Mating behaviour of Setipellis stigmatica (Gastropoda: Cepolidae) in captivity, morphology of dart and spermatophore
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Published
Jul 22, 2022
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Abstract
Setipellis stigmatica (Cepolidae) is a hermaphroditic, Cuban endemic land snail, of which mating behaviour has never been studied. Here, we described the mating behaviour and the use of the dart apparatus of S. stigmatica, in captivity, including data on the morphology of the dart and the spermatophore. The study was conducted in November 2012 and between January-February 2016. Thirteen adult individuals were collected in Escaleras de Jaruco, Cuba. Individuals were kept isolated in plastic containers between seven and 14 days before the mating sessions. Mating duration averaged 164 min and consisted of three stages: courtship, copulation and post-copulation. On average, courtship lasted 107 min, and included tactile and oral contacts, and consumption of mucus secreted by partially everted genitalia during intromission attempts. Copulation started simultaneously and lasted on average 43 min. During this stage took place the reciprocal exchange of spermatophores. The spermatophore was formed by three regions: neck, body and tail, without spines but with transversal ridges in the neck and body. There is a prominent bulge in the body just in its junction with the neck. We suggested that this hook could slow down spermatophore movement into the bursa copulatrix. Post-copulation average was 9 min; penis withdrawal established the beginning of this stage. During all mating stages, pairs did not exhibit circling movements but two uses of the dart apparatus were distinguished: rubbing and stabbing, all of which were mainly directed toward the anterior region of the partner’s body, usually without loss of the dart.
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Cuba, Mollusca, reproduction, endemic species
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Baminger, H., & Haase, M. (2000). Variation of distal genitalia in the simultaneously hermafroditic land snail Arianta arbustorum (Pulmonata, Stylommatophora) caused by sexual selection? Biological Journal of Linnean Society, 71(4), 599–613. https://doi. org/10.1111/j.1095-8312.2000.tb01280x.
Baur, B. (2010). Stylommatophoran gastropods. En J. L. Leonard y A. Córdoba-Aguilar (Eds.), The Evolution of primary sexual characters in animals (pp. 538–552). Oxford University Press.
Baur, B., & Baur, A. (2017). Reproductive strategies in stylommatophoran gastropods. En S. Saleuddin y S. Mukai (Eds.), Physiology of molluscs: a collection of selected reviews (pp. 311–377). Apple Academic Press Waretown.
Bosch-Diaz, C. (2021). Variabilidad de la conducta de apareamiento y los órganos genitales de Setipellis stigmatica (L. Pfeiffer, 1841) (Gastropoda: Cepolidae) [Tesis de Maestría, Universidad de La Habana].
Bouchet, P., Rocroi, J. P., Hausdorf, B., Kaim, A., Kano, Y., Nützel, A., Parkhaev, P., Schrödl, M., & Strong, E. E. (2017). Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia, 61(1–2), 1–526. https://doi. org/10.4002/040.061.0201.
Calcutt, J., Cuezzo, M. G., Jackson, M., & Salvador, R. B. (2020). Phylogenetic relationships and classification of Solaropsidae (Gastropoda: Stylommatophora). Archiv für Molluskenkunde, 149(2), 181–193. https://doi.org/10.1127/arch.moll/149/181-193.
Chase, R. (2007). The function of dart shooting in helicid snails. American Malacological Bulletin, 23(1), 183–189. https://doi.org/10.4003/0740-2783-23.1.183.
Davison, A., & Mordan, P. B. (2007). A literature database on the mating behavior of stylommatophoran land snails and slugs. American Malacological Bulletin, 23(1), 173–181. https://doi.org/10.4003/0740-2783-23.1.173.
Davison, A., Wade, C. M., Mordan, P. B., & Chiba, S. (2005). Sex and darts in slugs and snails (Mollusca: Gastropoda: Stylommatophora). Journal of Zoology, 267(4), 329–338. https:// doi.org/10.1017/S0952836905007648
Eberhard, W. G. (2011). Experiments with genitalia: a commentary. Trends in Ecology and Evolution, 26(1), 17–21. https://doi.org/10.1016/j.tree.2010.10.009.
Eberhard, W. G. (2015). Cryptic female choice and other types of post-copulatory sexual selection. En A. Peretti y A. Aisenberg (Eds.), Cryptic female choice in arthropods (pp. 1–26). Springer.
Espinosa, J., & Ortea, J. (1999). Moluscos terrestres del archipiélago cubano. Avicennia, 2, 1–137.
Garefalaki, M. E., Kalyva, S., Janicke, T., & Staikou, A. (2017). Intraspecific variation in reproductive characters is associated with the strength of sexual selection in the hermaphroditic land snail Cornu aspersum. Behavioural Ecology Sociobiology, 71(10), 150–161. https://doi.org/10.1007/s00265-017-2383-4.
Hernández, M. (2015). Mating behaviour in Jeanneretia ss. (Helicoidea: Cepolidae), endemic of the western region of Cuba. Unitas Malacologica Newletter, 35, 7–9.
Hernández, M., Backeljau, T., & Bauzá, M. A. (2021). Genital anatomy, jaw, and radula of the species of the genus Jeanneretia (Helicoidea: Cepolidae), endemic to western Cuba. Archiv für Molluskenkunde, 150, 13–29. https://doi.org/10.1127/arch.moll/150/013-029.
Hernández, M., Bauzá, M. A., & Backeljau, T. (2022). Genital anatomy, jaw and radula of Guladentia subtussulcata (Helicoidea, Cepolidae), endemic to western Cuba. Zookeys, 1080, 99–106. https://doi.org/10.3897/zookeys.1080.73194.
Hernández, M., Bauzá, M. A., Franke, S., & Fernández, A. (2020). A new genus and species of cepolid from Cuba (Pulmonata, Helicoidea). Ruthenica, 30(3), 155–164. https://doi. org/10.35885/ruthenica.2021.30(3).3.
Kimura, K., & Chiba, S. (2015). The direct cost of traumatic secretion transfer in hermaphroditic land snails: individuals stabbed with a love dart decrease lifetime fecundity. Proceedings of Royal Society B, 282(1804), 20143063. https://doi.org/10.1098/rspb.2014.3063.
Kimura, K., & Chiba, S. (2013). Delayed spermatophore removal in the land snail Euhadra peliomphala. Biological Journal of Linnean Society, 108(4), 806–811. https://doi. org/10.1111/bij.12008.
Kimura, K., Chiba, S., & Koene, J. M. (2014). Common effect of the mucus transferred during mating in two dart-shooting snail species from different families. Journal of Experimental Biology, 217, 1150–1153. https://doi.org/10.1242/jeb.095935.
Koene, J. M., & Chiba, S. (2006). The way of the samurai snail. American Naturalist, 168(4), 553–555. https://doi.org/10.1086/508028.
Koene, J. M., & Reyes-Tur, B. (2020). Cuban Cupids: Mating behaviour and physiology of dart-possessing land snails. The Malacologist, 70, 26–27.
Koene, J. M., & Schulenburg, H. (2005). Shooting darts: co-evolution and counter-adaptation in hermaphroditic snails. BMC Evolutionary Biology, 5, 25. https://doi.org/10.1186/1471- 2148-5-25.
Koene, J. M., Jansen, R. F., Ter Maat, A., & Chase, R. (2000). A conserved location for the central nervous system control of the mating behaviour in gastropod molluscs: evidence from a terrestrial snail. Journal of Experimental Biology, 203, 1071–1080. https://doi. org/10.1242/jeb.203.6.1071.
Lange, R., Reinhard, K., Michiels, N. K., & Anthes, N. (2013). Functions, diversity, and evolution of traumatic mating. Biological Reviews, 88, 585–601. https://doi.org/10.1111/brv.12018.
Lodi, M., & Koene, J. M. (2016). The love-darts of land snails: integrating physiology, morphology and behaviour. Journal of Molluscan Studies, 82(1), 1–10. https://doi.org/10.1093/mollus/ eyv046.
Lodi, M., Staikou, A., Janssen, R., & Koene, J. M. (2017). High level of sperm competition may increase transfer of accessory gland products carried by the love dart of land snails. Ecology and Evolution, 7(24), 11148–11156. https://doi.org/10.1002/ece3.3385.
Méndez-Hernández, A. A. (2011). Variabilidad del dardo en especies de moluscos de la familia Cepolidae: implicaciones para la selección sexual [Tesis de Licenciatura, Universidad de Oriente].
Miller, W. B., & Naranjo-García, E. (1991). Familial relationships and biogeography of the western American and Caribbean Helicoidea (Mollusca: Gastropoda: Pulmonata). American Malacological Bulletin, 8(2), 147–153. https://biostor.org/reference/143272.
Nordsieck, H. (1987). Revision des systems der Helicoidea (Gastropoda: Stylommatophora). Archiv für Molluskenkunde, 118(1/3), 9–50. https://doi.org/10.5962/bhl.title.141070.
Nordsieck, H. (2013). Higher classification of Helicoidea (Gastropoda: Stylommatophora) and the molecular analyses of their phylogeny. Disponible en https://www.hnords.de. Último acceso 12–VII–2014.
Nordsieck, H. (2017). Pulmonata, Stylommatophora, Helicoidea: Systematics with comments. ConchBooks, Hackenheim.
Razkin, O., Gómez-Moliner, B. J., Prieto, C. E., Martínez-Ortíz, A., Arrébola, J. R., Muñoz, B., Chueca, L. J., & Madeira, M. O. (2015). Molecular phylogeny of the western Palaearctic Helicoidea (Gastropoda, Stylommatophora). Molecular Phylogenetic Evolution, 83, 99–117. https://doi.org/10.1016/j.ympev.2014.11.014.
Reyes-Tur, B., Allen, J. A., Cuellar-Araujo, N., Hernández, N., Lodi, M., Méndez-Hernández, A. A., & Koene, J. M. (2015). Mating behaviour, dart shape and spermatophore morphology of the Cuban tree snail Polymita picta (Born, 1780). Journal of Molluscan Studies, 81, 187–195. https://doi.org/10.1093/mollus/eyu089.
Reyes-Tur, B., Fernández-Velázquez, A., & Ortiz, Y. (2000). Conducta de apareamiento y aspectos de la relación estructura-función del sistema reproductor en Polymita muscarum Lea 1834, (Gastropoda: Pulmonata). Revista Biología, 14(2), 160–166.
Reyes-Tur B., Gordillo-Pérez, M. J., Bosch-Diaz, C., Rodríguez-Potrony, H., & Rodríguez- Matos, J. (2020). Apareamiento, espermatóforo y aparato del dardo de Polymita brocheri (Gastropoda: Cepolidae): conducta y morfología. Revista Cubana de Ciencias Biológicas, 8(1), 1–16.
Reyes-Tur, B., & Koene, J. M. (2007). Use of dart apparatus by hermaphroditic land snail Polymita muscarum (Lea, 1834). Animal Biology, 57(2), 261–266. https://doi. org/10.1163/157075607780377974.
Rodríguez-Potrony, H., Bosch-Diaz, C., Gordillo-Pérez, M. J., Rodríguez-Matos, J., & Reyes-Tur, B. (2020). Parámetros reproductivos, historia de vida y crecimiento de Polymita brocheri (Gastropoda: Cepolidae) en condiciones de cautiverio. Poeyana, 510, 10–17.
Schärer, L., & Ramm, S. A. (2016). Hermaphrodites. En R. M. Kliman (Ed.), Encyclopedia of Evolutionary Biology (Vol. 2, pp. 212–224). Elsevier Science Publishing.
Schileyko, A. A. (1991). Taxonomic status phylogenetic relations and system of the Helicoidea sensu lato. Archiv für Molluskenkunde, 120(4/6), 187–236.
Schileyko, A. A. (2004). Treatise on recent terrestrial pulmonate molluscs. Part 12. Bradybaenidae, Monadeniidae, Xanthonyc- hidae, Epiphragmophoridae, Helminthoglyptidae, Elonidae, Humboldtianidae, Sphincterochilidae, Cochlicellidae. Ruthenica, 2, 1627–1763.
Sei, M., Robinson, D. G., Geneva, A. J., & Rosenberg, G. (2017). Doubled helix: Sagdoidea is the overlooked sister group of Helicoidea (Mollusca: Gastropoda: Pulmonata). Biological Journal of Linnean Society, 122(4), 697–728. https://doi.org/10.1093/biolinnean/blx082.
Stewart, M. J., Wang, T., Koene, J. M., Storey, K. B., & Cummins, S. F. (2016). A “love” dart allohormone identified in the mucous glands of hermaphroditic land snails. Journal of Biological Chemistry, 291(15), 7938–7950. https://doi.org/10.1074/jbc.M115.704395.
Tompa, A. S. (1984). Land snails (Stylommatophora). En A. S. Tompa, N. H. Verdonk y J. A. M. van den Biggelaar (Eds.), The Mollusca (Vol. 7, pp. 47–140). Elsevier Science Publishing.
Wilcox, D., Dove, B., McDavid D., & Greer, D. (2002). UTHSCSA Image tool for Windows, version 3.0. University of Texas, Health Science Center.
Baminger, H., & Haase, M. (2000). Variation of distal genitalia in the simultaneously hermafroditic land snail Arianta arbustorum (Pulmonata, Stylommatophora) caused by sexual selection? Biological Journal of Linnean Society, 71(4), 599–613. https://doi. org/10.1111/j.1095-8312.2000.tb01280x.
Baur, B. (2010). Stylommatophoran gastropods. En J. L. Leonard y A. Córdoba-Aguilar (Eds.), The Evolution of primary sexual characters in animals (pp. 538–552). Oxford University Press.
Baur, B., & Baur, A. (2017). Reproductive strategies in stylommatophoran gastropods. En S. Saleuddin y S. Mukai (Eds.), Physiology of molluscs: a collection of selected reviews (pp. 311–377). Apple Academic Press Waretown.
Bosch-Diaz, C. (2021). Variabilidad de la conducta de apareamiento y los órganos genitales de Setipellis stigmatica (L. Pfeiffer, 1841) (Gastropoda: Cepolidae) [Tesis de Maestría, Universidad de La Habana].
Bouchet, P., Rocroi, J. P., Hausdorf, B., Kaim, A., Kano, Y., Nützel, A., Parkhaev, P., Schrödl, M., & Strong, E. E. (2017). Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia, 61(1–2), 1–526. https://doi. org/10.4002/040.061.0201.
Calcutt, J., Cuezzo, M. G., Jackson, M., & Salvador, R. B. (2020). Phylogenetic relationships and classification of Solaropsidae (Gastropoda: Stylommatophora). Archiv für Molluskenkunde, 149(2), 181–193. https://doi.org/10.1127/arch.moll/149/181-193.
Chase, R. (2007). The function of dart shooting in helicid snails. American Malacological Bulletin, 23(1), 183–189. https://doi.org/10.4003/0740-2783-23.1.183.
Davison, A., & Mordan, P. B. (2007). A literature database on the mating behavior of stylommatophoran land snails and slugs. American Malacological Bulletin, 23(1), 173–181. https://doi.org/10.4003/0740-2783-23.1.173.
Davison, A., Wade, C. M., Mordan, P. B., & Chiba, S. (2005). Sex and darts in slugs and snails (Mollusca: Gastropoda: Stylommatophora). Journal of Zoology, 267(4), 329–338. https:// doi.org/10.1017/S0952836905007648
Eberhard, W. G. (2011). Experiments with genitalia: a commentary. Trends in Ecology and Evolution, 26(1), 17–21. https://doi.org/10.1016/j.tree.2010.10.009.
Eberhard, W. G. (2015). Cryptic female choice and other types of post-copulatory sexual selection. En A. Peretti y A. Aisenberg (Eds.), Cryptic female choice in arthropods (pp. 1–26). Springer.
Espinosa, J., & Ortea, J. (1999). Moluscos terrestres del archipiélago cubano. Avicennia, 2, 1–137.
Garefalaki, M. E., Kalyva, S., Janicke, T., & Staikou, A. (2017). Intraspecific variation in reproductive characters is associated with the strength of sexual selection in the hermaphroditic land snail Cornu aspersum. Behavioural Ecology Sociobiology, 71(10), 150–161. https://doi.org/10.1007/s00265-017-2383-4.
Hernández, M. (2015). Mating behaviour in Jeanneretia ss. (Helicoidea: Cepolidae), endemic of the western region of Cuba. Unitas Malacologica Newletter, 35, 7–9.
Hernández, M., Backeljau, T., & Bauzá, M. A. (2021). Genital anatomy, jaw, and radula of the species of the genus Jeanneretia (Helicoidea: Cepolidae), endemic to western Cuba. Archiv für Molluskenkunde, 150, 13–29. https://doi.org/10.1127/arch.moll/150/013-029.
Hernández, M., Bauzá, M. A., & Backeljau, T. (2022). Genital anatomy, jaw and radula of Guladentia subtussulcata (Helicoidea, Cepolidae), endemic to western Cuba. Zookeys, 1080, 99–106. https://doi.org/10.3897/zookeys.1080.73194.
Hernández, M., Bauzá, M. A., Franke, S., & Fernández, A. (2020). A new genus and species of cepolid from Cuba (Pulmonata, Helicoidea). Ruthenica, 30(3), 155–164. https://doi. org/10.35885/ruthenica.2021.30(3).3.
Kimura, K., & Chiba, S. (2015). The direct cost of traumatic secretion transfer in hermaphroditic land snails: individuals stabbed with a love dart decrease lifetime fecundity. Proceedings of Royal Society B, 282(1804), 20143063. https://doi.org/10.1098/rspb.2014.3063.
Kimura, K., & Chiba, S. (2013). Delayed spermatophore removal in the land snail Euhadra peliomphala. Biological Journal of Linnean Society, 108(4), 806–811. https://doi. org/10.1111/bij.12008.
Kimura, K., Chiba, S., & Koene, J. M. (2014). Common effect of the mucus transferred during mating in two dart-shooting snail species from different families. Journal of Experimental Biology, 217, 1150–1153. https://doi.org/10.1242/jeb.095935.
Koene, J. M., & Chiba, S. (2006). The way of the samurai snail. American Naturalist, 168(4), 553–555. https://doi.org/10.1086/508028.
Koene, J. M., & Reyes-Tur, B. (2020). Cuban Cupids: Mating behaviour and physiology of dart-possessing land snails. The Malacologist, 70, 26–27.
Koene, J. M., & Schulenburg, H. (2005). Shooting darts: co-evolution and counter-adaptation in hermaphroditic snails. BMC Evolutionary Biology, 5, 25. https://doi.org/10.1186/1471- 2148-5-25.
Koene, J. M., Jansen, R. F., Ter Maat, A., & Chase, R. (2000). A conserved location for the central nervous system control of the mating behaviour in gastropod molluscs: evidence from a terrestrial snail. Journal of Experimental Biology, 203, 1071–1080. https://doi. org/10.1242/jeb.203.6.1071.
Lange, R., Reinhard, K., Michiels, N. K., & Anthes, N. (2013). Functions, diversity, and evolution of traumatic mating. Biological Reviews, 88, 585–601. https://doi.org/10.1111/brv.12018.
Lodi, M., & Koene, J. M. (2016). The love-darts of land snails: integrating physiology, morphology and behaviour. Journal of Molluscan Studies, 82(1), 1–10. https://doi.org/10.1093/mollus/ eyv046.
Lodi, M., Staikou, A., Janssen, R., & Koene, J. M. (2017). High level of sperm competition may increase transfer of accessory gland products carried by the love dart of land snails. Ecology and Evolution, 7(24), 11148–11156. https://doi.org/10.1002/ece3.3385.
Méndez-Hernández, A. A. (2011). Variabilidad del dardo en especies de moluscos de la familia Cepolidae: implicaciones para la selección sexual [Tesis de Licenciatura, Universidad de Oriente].
Miller, W. B., & Naranjo-García, E. (1991). Familial relationships and biogeography of the western American and Caribbean Helicoidea (Mollusca: Gastropoda: Pulmonata). American Malacological Bulletin, 8(2), 147–153. https://biostor.org/reference/143272.
Nordsieck, H. (1987). Revision des systems der Helicoidea (Gastropoda: Stylommatophora). Archiv für Molluskenkunde, 118(1/3), 9–50. https://doi.org/10.5962/bhl.title.141070.
Nordsieck, H. (2013). Higher classification of Helicoidea (Gastropoda: Stylommatophora) and the molecular analyses of their phylogeny. Disponible en https://www.hnords.de. Último acceso 12–VII–2014.
Nordsieck, H. (2017). Pulmonata, Stylommatophora, Helicoidea: Systematics with comments. ConchBooks, Hackenheim.
Razkin, O., Gómez-Moliner, B. J., Prieto, C. E., Martínez-Ortíz, A., Arrébola, J. R., Muñoz, B., Chueca, L. J., & Madeira, M. O. (2015). Molecular phylogeny of the western Palaearctic Helicoidea (Gastropoda, Stylommatophora). Molecular Phylogenetic Evolution, 83, 99–117. https://doi.org/10.1016/j.ympev.2014.11.014.
Reyes-Tur, B., Allen, J. A., Cuellar-Araujo, N., Hernández, N., Lodi, M., Méndez-Hernández, A. A., & Koene, J. M. (2015). Mating behaviour, dart shape and spermatophore morphology of the Cuban tree snail Polymita picta (Born, 1780). Journal of Molluscan Studies, 81, 187–195. https://doi.org/10.1093/mollus/eyu089.
Reyes-Tur, B., Fernández-Velázquez, A., & Ortiz, Y. (2000). Conducta de apareamiento y aspectos de la relación estructura-función del sistema reproductor en Polymita muscarum Lea 1834, (Gastropoda: Pulmonata). Revista Biología, 14(2), 160–166.
Reyes-Tur B., Gordillo-Pérez, M. J., Bosch-Diaz, C., Rodríguez-Potrony, H., & Rodríguez- Matos, J. (2020). Apareamiento, espermatóforo y aparato del dardo de Polymita brocheri (Gastropoda: Cepolidae): conducta y morfología. Revista Cubana de Ciencias Biológicas, 8(1), 1–16.
Reyes-Tur, B., & Koene, J. M. (2007). Use of dart apparatus by hermaphroditic land snail Polymita muscarum (Lea, 1834). Animal Biology, 57(2), 261–266. https://doi. org/10.1163/157075607780377974.
Rodríguez-Potrony, H., Bosch-Diaz, C., Gordillo-Pérez, M. J., Rodríguez-Matos, J., & Reyes-Tur, B. (2020). Parámetros reproductivos, historia de vida y crecimiento de Polymita brocheri (Gastropoda: Cepolidae) en condiciones de cautiverio. Poeyana, 510, 10–17.
Schärer, L., & Ramm, S. A. (2016). Hermaphrodites. En R. M. Kliman (Ed.), Encyclopedia of Evolutionary Biology (Vol. 2, pp. 212–224). Elsevier Science Publishing.
Schileyko, A. A. (1991). Taxonomic status phylogenetic relations and system of the Helicoidea sensu lato. Archiv für Molluskenkunde, 120(4/6), 187–236.
Schileyko, A. A. (2004). Treatise on recent terrestrial pulmonate molluscs. Part 12. Bradybaenidae, Monadeniidae, Xanthonyc- hidae, Epiphragmophoridae, Helminthoglyptidae, Elonidae, Humboldtianidae, Sphincterochilidae, Cochlicellidae. Ruthenica, 2, 1627–1763.
Sei, M., Robinson, D. G., Geneva, A. J., & Rosenberg, G. (2017). Doubled helix: Sagdoidea is the overlooked sister group of Helicoidea (Mollusca: Gastropoda: Pulmonata). Biological Journal of Linnean Society, 122(4), 697–728. https://doi.org/10.1093/biolinnean/blx082.
Stewart, M. J., Wang, T., Koene, J. M., Storey, K. B., & Cummins, S. F. (2016). A “love” dart allohormone identified in the mucous glands of hermaphroditic land snails. Journal of Biological Chemistry, 291(15), 7938–7950. https://doi.org/10.1074/jbc.M115.704395.
Tompa, A. S. (1984). Land snails (Stylommatophora). En A. S. Tompa, N. H. Verdonk y J. A. M. van den Biggelaar (Eds.), The Mollusca (Vol. 7, pp. 47–140). Elsevier Science Publishing.
Wilcox, D., Dove, B., McDavid D., & Greer, D. (2002). UTHSCSA Image tool for Windows, version 3.0. University of Texas, Health Science Center.
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How to Cite
Reyes-Tur, B., Bosch-Diaz, C., & Hernández, M. (2022). Mating behaviour of Setipellis stigmatica (Gastropoda: Cepolidae) in captivity, morphology of dart and spermatophore. Novitates Caribaea, (20), 69–83. https://doi.org/10.33800/nc.vi20.310
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