caracol chino Muricanthus nigritus para su repoblación y preservación en Guasave, Sinaloa, México. In J.C. Chávez-Comparán & J. Mimbela-López (Eds.), Avances sobre Investigaciones Marinas y Acuícolas del Pacífico Mexicano (1ª ed., pp 112-117). Colima, México: Universidad de Colima.
Góngora-Gómez, A.M., García-Ulloa, M., Domínguez-Orozco, A.L., & Camacho-Sánchez, F.Y. (2011). Aspectos reproductivos cuantitativos del caracol murex negro, Hexaplex nigritus (Philipi, 1845) en condiciones de laboratorio. Ciencia y Mar, XV(44), 31-34.
González, K.A., & Gallardo, C.S. (1999). Embryonic and larval development of the muricid snail Chorus giganteus (Lesson, 1829) with and assessment of the developmental nutrition source. Ophelia, 51(2), 77-92. DOI: 10.1080/00785326.1999.10409400
Güler, M., & Lök, A. (2014). Embryonic development and intracapsular feeding in Hexaplex trunculus (Gastropoda: Muricidae). Marine Ecology, 35, 193-203. DOI: 10.1111/maec.12066
Ito, K. (1997). Egg-size and -number variations related to maternal size and egg, and the relationship between egg size and larval characteristics in an annual marine gastropod, Haloa japonica (Opisthobranchia; Cephalaspidea). Marine Ecology Progress Series, 152, 187-195.
Jagadis, I., Shunmugasundaram, K., Sathakkathulla, Md., & Mohanraj, T. (2013). Spawning, intracapsular development and production potential of viable juveniles of a murex Chicoreus virgineus var. ponderosa Sowerby under laboratory conditions. Agricultural Sciences, 4, 244-248. DOI: 10.4236/as.2013.45035
Jagadis, I., Kavitha, M., Padmanathan, J., Maharshi, A., & Varadarajakumar, A. (2017). Lessons on broodstock maintenance, spawning, larval rearing and juvenile production of marine gastropods of ornamental value. Aquaculture Research, 48(5), 2581-2592. DOI: 10.1111/are.13094
Lima, G., & Pechenik, J. (1985). The influence of temperature on growth rate and length of larval life of the gastropod, Crepidula plana Say. Journal of Experimental Marine Biology and Ecology, 90, 55-71. DOI: 10.1016/0022-0981(85)90074-7
Lord, A. (1986). Are the contents of egg capsules of the marine gastropod Nucella lapillus (L.) axenic? American Malacological Bulletin, 42, 201-203.
Mahmoud, M.A.M., Mohammed, T.A.A., & Yassien, M.H. (2013). Spawning frequency, larval development and growth of Muricid gastropod Chicoreus ramosus (Linnaeus, 1758) in the Laboratory at Hurghada, Northern red Sea, Egypt. Egyptian Journal of Aquatic Research, 39, 125-131. DOI: 10.1016/j.ejar.2013.07.002
Moffa, R., Chávez, J., Bastardo, G., Villalba, W., & Crescini, R. (2017). Desarrollo intracapsular del gasterópodo Fasciolaria tulipa (Linnaeus, 1758) (Mollusca: Neograstropoda: Fasciolariidae) en condiciones de laboratorio. Amici Molluscarum, 25(1-2), 19-26.
Munguía-Vega, A., Torre, J., Turk-Boyer, P., Marinone, G., Lavin, M., … Cudney-Bueno, R. (2015). PANGAS: An Interdisciplinary Ecosystem-Based Research Framework for Small-Scale Fisheries in the Northern Gulf of California. Journal of the Southwest, 57(2-3), 337-390.
Naegel, L., & Cooksey, C.J. (2002). Tyrian purple from marine muricids, especially from Plicopurpura pansa (Gould, 1853). Journal of Shellfish Research, 21(1), 193-200.
Naegel, L.C.A., & Gómez del Prado-Rosas, M.C. (2004). Embriogénesis y desarrollo larvario intra-capsular de Plicopurpura pansa (Gould, 1853) (Prosobranchia, Muricidae) en condiciones de laboratorio. Ciencias Marinas, 30(2), 297-310.
Najmudeen, T.M., & Victor, A.C.C. (2004). Seed production and juvenile rearing of the tropical abalone Haliotis varia Linnaeus 1758. Aquaculture, 234, 277-292. DOI: 10.1016/j.aquaculture.2003.12.013
Navarro, J.M., Leiva, G.E., Gallardo, C.S., & Varela, C. (2002). Influence of diet and temperature on physiological energetics of Chorus giganteus (Gastropoda: Muricidae) during reproduction conditioning. New Zealand Journal of Marine and Freshwater Research, 36, 321-332. DOI: 10.1080/00288330.2002.9517089
Pastorino, G., Penchaszadeh, P.E., & Scarabino, F. (2007). Egg capsules, eggs and embryos of the southwestern Atlantic gastropod Coronium coronatum (Gastropods: Muricidae). Journal of Molluscan Studies, 73, 61-65. DOI: 10.1093/mollus/eyp024
Pechenik, J., & Lima, G. (1984). Relationship between growth, differentiation, and length of larval life for individually reared larvae of the marine gastropod, Crepidula fornicata. The Biological Bulletin, 166, 537-54.
Pechenik, J.A., Chang, S.C., & Lord, A. (1984). Encapsulated development of the marine prosobranch gastropod Nucella lapillus. Marine Biology, 78, 223-229. DOI: 10.1007/BF00394705
Poutiers, J.M. (1995). Bivalvos. In W. Fischer, F. Krupp, W. Schneider, C. Sommer, K. Carpenter, & V.H. Neim (Eds.), Guía FAO para la identificación de especies para los fines de pesca: Pacífico Centro-Oriental: Invertebrados (1st. ed., pp. 224-297). Rome, Italy: Food and Agriculture Organization.
Prescott, R., & Cudney-Bueno, R. (2008). Mobile ‘reefs’ in the northeastern Gulf of California: aggregations of black murex snails Hexaplex nigritus as habitat for invertebrates. Marine Ecology Progress Series, 367, 185-192. DOI: 10.3354/meps07450
R Core Team. (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from: https://www.R-project.org
Rawlings, T.A. (1995). Direct observation of encapsulated development in Muricid Gastropods. The Veliger, 38(1), 54-60.
Riquelme, C.E., & Chávez, P.C. (1991). Colonization of vibrios on developmental stages of Concholepas concholepas (Bruguière, 1789) (Mollusca: Muricidae). In K. Koop (Ed.), Ecology of Marine Aquaculture. Workshop on Research in Aquaculture (1st. ed., pp. 84-95). Chile: International Foundation for Science.
Romero, M.S., Lohrmann, K., Bellolio, G., & Dupre, E. (2003). Comparative observations on reproduction, spawning, and early veligers of three common subtidal mesograstropods from North Central Chile. The Veliger, 46(1), 50-59.
Romero, M.S., Gallardo, C.S., & Bellolio, G. (2004). Egg laying and embryonic-larval development in the snail Thais (Stramontia) chocolata (Duclos, 1832) with observations on its evolutionary relationships within the Muricidae. Marine Biology, 145(4), 681-692. DOI 10.1007/s00227-004-1368-9
Schwab, D.B., & Allen, J.D. (2014). Size-specific maternal effects in response to predator cues in an intertidal snail. Marine Ecology Progress Series, 499, 127-141. DOI: 10.3354/meps10652
SEMARNAT. (2020). Secretaría de Medio Ambiente y Recursos Naturales. Recuperado de www.dgeiawf.semarnat.gob.mx:8080/ibi_apps/WFServlet?IBIF.ex=D2_PESCA01_03&IBIC_user=dgeia.mce&IBIC_pass=dgeia_mce&NOMBREANIO=*
Smith, K.E., & Thatje, S. (2013). Nurse egg consumption and intracapsular development in the common whelk Buccinum undatum (Linnaeus 1758). Helgoland Marine Research, 67, 109-120. DOI: 10.1007/s10152-012-0308-1
Stump, T.E. (1975). Pleistocene molluscan paleoecology and community structure of the Puerto Libertad region, Sonora, Mexico. Palaeogeography, Palaeoclimatology, Palaeoecology, 17(3), 177-226.
Wayne, N.L. (2001). Regulation of seasonal reproduction in mollusks. Journal of Biological Rhythms, 16(4), 391-402. DOI: 10.1177/074873001129002097
Zupo, V., & Patti, F.P. (2009). Laboratory spawning, larval development and metamorphosis of the marine snail Nassarius reticulatus (L.) (Caenogastropoda, Nassaridae). Invertebrate Reproduction and Development, 53(1), 23-31. DOI: 10.1080/07924259.2009.9652286
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Copyright (c) 2020 Andrés Martín Góngora-Gómez, Misael Pinzón-Zúñiga, Juan Antonio Hernández-Sepúlveda, Manuel II García-Ulloa, Brenda Paulina Villanueva-Fonseca, Manuel García-Ulloa