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Comparative Anatomy and Phylogeny of the Cloacae of Salamanders (Amphibia: Caudata)

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Comparative Anatomy and Phylogeny of the Cloacae of Salamanders (Amphibia: Caudata) JOURNAL OF MORPHOLOGY 212~305-322 (1992) Comparative Anatomy and Phylogeny of the Cloacae of Salamanders (Amphibia: Caudata). Vi. Ambystomatidae and Dicamptodontidae DAVID M. SEVER Department of Biology, Saint Mary's College, Notre Dame, Indiana 46556 ABSTRACT Histology of the cloacae of Rhyacotriton olympicus and represen- tative species from the genera Ambystoma and Dicamptodon was examined by light microscopy. Females of Ambystoma possess sperm storage glands, the spermathecae, as well as ventral glands and dorsal glands, both of uncertain function. Females of Ambystoma examined from the subgenus Linguaelapsus differ from those in the subgenus Ambystoma by possessing more extensive ventral gland clusters and a shorter cloacal tube. Females of Dicamptodon possess spermathecae and ventral glands, but differ in cloacal conformation from females of Ambystoma and lack the dorsal glands. Females of R. olympi- cus possess more extensive epidermal lining in the cloaca than that found in females of Ambystoma and Dicarnptodon, and the only glands present are spermathecae, which cluster around a tube in the dorsal roof. Males of Ambystoma, Dicamptodon, and R. olympicus possess five types of cloacal glands (dorsal pelvic glands, lateral pelvic glands, anterior ventral glands, posterior ventral glands, and Kingsbury's glands) that function in spermato- phore formation, and vent glands that may produce a courtship pheromone. In Ambystoma and Dicamptodon, vent glands secrete along the medial borders of the cloacal orifice. Males of A. opacum and A. talpoideum differ from males of other species examined from the two genera by possessing more extensive vent glands. Males of R. olympicus possess unique vent glands in which tubules secrete onto the surface of vent lobes lateral to the posterior end of the cloacal orifice, and distal ends of the glands pass anteriorly, superficial to the fascia enclosing the other cloacal glands. The results from analysis of cloacal anatomy support other data indicating that Ambystoma and Dicamptodon are sister groups, and that Rhyacotriton olympicus is not closely related to either of the other two genera and merits placement in a separate family. o 1992 Wiley-Liss, Inc. This paper reviews existing literature and Trueb ('86) illustrate the external appear- presents additional descriptions of cloacal ance of the cloacal region of male and female anatomy for the North American salamander A.jeffersonianum in breeding condition, and families Ambystomatidae, containing the gen- the relationships of the cloacal cavities to era Ambystoma (27 species) and Rhyacosire- urogenital and digestive structures of sala- don (4 species), and Dicamptodontidae, con- manders are shown by Sever ('92b). In the sisting of Dicamptodon (4 species) and present paper, the female cloacal anatomy of monotypic Rhyacotriton (Frost, '85). Descrip- three species of Dicamptodon and seven spe- tions exist for the male cloacal anatomy of cies of Ambystoma is described for the first Dicamptodon tenebrosus and Rhyacotriton time. This paper is the sixth in a series on the olympicus (Sever, '88a) and for eight species comparative anatomy and evolution of the of Ambystoma (Sever, '81, '87, '88a; Sever et cloacal region of salamanders (Sever, '91a,b; al., '89; Licht and Sever, '91). Descriptions of '92a-c). female cloacal anatomy, however, are limited to brief reports on A, tremblayi and R. olym- MATERIALS AND METHODS picus (Sever, '87) and more detailed studies Snout-vent length (SVL) refers to the dis- on A. maculatum (Kingsbury, 1895) and A. tance from the tip of the snout to the poste- gracile (Licht and Sever, '91). Duellman and rior edge of the vent. Cloacal anatomy was o 1992 WILEY-LISS, INC. 306 D.M. SEVER examined following excision of the cloacal and/or presence of sperm in the spermathe- region and its histological preparation for cae. Stebbins ('54) reported that mature ova light microscopy. Specimens examined (Ap- of D. ensatus are 5-6 mm in diameter, and pendix I) were initially preserved in 10% neu- Nussbaum ('85, '87) reported mean (ovipos- tral-buffered formalin, and were stored in ited) ova sizes of 5.5 mm for D. copei and 6.6 60% isopropanol or 65% ethanol before re- mm €or D. ensatus. moval of cloacal tissue. In one Dicamptodon copei (UMMZ Cloacal tissue was rinsed in water, dehy- 134960.1, 101.5 mm SVL), ovarian follicles drated in ethanol, cleared in toluene or Histo- are only 0.75-1.25 mm in diameter, but ovi- sol (National Diagnostics, Inc., Manville, New ducts are convoluted, and some sperm are Jersey), and embedded in paraffin; 10-pm present in the spermathecae; thus this speci- sections were then cut with a rotary micro- men is mature. The other D. copei (UMMZ tome. Some sections from each species were 134961) had the ovaries removed and lacks stained with hematoxylin-eosin (for general sperm in the spermathecae, but it is consid- cytology), and others were stained or treated ered mature because the oviducts are convo- with Mallory's triple stain (connective tis- luted and the specimen is even larger (110.0 sue), ninhydrin Schiff/fast green (proteins), mm SVL) than other mature specimens. periodic acid-Schiff s (PAS) reagentlfast The only Dicamptodon aterrimus exam- green FCF (neutral carbohydrates), and/or ined (UMMZ 134671, 135 mm SVL) is meta- alcian blue/nuclear fast red at pH 2.5, or morphosed, has large ovarian follicles (4.5- toluidine blue (acid mucopolysaccharides). 5.25 mm in diameter), and is thus considered Staining procedures followed Humason ('79). mature; however, it has not recently mated Three-dimensional reconstructions were since the spermathecae lack sperm. Of the performed on transverse sections through three D. tenebrosus used in the present study, the cloacae of a male Ambystoma laterale, only one is metamorphosed and definitely and male and female A. opacum, Dicampto- mature. This individual (UMMZ 134955,279 don copei, and Rhyacotriton olympicus. These mm SVL)has ovarian follicles about 5 mm in reconstructions were done using PC3D soft- diameter and some sperm in the spermathe- ware (Jandel Scientific, Corte Madera, CAI cae. Neither branchiate D. tenebrosus exam- and a Jandel digitizing tablet with a Zenith ined possesses spermathecal sperm; both were ZF-248 microcomputer. Every 4th to 15th collected September 13, 1975. One (UMMZ section was digitized for image reconstruc- 137462.1, 130 mm SVL) has ovarian follicles tion following procedures outlined by Sever 1.5-1.75 mm in diameter and is probably ('91a). immature, while the other (UMMZ 137462.2, Sever ('91a) used a ratio of cloacal tube 141 mm SVL) has ovarian follicles 4.0-5.0 length divided by total cloacal length (CTL/ mm in diameter and may be mature. TCL) to express the relative size of the cloa- cal tube. The cloacal tube is cylindrical and RESULTS extends caudally to the cloacal chamber, a Female cloacal anatomy cavity dorsal to the vent. To determine Ambystomatidae lengths, the number of transverse sections of Reconstructions based on serial sections the cloacal tube and cloacal chamber was through the cloaca of a female Ambystoma counted. The section immediately posterior opacum are shown in Figure 1. Histological to the junction of the Wolffian ducts with the sections through cloacae are illustrated for A. hindgut was considered the most anterior opacum, A. gracile, A. maculatum, and A. section of the cloacal tube. tremblayi in Figure 2, and €or A. annulatum Dicamptodon copei normally is an obligate and A. barbouri in Figure 3. The three types paedomorph, and D. aterrimus and D. tene- of glands Kingsbury (1895) reported for A. brosus are facultative paedomorphs (Nuss- maculatum occur in all species. Interspecific baum, '70, '83; Good, '89). Dicamptodon ater- variation occurs in cloacal conformation and rimus and D. tenebrosus prior to 1989 were anatomy of the ventral gland. considered conspecific with D. ensatus, a spe- cies now restricted to parts of northern Cali- Cloacal conformation. The cloacal tube is fornia (Good, '89) and not examined for the present in all specimens examined except that present study. Maturity of branchiate fe- of Ambystoma annulatum, in which the males was determined by large size of ovar- Wolffian ducts do not join until the anterior ian follicles, convolution of the oviducts, end of the cloacal tube, so that a definite SALAMANDER CLOACAE 307 A C Fig. 1. Three-dimensional reconstructions of the clo- sections of the cloacal walls represents approximately aca of a female Ambystoma opacum (UMMZ 187373). 120 pm. Av, anterior ventral glands; Cc, cloacal chamber; Right lateral view with sections rotated 25“ clockwise. A: Cg, central groove; Ct, cloacal tube; Dg, dorsal glands; St, Walls of the cloacal cavities. B: Spermathecae. C: Ante- spermathecae. rior ventral gland. D: Dorsal gland. The distance between cloacal tube is not present (Fig. 3A). In the Posteriorly, the large dorsolateral foldsjoin other forms, the CTL/TCL quotient ranges medially, obliterating the central groove. In from 0.17 (A.texanum) to 0.38 (A.laterale). Ambystoma barbouri, A. jeffersonianum, A. In the species with a cloacal tube, the ante- laterale, A. opacum, A. platineum, and A. rior half is narrowed dorsally and widened tremblayi, obliteration of the central groove ventrally. The pseudostratified epithelium is occurs at the anterior end of the cloacal cham- formed into thick longitudinal folds or rugae ber (Figs. IA, 2B,C). In A. gracile, A. macula- (Fig. 2A) that are ciliated. At the midpoint of tum, A. talpoideum, and A. tigrinum, the the cloacal tube, the dorsal half widens. In central groove ends prior to the claacal cham- the posterior half of the cloacal tube, a pair of ber, and the posterior fourth of the cloacal large folds appears in the lateral walls, form- tube is a flattened slit (Fig. 2D). Since the ing a ‘‘central groove” between them (Figs. cloacal tube is absent in A. annulatum, the lA, 2A).
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