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Ultrastructure of the Spermathecae of Necturus Beyeri (Amphibia: Proteidae) in Relation to Its Breeding Season Author(S): David M

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Ultrastructure of the Spermathecae of Necturus Beyeri (Amphibia: Proteidae) in Relation to Its Breeding Season Author(S): David M Ultrastructure of the Spermathecae of Necturus beyeri (Amphibia: Proteidae) in Relation to Its Breeding Season Author(s): David M. Sever and Henry L. Bart, Jr. Source: Copeia, Vol. 1996, No. 4 (Dec. 27, 1996), pp. 927-937 Published by: American Society of Ichthyologists and Herpetologists Stable URL: http://www.jstor.org/stable/1447655 . Accessed: 27/12/2010 15:11 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at . http://www.jstor.org/action/showPublisher?publisherCode=asih. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. American Society of Ichthyologists and Herpetologists is collaborating with JSTOR to digitize, preserve and extend access to Copeia. http://www.jstor.org Copeia, 1996(4), pp. 927-937 Ultrastructure of the Spermathecae of Necturusbeyeri (Amphibia:Proteidae) in Relation to Its Breeding Season DAVID M. SEVER AND HENRY L. BART JR. Sperm occurred in the spermathecae of all female Necturus beyeri collected in a Louisiana stream from Dec. through May, including those taken from nests after oviposition in May. The spermathecae possessed two types of epithelial cells: dark cells, with secretory vacuoles 1-2 jm dia; and light cells, with secretory vacuoles 0.5-1.0 im dia. The vacuoles of both types of cells contained glyco- proteins that were secreted into the lumen and bathed sperm during storage. The vacuoles were most abundant early in the breeding season, and light cells in individuals examined after oviposition were completely depleted whereas dark cells retained vacuoles only along the luminal border. If the secretions help maintain sperm viability, the depletion of secretory product could limit the storage of remnant sperm during the summer and fall months. However, no evidence of sperm degradation was found, and the fate of sperm remaining in the spermathecae following fertilization is unknown. Necturus beyeri can store sperm for at least six months prior to oviposition. THE Proteidae consists of five species of from Talisheek Creek between the Gulf, Mo- branchiated, aquatic salamanders in the bile, and Ohio Railroad crossing at Talisheek genus Necturus from eastern North America and and the LA Hwy 41 crossing, Saint Tammany Proteus anguinus from the Adriatic coast of Parish, Louisiana (Table 1). Specimens collect- northeastern Italy and Croatia (Frost, 1985). ed in May were postoviposition females re- Like other salamanders in the suborder Sala- moved from nests. Numbers of embryos in each mandroidea, cloacal glands in males produce nest at the time of guardian removal are given spermatophores and cloacal glands, called sper- in Table 1. We collected other specimens with mathecae, in females store sperm (Sever, 1991 a, modified Thiel-Turkay traps baited with earth- 1992b). The actual transfer of a spermatophore worms (Manning, 1986). We sacrificed these and fertilization has never been observed in the specimens before oviposition. Proteidae. Salthe (1967) suggested that sper- We sacrificed specimens 0-2 days after col- matophore transfer in proteids is via cloacal ap- lection by immersion in 10% MS-222. We ex- position. Eggs apparently are fertilized by re- cised cloacal regions and preserved them in a lease of sperm from the spermathecae as the 1:1 solution of 2.5% glutaraldehyde in Millon- eggs pass through the cloaca (Jordan, 1893; ig's phosphate buffer at pH 7.4 and 3.7% form- Boisseau and Joly, 1975). aldehyde buffered to pH 7.2 with monobasic Ultrastructure of sperm storage in the the and dibasic phosphate (NBF). We preserved car- spermathecae of female salamanders has been casses in NBF and cataloged them into the Tu- described in the Ambystomatidae (Sever and lane Museum of Natural History (TU) herpe- Kloepfer, 1993; Sever, 1995; Sever et al., 1995), tology collection (Table 1). Plethodontidae (Pool and Hoage, 1973; Davitt After fixing cloacal tissue in glutaraldehyde: and Larsen, 1988a; Sever and Brunette, 1993), formalin, we subsequently prepared it by par- and Salamandridae (Dent, 1970; Brizzi et al., affin infiltration for light microscopy (LM), or 1995; Sever et al., 1996), but no reports exist for embedding in epoxy resin for semithin (LM) for the Proteidae. In this paper, we report on or ultrathin sections for transmission electron aspects of female sperm storage during the microscopy (TEM). For the paraffin method, we breeding season of Necturus beyeri in a popula- rinsed the tissue in water after fixation, dehy- tion in which certain other aspects of the re- drated it in ethanol, and cleared it in Histosol production were studied by Shoop (1965), and (National Diagnostics, Inc., Manville, NJ) prior we describe the cytology of the spermathecae to embedment in paraffin. We cut sagittal sec- of N. beyeriduring the breeding season. tions (10 ,Lm)with a rotary microtome, affixed them to albuminized slides, and stained alter- MATERIALSAND METHODS nate slides with hematoxylin-eosin (HE) for gen- eral cytology or alcian blue at pH 2.5 (AB) for This study was based on 17 specimens of N. glycosaminoglycans with a counterstain of pe- beyeri collected 13 Dec. 1993 to 8 Jan. 1995 riodic acid and Schiffs reagent (PAS) for "neu- ? 1996 by the American Society of Ichthyologists and Herpetologists 928 COPEIA, 1996, NO. 4 TABLE 1. VOUCHER,SIZE, AND OVARIANDATA FORFEMALE Necturus beyeriUSED IN THIS STUDY. Meanova CollectionDate TU no. SVL (mm) GSI' Ova Nb size (mm) 13 Dec. 1993 23401 112 0.025 50 2.33 23402 110 0.029 60 2.37 23403 106 0.039 57 2.51 23404 112 0.042 54 2.50 2 Jan. 1994 23405 129 0.044 76 2.91 23406 108 0.045 41 2.99 23407 145 0.025 59 2.42 13 March 1994 23408 116 0.064 28 4.62 23409 129 0.034 36 3.39 23411 104 0.086 38 3.98 23412 127 0.048 37 3.66 22 May 1994 23414 119 nesting 37 23415 116 nesting 26 23416 138 nesting 33 23417 117 nesting 32 4 Dec. 1994 23528 114 0.022 47 2.22 8 Jan. 1995 23538 103 0.041 35 2.90 * Gonadosomaticindex (ovaryweight as proportionof body weight withoutviscera). bTotal numberof ova in left and ovaries or in nest. c enlargedyellow right (= clutch), embryos Meansize (mm)of 10 randomly-selectedova. tral" carbohydrates such as glucose, galactose, position, but the glands appeared relatively re- mannose, and sialic acids. These staining pro- duced in diameter, especially those glands that cedures followed Kiernan (1990). lacked sperm (Fig. 1D). In the latter glands, After initial fixation for TEM, we rinsed tis- "light cells," whose ultrastructure is described sues in Millonig's buffer, postfixed in 2% os- below, were particularly conspicuous (Fig. 1D). mium tetroxide, dehydrated in ethanol, cleared In paraffin sections, apical portions of the sper- in propylene oxide, and embedded in an epoxy mathecal epithelium were mainly PAS+, al- resin (EMBED-812; Electron Microscopy Sci- though some AB+ areas occurred as well (see ences, Fort Washington, PA). We cut semithin also Sever, 1994). PAS+ substances also oc- sections (0.5-1.0 ium)for light microscopy with curred around clusters of sperm in the lumen. glass knives, placed on them microscope slides, In plastic sections, the secretory material stained and stained them with toluidine blue. We col- darkly with toluidine blue but was not meta- lected ultrathin (70 nm) sections for TEM on chromatic. The staining reactions were most uncoated copper grids and stained them with intense in those specimens sacrificed prior to uranyl acetate and lead citrate. We cut sections oviposition. on RMC XL1000 or RMC MT7 ultramicro- Transmission electron microscopy revealed tomes and viewed ultrathin sections with a Hi- two types of epithelial cells that were distin- tachi H-300 transmission electron microscope. guished based upon the size of their secretory vacuoles and the electron density of their cy- RESULTS toplasm (Figs. 2-3). In "dark cells," the secre- tory vacuoles were generally 1-2 ,m dia and As reported by Sever (1992b), the sperma- consisted of a central dense area (0.5-0.7 ,um thecae of female N. beyeriwere simple tubular dia) surounded by an outer, more lucent, floc- exocrine glands that opened onto the roof of culent material (Fig. 2B-C). Secretory vacuoles the cloaca. Sperm occurred in the spermathecae also were present in light cells, at least prior to of all specimens examined (Fig. 1). Sperm were oviposition, but these vacuoles were 0.5-1.0 ,m not evenly distributed among the glands, how- dia, with a central dense material that usually ever, and some glands or at least portions of was 0.3-0.5 ,m dia (Fig. 3A-D). Light cells were some glands were devoid of sperm in each spec- interspersed among dark cells, and apical ends imen. When present in a gland, sperm were of both cell types were on the luminal border randomly oriented and clustered in the center (Fig.
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