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

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JOURNAL OF MORPHOLOGY 211:63-72 (1992) Comparative Anatomy and Phylogeny of the Cloacae of Salamanders (Amphibia: Caudata). Ill. Amphiumidae DAVID M. SEVER Department of Biology, Saint Mary's College, Notre Dame, Indiana 46556 ABSTRACT Histological descriptions of female and male cloacae are pre- sented for the three species of Amphiuma. Little interspecific variation occurs in either females or males. Females possess numerous spermathecae around the walls of the posterior cloacal tube and anterior cloacal chamber as well as rudimentary vent glands, of uncertain homology, in the caudal end of the cloacal chamber. Ventral glands such as those known from female salamanders in other families are absent, likely a secondary loss in the amphiumid clade. In a female A. tridactylum with large ovarian follicles (5- to 8-mm diameter), the lips of the cloacal orifice are highly cornified, and stored sperm in the spermath- ecae appear in organized bundles, either free in the lumen or with the sperm heads seemingly buried in the spermathecal epithelium. Males possess some gland clusters present in other members of the suborder Salamandroidea (dorsal pelvic glands, vent glands, Kingsbury's glands, anterior ventral glands) but lack others (lateral pelvic glands, posterior ventral glands), resulting in the most plesiomorphic cloacal anatomy in the suborder. However, males possess an autapomorphic gland cluster, called the pit glands, in the posterior wall of the cloacal chamber. The pit glands consist of shallow infoldings of the cloacal epithelium unlike other cloacal glands, which are relatively tubular and elon- gate. The "pits" contain columnar eosinophilic cells that give positive staining reactions for acid mucopolysaccharides and proteins. The salamander family Amphiumidae con- found that amphiumids possess the most ple- sists of three species of Amphiuma found in siomorphic cloacal anatomy in the suborder the southeastern United States. Amphiumas Salamandroidea. This paper presents histo- are elongate salamanders with reduced limbs, logical descriptions of amphiumid cloacae in and adults retain one external gill slit, a order to extend the observations of Wilson paedomorphic character (Duellman and ('41) and Kreeger ('42) and to provide the Trueb, '86). Individuals of two species, Amph- anatomical basis for the character states used iuma means and A. tridactylum, are large, by Sever ('91). often in excess of 70-cm snout-vent length MATERIALS METHODS (SVL), and are aquatic, while A. pholeter is a AND dwarf species, 20- to 25-cm SVL, that usually SVL refers to the distance from the tip of is found burrowing in mucky banks (Conant, the snout to the posterior end of the vent. '75). Specimens, as far as known, were initially Davison (1895) described the gross anat- preserved in 10% formalin, and some were omy of the cloacae of male and female Amph- stored in isopropanol or ethanol of varying iuma means and was the first to provide concentrations before cloacae were excised anatomical evidence for internal fertilization for histological preparation. Specimens used in the family. Kreeger ('42) provided a histo- are in the collections of the University of logical description of the cloaca of female A. Michigan Museum of Zoology (UMMZ), Flor- tridactylum, but the only such account for ida Museum of Natural History (FM), or in male amphiumids is an abstract by Wilson my possession (DMS). The following speci- ('41) on the same species. Sever ('91) listed mens were examined histologically: Amphi- presencelabsence data for 23 cloacal charac- ters in amphiumids and other salamanders, Address reprint requests to Dr. David M. Sever, Department of and his cladistic analysis of these characters Biology, Saint Mary's College, Notre Dame, IN 46556. G 1992 WILEY-LISS, INC. 64 D.M. SEVER uma means: female, DMS 3005, 232 mm, image reconstruction. Right lateral views June 22,1977, Alachua County, Florida, and were reconstructed by computer software, male, UMMZ 187365, 520 mm, April 14, with the sections rotated 25” clockwise. The 1987, Marion County, Florida; A. pholeter: cloacal displays were stretched appropriately female, UMMZ 186277, 238 mm, July 31, in the anteroposterior direction to help allevi- 1985, and male, FM 62441,160 mm, May 12, ate geometric distortions caused by skipping 1985, Levy County, Florida; and A. tridacty- sections between those digitized. Each digi- lum: females, DMS 16111, 526 mm, DMS tized section of cloacal glands was repeated 16110, 528 mm, and UMMZ 187364, 575 once so that gaps between displayed sections mm, collection dates unknown, Orleans Par- were more nearly closed. Finally, alternate ish, Louisiana, and males, UMMZ 187363, digitized sections of the cloacal walls were 421 mm, and UMMZ 187366, 481 mm, no displayed to improve clarity. other data, and DMS 4103,725 mm, May 29, Following Sever (’78),the cloaca is divided 1974 (preserved 17 November 1980), Or- into the cloacal tube and the cloacal chamber. leans Parish, Louisiana. The cloacal tube is cylindrical and extends Following dehydration in ethanol, the ex- caudally to the cavity dorsal to the vent, the cised cloacal region was cleared in toluene or cloacal chamber. Relative length of the cloa- Histosol (National Diagnostics, Inc., Man- cal tube (cloacal tube length/total cloacal ville, NJ), embedded in paraffin, and 10-pm length = CTLITCL elsewhere) may have sagittal (male Amphiuma means) or trans- phyletic significance (Sever, ’91). To deter- verse (remaining specimens) sections cut with mine lengths, the number of transverse sec- a rotary microtome. Sections from each spe- tions of the cloacal tube and cloacal chamber cies were stained with hematoxylin-eosin were counted. The most anterior section of (H&E) (for general cytology), and additional the cloacal tube was considered the one imme- sections from some specimens were treated diately posterior to the junction of the Wolf- with diagnostic stains using procedures de- fian ducts with the hindgut. scribed by Humason (’79). Slides from fe- male A. pholeter and one female A. tridacty- RESULTS lum (UMMZ 187364) were stained with the Female cloacal anatomy ninhydrin-Schiff reactiodfast green (pro- One female Amphiuma tridactylum teins), periodic acid-Schiff reagent/ fast green (UMMZ 187364) has sperm in the spermath- FCF (PAS, neutral carbohydrates), and al- ecae and enlarged ovarian follicles (5-8 mm cian blue/nuclear fast red at pH 2.5 (acid in diameter). The other A. tridactylum and mucopolysaccharides). The cloacal sections the A. means lack sperm in their spermathe- of male A. pholeter were not subjected to cae and possess small ovarian follicles (<1 diagnostic staining, but some from male A. mm in diameter). Spermathecae are well de- means were stained with alcian blue. Sec- veloped but devoid of sperm in the A. pholeter tions from one male A. tridactylum (UMMZ examined. Three-dimensional reconstruc- 187363) were treated with PAS and alcian tions through the cloaca of A. pholeter are blue, and sections from another (DMS 4103) shown in Figure 1, and transverse sections were treated with PAS, alcian blue, and nin- through cloacae of A. pholeter and A. tridac- hydrin Schiff. No tests for lipids were done tylum are illustrated in Figure 2. since some reagents used for paraffin embed- ding remove lipids. Secretory products with a Cloaca1 conformation and anatomy of the stringy appearance were considered “fibrous” linings while spheroidal secretory droplets were The CTL/TCL quotient is 0.41 in A. means called “granular,” if uniformly small, or and 0.49 in A. pholeter. Some anterior and/or “globular,” if composed of coalesced gran- posterior sections are lacking in the Amphi- ules. uma tridactylum examined; thus the CTL/ Three-dimensional reconstructions of cloa- TCL could not be determined for that spe- cae of female and male Amphiuma pholeter cies. were done using PC3D software (Jandel Sci- Posterior to the junction of the urogenital entific, Corte Madera, California) and a Jan- ducts, the cloacal tube has rugose walls lined del digitizing tablet with a Zenith ZF-248 with glandular, alcian blue+, pseudostrati- microcomputer. Every sixth (female) or tenth fied epithelium. Some epithelial cells in the (male) transverse section was digitized for cloacal tube possess cilia. Cilia do not occur AMPHIUMA CLOACAE 65 Ct with enlarged ovarian follicles and spermato- zoa in the spermathecae is especially thick and cornified (Fig. 2G). Cloacal glands Spermathecae and vent glands occur in all specimens examined. In the Amphiuma tri- dactylum with large ovarian follicles, sperma- A tozoa occur in short, tubular glands in the A posterior half of the cloacal tube and the anterior two-fifths of the cloacal chamber, defining these glands as spermathecae. Glands similar in appearance and location, but devoid of sperm, occur in these regions in the other female amphiumids examined. An- teriorly, the first spermathecae appear dorso- medially, and more posteriorly they spread around the dorsal and lateral walls of the cloaca (Figs. lB, 2A-D). In one A. tridacty- 8 lum (DMS 16111) and in the A. means exam- ined, some glands appear around the inferior border of the cloacal tube as well (the “ven- B tral group” of spermathecae described by Kreeger, ’42).The most posterior spermathe- Fig. 1. Three-dimensiond reconstructions of the clo- cae are dorsomedial and, in A. pholeter, pass acal cavities and cloacal glands of female Amphiuma pholeter. Lateral view, with the anterior end (toward the into portions of the cloacal chamber where right) rotated clockwise 25”. A. Cloacal tube and cloacal the lining has become epidermal (Fig. 2D). chamber. B. Relationships of spermathecae and vent Spermathecal cytoplasm is scant and the glands to the cloacal cavities. The distance between sec- tions of the cloacal walls represents 120 pm. Cc, cloacal cells squamous in Amphiuma means and in chamber; Ct, cloacal tube; St, spermathecae; Vg, vent the A. tridactylum lacking stored sperm. The glands. spermathecal epithelium is eosinophilic and cuboidal in A. pholeter and in the A.
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