Histological study of the talon and glandular sac annex of Megalobulimus (Gastropoda, Strophocheilidae)

Authors

  • Haydee Temoche Universidad Nacional Mayor de San Marcos, Facultad de Ciencias Biológicas, Unidad de Posgrado, Lima, Perú. https://orcid.org/0000-0001-5654-9447
  • Betty Shiga Universidad Nacional Mayor de San Marcos, Facultad de Ciencias Biológicas, Lima, Perú. https://orcid.org/0000-0001-6460-6982
  • Rina Ramírez (2) Universidad Nacional Mayor de San Marcos, Facultad de Ciencias Biológicas, Lima, Perú; (3) Universidad Nacional Mayor de San Marcos, Museo de Historia Natural, Departamento de Malacología, Av. Arenales 1256, CP: 15072, Lima, Perú. https://orcid.org/0000-0003-1924-5844

DOI:

https://doi.org/10.15381/rpb.v17i3.27491

Keywords:

Land snails, carrefour gland, spermathecal tubules, oriented spermatozoa, synapomorphy

Abstract

In this study, the histology of the talon and the annex glandular sac (AGS) of the reproductive system from five species of Megalobulimus (Gastropoda, Stylommatophora, Strophocheilidae) is described. Hematoxylin-Eosin staining technique was used. It was found that the talon is a compact muscular structure housing the fertilization pouch, a tubular structure lined by folded ciliated cylindrical epithelium, to whose proximal end the hermaphroditic duct connects. This duct terminates in the fertilization chamber, from which the spermathecal tubules originate. These tubules branch out to their blind ends and store exogenous sperm. In the tubules, spermatozoa were observed, mostly with their heads attached to the ciliated epithelial cells and their tails free in the lumen. The wall of the AGS has an outer layer of smooth muscle and, lining the lumen, a non-ciliated glandular columnar epithelium with various degrees of folding and subepithelial mucous cells. The secretions from these cells flow into the collecting duct near the base of the talon. Far from the albumen gland, a similar substance was observed along with exogenous sperm in the spermathecal tubules. Differences between species were identified, with the most significant and phylogenetically relevant feature being the differentiation of the talon, which was more pronounced in M. capillaceus compared to the other four species studied (M. popelairianus, M. carrikeri, M. leucostoma, and M. maximus).

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References

Barker GM. 2001. Gastropods on land: phylogeny, diversity and adaptive morphology. In: Barker GM, editor. The Biology of terrestrial molluscs. Ch. 1. Cambridge: CABI Publishing; p. 1-146. https://doi.org/10.1079/9780851993188.0000

Bawab FEl-. 2020. Invertebrate embryology and reproduction. London: Academic Press; 558 pp. https://doi.org/10.1016/C2016-0-04781-2

Beese K. 2007. The evolution of male and female reproductive traits in simultaneously hermaphroditic terrestrial gastropods. Tesis, Doctor en Filosofía. Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel.

Beese K, Armbruster GFJ, Beier K Baur B. 2009. Evolution of female sperm-storage organs in the carrefour of stylommatophoran gastropods. Journal of Zoological Systematics and Evolutionary Research 47: 49-60. https://doi.org/10.1111/j.1439-0469.2008.00491.x

Bequaert JC. 1948. Monograph of the Strophocheilidae, a Neotropical family of terrestrial mollusks. Bulletin of the Museum of Comparative Zoology 100 (1): 1-210.

Beltramino AA. 2016. Estudios morfo-anatómicos y moleculares de Megalobulimus spp. (Gastropoda Pulmonata) en la Argentina, principalmente de la Provincia De Misiones. Tesis, Doctor en Ciencias Naturales. La Plata: Universidad Nacional de La Plata. https://sedici.unlp.edu.ar/handle/10915/51969

Bojat N, Sauder U, Haase M. 2001. The spermathecal epithelium, sperm and their interactions in the hermaphroditic land snail Arianta arbustorum (Pulmonata, Stylommatophora). Zoomorphology 120: 149–157. https://doi.org/10.1007/s004350000031

Bojat NC, Sauder U, Haase M. 2002. Functional anatomy of the sperm storage organs in Pulmonata: the simple spermatheca of Bradybaena fruticum (Gastropoda, Stylommatophora). Zoomorfology 121: 243–255. https://doi.org/10.1007/s00435-002-0062-z

Borda V. 2014. Patrones de polimorfismo molecular y morfológico de Megalobulimus (mollusca, gastropoda) en el sur de los Andes del Perú. Tesis, Maestría en Biología Molecular. Lima: Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos. https://hdl.handle.net/20.500.12672/3855

Borda V, Ramírez R. 2013. Re-characterization of the Red-lip Megalobulimus (Gastropoda: Strophocheilidae) from Peru with description of a new species. Zoologia 30(6): 675–691. https://doi.org/10.1590/S1984-46702013005000008

Borda V, Ramírez R. 2016. The Genus Megalobulimus (Gastropoda: Strophocheilidae) from Peruvian Andes: Re-Description of Megalobulimus leucostoma and description of two new species. American Malacological Bulletin 34(1): 15–27. https://doi.org/10.4003/006.034.0108

Dennis MM, Molnár K, Kriska G, & Lőw P. 2021. Mollusca: Gastropoda. In: LaDouceur, EE, editor. Invertebrate histology. Hoboken, NJ: Wiley-Blackwell; p. 87 – 132.

Gómez BJ. 1991. Morphological and histological study of the genital ducts of Cryptazeca monodonta (Pulmonata, Orthurethra), with special emphasis on the auxiliary copulatory organ. Zoomorphology 111: 95–102. https://doi.org/10.1007/BF01632875

Gómez BJ. 2001. Structure and functioning of the reproductive system. In: Barker GM, editor. The Biology of terrestrial molluscs. Ch. 8. Cambridge: CABI Publishing; p. 331-355. https://doi.org/10.1079/9780851993188.0000

Gómez BJ, Serrano T, Angulo E. 1996. Morphology and fine structure of the glands of the dart-sac complex in Helicoidea (Gastropoda, Stylommatophora). Invertebrate Reproduction & Development 29(1): 47-55. https://doi.org/10.1080/07924259.1996.9672494

Haase M, Baur B. 1995. Variation in spermathecal morphology and storage of spermatozoa in the simultaneously hermaphroditic land snail Arianta arbustorum (Gastropoda: Pulmonata: Stylommatophora). Invertebrate Reproduction & Development 28(1): 33-41. http://dx.doi.org/10.1080/07924259.1995.9672461

Haszprunar G. 1996. The molluscan rhogocyte (pore cell, blasenzelle, cellule nucale) and its significance for ideas on nephridial evolution. Journal of Molluscan Studies 62(2): 185–211. https://doi.org/10.1093/mollus/62.2.185

Heller J. 2001. Life History Strategies. In: Barker GM, editor. The Biology of terrestrial molluscs. Ch. 1. Cambridge: CABI Publishing; p. 413-446. https://doi.org/10.1079/9780851993188.0000

Hylton-Scott ML. 1939. Estudio anatómico del Borus “Strophocheilus lorentzianus” (Doer) (Mol. Pulm.). Revista del Museo de la Plata 7(1): 217-278.

Jaramillo Roldán E, López Martínez J, Ramírez R, Velásquez Trujillo LE. 2014. Análisis morfológico del sistema reproductor e identificación molecular a través de los marcadores mitocondriales COI y 16S rRNA de Megalobulimus oblongus (Mollusca, Strophocheilidae) de Colombia. Revista peruana de biología 21(1): 079-088. http://doi.org/10.15381/rpb.v21i1.8250

Jong-Brink MD. 1969. Histochemical and electron microscope observations on the reproductive tract of Biomphalaria glabrata (Australorbis glabratus), intermediate host of Schistosoma mansoni. Zeitschrift fur Zellforschung und mikroskopische Anatomie 102(4): 507-542. http://doi.org/10.1007/BF00335491

Kokkinopoulou M, Spiecker L, Messerschmidt C, Barbeck M, Ghanaati S, Landfester K, Markl J. 2015. On the ultrastructure and function of rhogocytes from the pond snail Lymnaea stagnalis. PLoS One 10(10): e0141195. https://doi.org/10.1371/journal.pone.0141195

Kugler OE. 1965. A morphological and histochemical study of the reproductive system of the slug, Philomycus carolinianus (Bosc). Journal of Morphology 116(1): 117–131. https://doi.org/10.1002/jmor.1051160109

Leme JLM. 1973. Anatomy and systematics of the Neotropical Strophocheiloidea (Gastropoda, Pulmonata) with the description of a new family. Arquivos de Zooloologia, Sao Paulo 23(5): 295-337. https://doi.org/10.11606/issn.2176-7793.v23i5p295-337

Lind H. 1973. The functional significance of the spermatophore and the fate of spermatozoa in the genital tract of Helix pomatia (Gastropoda: Stylommatophora). Journal of Zoology 169(1): 39-64. https://doi.org/10.1111/j.1469-7998.1973.tb04652.x

Lynch TJ, Anderson PJ, Rotti PG, Tyler SR, Crooke AK, Choi SH, Montoro DT, Silverman CL, Shahin W, Zhao R, et al. 2018. Submucosal gland myoepithelial cells are reserve stem cells that can regenerate mouse tracheal epithelium. Cell Stem Cell 22(5): 653–667. https://doi.org/10.1016/j.stem.2018.03.017

Maltz TK, Jędrzejowska I, Sulikowska-Drozd A. 2017. On the histology, ultrastructure and function of the spermoviduct and free oviduct in egg-retaining door snails (Pulmonata: Clausiliidae). Journal of Molluscan Studies 83(2): 172–185. https://doi.org/10.1093/mollus/eyx002

Martoja R, Martoja-Pierson M. 1970. Técnicas de histología animal. Barcelona: Toray-Masson; 350 pp.

Moura KRS, Terra WR, Ribeiro AF. 2004. The functional organization of the salivary gland of Biomphalaria straminea (Gastropoda: Planorbidae): Secretory mechanisms and enzymatic determinations. Journal of Molluscan Studies 70(1): 21–29. https://doi.org/10.1093/mollus/70.1.21

Nicholas J. 1984. The biology of reproduction in two British pulmonate slugs. Doctor of Philosophy. Bangor University, Gwynedd, United Kingdom. Volume 1 and 2.

Ponder WF, Lindberg DR, Ponder JM. 2020. Biology and Evolution of the Mollusca. Volume 2. Boca Raton: CRC Press; 890 pp. https://doi.org/10.1201/9781351115254

Ramírez R, Borda V Romero P, Ramirez J, Congrains C, Chirinos J, Ramírez P, Velásquez LE, Mejía K. 2012. Biodiversidad y endemismo de los caracoles terrestres Megalobulimus y Systrophia en la Amazonia occidental. Revista Peruana de Biología 19 (1): 059-074. http://dx.doi.org/10.16925/sp.v10i20.909

Rigby JE. 1963. Alimentary and reproductive systems of Oxychilus cellarius (Müller) (Stylommatophora). Proceedings of the Zoological Society of London 141(2): 311-359. https://doi.org/10.1111/j.1469-7998.1963.tb01615.x

Schileyko LV, Schileyko AA. 1992. Additional findings on the morphology of the proximal part of the reproductive system of the Stylommatophora (Gastropoda, Pulmonata). Harvard University. Museum of Comparative Zoology. Special Occasional Publication (9): 1-13.

Shiga B. 2023. Estudio morfohistológico de la glándula pedal de caracoles (MOLLUSCA: GASTROPODA), productora de baba usada en cosmética. Tesis, Magíster en Zoología, mención en Morfología y Fisiología. Lima:Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos. https://hdl.handle.net/20.500.12672/21391

Silva FD, Simone LRL. 2022. Anatomy of two species of Megalobulimus (Strophocheilidae, Megalobuliminae) from South-Central Bahia, Brazil. Papéis Avulsos Zoologia 62: e202262066. http://doi.org/10.11606/1807-0205/2022.62.066

Simone LR-L, Leme JLM. 1998. Two new species of Megalobulimidae (Gastropoda, Strophocheiloidea) from north Sao Paulo, Brazil. Iheringia Serie Zoologia 85: 189-203.

Stanlen R. 1917. On the calcareous eggs of terrestrial Mollusca. Journal of Conchology 15: 154–164.

Tompa AS. 1976. A comparative study of the ultrastructure and mineralogy of calcified land snail eggs (Pulmonata: Stylommatophora). Journal of Morfology 150(4): 861-887. https://doi.org/10.1002/jmor.1051500406

van Mol J-J 1971. Notes anatomiques sur les Bulimulidae (Mollusques, Gasteropodes, Pulmones). Annales Société royale zoologique de Belgique 101: 183–225.

Wade CM, Mordan PB, Naggs F. 2006. Evolutionary relationships among the pulmonate land snails and slugs (Pulmonata, Stylommatophora). Biological Journal of the Linnean Socciety 87(4): 593–610. https://doi.org/10.1111/j.1095-8312.2006.00596.x

Zając KS, Kramarz PE. 2017. Terrestrial gastropods - how do they reproduce? Invertebrate Survival Journal 14(1): 199-209. https://doi.org/10.25431/1824-307X/isj.v14i1.199-209

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07/01/2024

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How to Cite

Temoche, Haydee, Betty Shiga, and Rina Ramírez. 2024. “Histological Study of the Talon and Glandular Sac Annex of Megalobulimus (Gastropoda, Strophocheilidae)”. Revista Peruana De Biología 31 (2): e27491. https://doi.org/10.15381/rpb.v17i3.27491.