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THE HYPOBRANCHIAL GLAND from the PURPLE SNAIL PLICOPURPURA PANSA (GOULD, 1853) (PROSOBRANCHIA: MURICIDAE) Author(S): LUDWIG C

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THE HYPOBRANCHIAL GLAND from the PURPLE SNAIL PLICOPURPURA PANSA (GOULD, 1853) (PROSOBRANCHIA: MURICIDAE) Author(S): LUDWIG C THE HYPOBRANCHIAL GLAND FROM THE PURPLE SNAIL PLICOPURPURA PANSA (GOULD, 1853) (PROSOBRANCHIA: MURICIDAE) Author(s): LUDWIG C. A. NAEGEL and CARLOS AUGUSTO AGUILAR-CRUZ Source: Journal of Shellfish Research, 25(2):391-394. Published By: National Shellfisheries Association DOI: http://dx.doi.org/10.2983/0730-8000(2006)25[391:THGFTP]2.0.CO;2 URL: http://www.bioone.org/doi/full/10.2983/0730-8000%282006%2925%5B391%3ATHGFTP %5D2.0.CO%3B2 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Shellfish Research, Vol. 25, No. 2, 391–394, 2006. THE HYPOBRANCHIAL GLAND FROM THE PURPLE SNAIL PLICOPURPURA PANSA (GOULD, 1853) (PROSOBRANCHIA: MURICIDAE) LUDWIG C. A. NAEGEL* AND CARLOS AUGUSTO AGUILAR-CRUZ Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional (CICIMAR/IPN) Apdo. Postal 592 LA PAZ, B.C.S. 23000 Mexico ABSTRACT Results are presented on the histology of the hypobranchial gland of the marine muricid Plicopurpura pansa (Gould 1853). The general structure and secretory features were investigated using light microscopy and histochemical methods for the determination of tryptophan/indol. The hypobranchial gland of P. pansa is an antero-posteriorly elongated organ located on the internal surface area of the mantle, that folds on its posterior side near the rectum, right of the ctenidia and anterior to the kidney. In dead animals it is easily distinguishable by the purple color that develops after removing the shell. Parallel to the hypobranchial gland, in the same position, can be found a black-pigmented structure, presumably the anal gland. The secretory epithelium, which forms the hypobranchial gland consists of at least six different and very long (156.7 ␮m) cell types. It was impossible to distinguish clearly the different histological regions of the hypobranchial gland, because the different cell types were uniformly distributed throughout the gland, with the exception of the rectal area. The number of acidophilic granular cells differed markedly between animals, probably because of different levels of secretion. In the mantle cavity was always found a large quantity of mucus and only occasionally acidophilic granulated secretory products. Only the two cell types with acidophilic granules in the hypobranchial gland showed histochemically strong positive reactions for tryptophan, indicating in these cells high concentrations of the precursors for “Tyrian Purple.” KEY WORDS: hypobranchial gland, purple snail, Plicopurpura pansa, Muricidae INTRODUCTION spite these exceptional properties of P. pansa, first as a source for “Tyrian Purple” and secondly about the state of the endangered Most marine snails in the families Muricidae and Thaididae, snail populations, little is known about the principal life-history which make up the genera Murex, Thais and Plicopurpura, pro- features, and many basic biological questions remain. Until now duce in the hypobranchial gland (mucus gland) a viscous liquid studies are lacking on the histology of the hypobranchial gland of secretion containing, besides mucus and biologically active com- P. pansa. The objectives of this study are to gain a better under- pounds, minute amounts of chromogens. These develop enzymati- standing of the biological function of this gland (1) by examining cally in light and oxygen into a purple pigment known as “Tyrian the general morphological features of the P. pansa hypobranchial Purple,” Royal Purple” or “Shellfish Purple.” Fretter and Graham gland using compound light microscopy; (2) determining by his- (1994) considered the main function of the hypobranchial gland to tochemical means the inner-cellular sites of tryptophan and (3) be a secretor of mucus for trapping and cementing particulate comparing the results with previously published reports about the matter sucked into the mantle cavity with the respiratory water histology of the hypobranchial gland from other Muricidae and current prior to its expulsion. Thaidae. The carnivorous, gonochoristic, marine, muricid purple snail Plicopurpura pansa (Gould, 1853) inhabits intertidal rocky shores MATERIALS AND METHODS exposed to high impact waves of the open sea. The range of P. More than 100 specimens of an unexploited population of P. pansa extends from the northwest coast of Mexico (Baja Califor- pansa were collected in 2001 from intertidal rocks on days during nia Sur) (Clench 1947, Keen 1971) to northern Peru (Peña 1970, extreme low-water spring tides at Playa Cerrito on the Pacific Paredes et al. 1999). The snail is not too small (shell length aver- coast (23°19Ј54ЉN and 110°10Ј38ЉW), about 80 km south-west of ages 30 mm but can be as large as 90 mm), and at low tides it is La Paz. The average size of the males was 25.87 mm (range relatively easily gathered. An exceptional property of P. pansa, in 14.86–43.5 mm), of the females 30.14 mm (range 13–73.9 mm). comparison with that of other muricids, is that it ejects its dye- Injecting a 10% neutral, buffered, formalin solution into the producing liquid in such large quantity, that there is no need to kill snails preserved the tissue of the animals. About 24 h later in the the animal to obtain the “Tyrian Purple.” Furthermore, the hypo- laboratory eight animals were selected and removed from the shell, branchial gland is so active that the snails can be “milked” peri- subsequently dehydrated in an alcohol series, cleared with butyl- odically without harming the animals (Rios-Jara et al. 1994, Nae- ated hydroxanisole, and embedded in paraffin. Longitudinal and gel 2005). For these reasons it is not unexpected that P. pansa is transversal sections (5 ␮m) were prepared of the hypobranchial exploited for “Tyrian Purple” production, probably since pre- gland, and according to the methodology by Humason (1979), Colombian times. In recent years however, with increasing public stained with Ferric Hematoxylin-Eosin or Mallory Trichromic awareness of natural colors, the commercial exploitation of P. stain. To prove the presence of tryptophan, as the origin of the pansa for dyeing kimonos with “Tyrian Purple” had reached in precursors for “Tyrian Purple” (Verhecken 1989), the histochem- Mexico such levels as to threaten the survival of the species. In ical method for the demonstration of tryptophan (Davenport 1960) 1988 P. pansa had to be declared by the Mexican government a was applied. species under special protection (Anonymous, 1988; 1994). De- RESULTS The hypobranchial gland of P. pansa is an antero-posteriorly *Corresponding author. E-mail: [email protected] elongated organ located at the internal surface area of the mantle, 391 392 NAEGEL AND AGUILAR-CRUZ that folds on its posterior side near the rectum, right of the ctenidia and anterior to the kidney (Fig. 1). On dead animals it is easily distinguishable by the purple color that develops after the removal of the shell. Parallel to the hypobranchial gland in the same posi- tion can be found a black pigmented structure, presumably the anal gland. The secretory epithelium, which forms the hypobranchial gland consists of at least six different and very long (156.7 ␮m) noncili- ated cell types: (a) eosinophilic cells with an irregular cytoplasmic texture, (b) very abundant goblet mucus cells, (c) cells with strong acidophilic granules, (d) cells with light acidophilic granules, (e) a few cells at the rectal area with very fine basophilic granules and (f) empty cells. Figure 2 shows a section of the hypobranchial gland: the basal membrane with the longitudinal muscle cells, eosinophilic and goblet mucus cells and cells with acidophilic granules. At the right side of the photograph is shown the mantle cavity with secreted mucus and acidophilic granules. At the left side is shown the external cubical epithelium, which is in contact with the shell. Figure 2. Microphotograph of the hypobranchial gland. bm, basal It was impossible to distinguish clearly the different histologi- membrane; ec, empty cell; eoc, eosinophilic granulated cell; apc, aci- cal regions of the hypobranchial gland because the different cell dophilic granules; lm, longitudinal muscle; mc, mucus cell. Bar = 20 µm. types were uniformly distributed in the gland. The exception was the rectal area —the only region where a cell type was found with branchial gland showed a histochemically strong positive reaction very fine basophilic granules and where the number of mucus cells for tryptophan, indicating that in these cells there are high con- and cells with acidophilic granules was reduced. Along the glan- centrations of the precursors or chromogens for “Tyrian Purple.” dular epithelium in the basal tissue were found a few blood vessels and a thin
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