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Herpetologists' League Male Rhyacotriton olympicus (Dicamptodontidae: Urodela) Has a Unique Cloacal Vent Gland Author(s): David M. Sever Source: Herpetologica, Vol. 44, No. 3 (Sep., 1988), pp. 274-280 Published by: Herpetologists' League Stable URL: http://www.jstor.org/stable/3892341 Accessed: 30-06-2015 16:02 UTC REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/3892341?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references.

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Herpetologica,44(3), 1988, 274-280 ? 1988 by The Herpetologists' League, Inc.

MALE RHYACOTRITON OLYMPICUS (DICAMPTODONTIDAE: URODELA) HAS A UNIQUE CLOACAL VENT GLAND DAVID M. SEVER

Department of Biology, Saint Mary's College, Notre Dame, IN 46556, USA ABSTRACT: The square vent lobes of Rhyacotritonolympicus are the external manifestationof subdermalvent glands, which, insteadof secretinginto the cloacal orificeas in other species, secrete at the posterior tips of the vent lobes. Aside from the vent gland autapomorphy, male cloacal anatomy of R. olympicus is similar to that of Dicamptodon, Ambystoma, and members of the Plethodontidae.Rhyacotritonolympicus, however,shareswith Dicamptodon and Ambystomasome cloacal charactersthat are different in the Plethodontidae.Pheromonesmay be released from the vent gland during "tail curling".

Key words: Cloaca; Anatomy;Caudata;Dicamptodontidae;Rhyacotriton THE observation that male Rhyacotriton olympicus possesssuperficialvent lobes that are square in outline has been made by many authors (e.g., Anderson, 1968; Behler and King, 1979; Bishop, 1947; Cochran and Goin, 1970; Conant, 1975; Stebbins, 1954, 1966). Bishop (1947) stated that the posterior angles of the vent lobes are light-tipped and visible dorsally.In this paper, I report that the vent lobes are the external manifestation of an internal cloacal anatomy that is autapomorphic for the species. Rhyacotriton is a monotypic genus generally placed with the two extant species of Dicamptodon in the family Dicamptodontidae although, prior to Hecht and Edwards (1977), the dicamptodontids were usually given subfamilial statusin the Ambystomatidae (Tihen, 1958). No descriptionexistsof cloacalanatomy for males of any dicamptodontid, and the only descriptions for male ambystomatids are for Ambystoma maculatum (Kingsbury, 1895), A. opacum (Noble and Brady, 1933), and A. tigrinum (Sever, 1981). In this paper, I also provide the first descriptions of cloacal anatomy for D. copei and D. ensatus as well as for various additional species of Ambystoma. MATERIALS AND METHODS

All specimens used in this study were deposited in the herpetological collections of the Museum of Zoology, The University of Michigan. Snout-vent length (SVL) was

measured from snout to posterior end of the vent in animals stored in 65% ethanol or 60% isopropanol after fixation in 10% neutral buffered formalin. I examined 19 males of Rhyacotriton olympicus; one (50.9 mm SVL) was collected on 19 June 1981 in Clallam County, Washington, and the rest (46.5-52.5 mm SVL) were collected on 13 April 1968 (12) and 29 May 1973 (4) in MultnomahCounty, Oregon. I examined two Dicamptodon copei (106.0 mm and 107.9 mm SVL),both collected 24 August 1969 in Skamania County, Washington. Metamorphosed D. ensatus that I examined were collected in Benton County, Oregon on 17 May 1969 (128 mm SVL) and 8 October 1967 (147 mm SVL). Branchiated individuals of D. ensatus in which histological examination of the testes showed active spermatogenesis were considered paedomorphs, and I examined two such individuals; one (133 mm SVL) was collected on 18 August 1950 in Lane County, Oregon, and the other (122 m SVL) was collected on 13 September 1975 in Linn County, Oregon. I reexamined slides prepared and described by Sever (1981) from five male specimens of Ambystoma tigrinum. In addition, I examined male specimens of the following species:A. jeffersonianum (77.2 mm SVL and 81.6 mm SVL, collected 8 March 1983 in Frederick County, Virginia); A. laterale (43.5 mm SVL, collected 13 September 1975 in Manitowoc County,

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Wisconsin);A. maculatum (86.5 mm SVL, collected 18 March 1971 in Hocking County, Ohio); A. opacum (50.8 mm SVL, collected in fall 1983 in Florida, exact locality unknown);A. talpoideum (55.2 mm SVL, collected 22 February 1982 in Henderson County, North Carolina);and A. texanum (56.9 mm SVL, collected 16 February 1973 in Beauregard Parish, Louisiana). The cloaca of one R. olympicus (51.3 mm SVL) was examined by gross dissection, and cloacae from the remaining R. olympicus and all other species were examined by light microscopy following histological preparationusing proceduresdescribed by Humason (1979) and the following. Cloacae were excised, dehydrated in ethanol, cleared in Histosol (National Diagnostics, New Jersey), and embedded in paraffin.Transversesections and, in cases where multiple specimens were examined, sagittal and/or frontal serial sections were cut by rotary microtome at 10,m. Slides were stained or treated with hematoxylin/eosin (general cytology), periodic acid/Schiff's reagent (PASgeneralcarbohydrates)counterstainedwith fast green, alcian blue at pH 2.8 (acid mucopolysaccharides) counterstained with nuclear fast red, and the ninhydrin Schiff reaction (proteins)counterstainedwith fast green. RESULTS

Rhyacotriton olympicus Kingsbury'sglands are short basophilic glands with cuboidal cells. These glands secrete into a narrowed, dorsal portion of the anterior one-half of the cloacal tube (Fig. 1A). The secretion of Kingsbury's glandsis granularand reactspositivelywith PAS and alcian blue but not with ninhydrin Schiff. Pelvic glands are elongate eosinophilic glands with cuboidal cells. Pelvic glands secrete into a depression of the posterior one-half of the cloacal tube and caudad to this depressionalong the dorsolateralwalls of the cloacal tube and anterior cloacal chamber (Fig. 1B,C). Distal ends pass anteriorly. The secretion of pelvic glands is globular and reacts positively with nin-

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hydrin Schiff. Also, the globular material in dorsalportionsof the pelvic gland reacts strongly with PAS and alcian blue while that in lateral portions reacts weakly. Anteriorventral glands are elongate basophilic glands with distal ends that pass cephalad. Anterior ventral glands secrete onto the medial edges of obliquely oriented folds, the cloacal rugae (Fig. 1B,C). These rugae originate in the floor of the anterior cloacal tube and slant inferiorly to terminate on the lips of the anterioronehalf of the cloacal orifice and are the major conformational feature of the walls of the inferior one-half of the anterior cloacal chamber. Posterior to the folds, the walls of the cloacal chamber possess short papillae which in turn are replaced by stratified epithelium in the caudal angle of the vent. A small group of posteriorly passing ventral glands appears in the anterior cloacal chamber between pelvic and anterior ventral glands (Fig. IC). Posteriorventral glands stain more lightly with hematoxylin and are wider in relative diameter and shorter in length than anterior ventral glands. In the posteriorone-half of the cloacal chamber, posterior ventral glands replace pelvic and anterior ventral glands and are the only cloacal glands secreting into the cloaca, although no glands secrete into the caudal angle of the vent. The granular secretion of the ventral glands reacts similarly to that of Kingsbury's glands. The cells are squamous in ventral glands with abundant luminal substance. The vent glands of R. olympicus pass from secretory pores on the posterior, lateral tips of the swollen vent lobes anteriorly to the caudal border of the ischium (Figs. 1C-F, 2). The glands are simple but convoluted.The number of separateglands is difficult to ascertain, but I counted 1721 glands passing from the gland orifices on each side. The gland mass is pressed close to the skin, which lacks mucous and granularglands in the vent gland area, and to the skeletal muscle bundles surrounding the other cloacal glands. The most medial vent glands lie adjacent to ventral glands along the cloacal orifice (Figs. 1C,D, 2B).


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FIG. 1. Transverse sections through the cloaca from (A) anterior to (E) posterior of a male Rhyacotriton olympicus, 50.9 mm SVL. Scale in lower right corner = 250,um for A-E and 50,utm for F. Sections stained in hematoxylin/eosin. (A) Anterior end of the cloacal tube. (B) Depression of the cloacal tube roof. (C) Anterior end of the cloacal chamber. (D) Anterior one-third of the cloacal chamber. (E) Posterior end of the cloacal chamber. (F) Same as E, higher magnification of area with vent gland orifices. AV = anterior ventral gland; CC = cloacal chamber; CT = cloacal tube; DP = dorsal pelvic gland; K = Kingsbury's gland; LP = lateral pelvic gland; 0 = vent gland orifices; PV = posterior ventral gland; V = vent gland.


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The cells of active vent glands have basal nuclei and generally are columnar. Interspersed irregularly among the columnar cells are ones in which the apical portionappearsabsent, perhapsindicating an apocrinesecretion mode. The variation in cell height results in a festooned appearance.The eosinophilic secretion of the vent glands consists of small globules in the cytoplasmand a colloidal luminal substance which may have some granular secretion around the edges. The secretion reacts strongly with ninhydrin Schiff and moderately with PAS. The secretion does not stain with alcian blue. Other Species Transversesections through the cloaca of a male Dicamptodon copei are shown in Fig. 3. The cloacal conformation and the anatomy of Kingsbury's, pelvic, and ventral glands in the other species examined generally resemble those of R. olympicus. The posteriorventral gland, however, is better developed in the other species and is especially large in Ambystoma opacum and A. talpoideum. In a paedomorphic Dicamptodon ensatus (122 mm SVL) and a D. copei (106.0 mm SVL), the posterior ventral gland cluster was the only group of cloacal glands hypertrophied. As in R. olympicus, posteriorventral glands of the other species are the most caudad group of cloacal glands to secrete into the cloacal orifice, and their area of secretion ceases just prior to the caudal angle of the vent, except in D. copei, in which no cloacal glandssecrete into the entire posterioronehalf of the cloacal orifice. The "lateral pelvic gland" and "primary and secondaryfolds" (Fig. 3B,C) are readily recognized in the other species and are as described for A. tigrinum by Sever (1981). In R. olympicus, the portion of the pelvic gland similar in cytology and staining to the "lateral" portion of the other species is limited (Fig. IB), and the primary and secondary folds are not welldeveloped. The major difference in cloacal anatomy between R. olympicus and the other

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A

B FIG. 2.-Diagrams of the relation of vent glands to the external cloacal region in male Rhyacotriton olympicus: (A) lateral view; (B) ventral view. Labels same as for Fig. 1 plus CO = cloacal orifice, VG ventral glands.

species examined is anatomy of the vent gland. In all other species, the vent gland secretes onto the epidermis surrounding the cloacal orifice and onto papillae just inside the cloacal orifice (Fig. 3C-E). The extent of the vent gland varies interspecifically with the largest mass of glands found in A. talpoideum and A. opacum. In those two species, and in A. texanum, D. copei, and D. ensatus, the vent gland secretes into the cloacal orifice from its anteriorend until just cephalad to the area where posterior ventral glands cease secreting into the cloacal orifice. The vent glands in these species generally pass laterally, although their distal ends often curve anteriorlyor posteriorly,resulting in transversesections of vent glands appearing in some of the most cephalad as well as caudad sectionsof the cloaca (Fig. 3A,F). In A. talpoideum, some of the anteriorly


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sections through the cloaca from (A) anterior to (F) posterior of a male Dicamptodon Sections stained in hematoxylin/eosin. (A) Anterior end of the cloacal tube. (B) Depression of the cloacal tube roof. (C) Anterior end of the cloacal chamber. (D) Anterior one-third of the cloacal chamber. (E) Anterior two-thirds of the cloacal chamber. (F) Posterior end of the cloacal chamber. Labels same as for Fig. 1 plus PF = primary folds, SF = secondary folds. FIG. 3.-Transverse

copei, 107.9 mm SVL. Scale in lower right corner = 300 ,m.

passing vent glands are so elongate that the distal ends of these glands curve dorsally to lie anteriorto the pelvic gland cluster. In A. jeffersonianum, A. latera'le, and

A. maculatum, the vent gland is more limited as described for A. tigrinum by Sever (1981). In these species, the vent gland cluster consists of a small number of elongate, thick glands that secrete with pos-


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teriorventral glands toward the caudal end of the cloaca, but have distal ends that pass anterolaterally. The cytology and staining reactions of cloacal glands of the other species are similar to those described for R. olympicus, except that some alcian blue positive material occurs in some posterior vent glands of D. copei and D. ensatus. DISCUSSION

Vent glands secrete onto the epidermis lining the caudal angle of the vent in males of many plethodontids, including species of Plethodon (Sever, 1978), Desmognathus (Sever, 1983), and the hemidactyliine genera (Sever, 1980, 1981, 1985, 1986). The 4-5 pairs of elongate, eosinophilic glands that secrete into the caudal end of the vent in Ambystoma tigrinum were considered homologous to the plethodontid vent glands by Sever (1981), and that usage is continued here for similar gland clusters in the additional species of Ambystoma and Dicamptodon examined. Male R. olympicus lack vent glands secreting into the cloacal orifice, but I apply the name "vent gland" to the large cluster of glands that secretes onto the skin lateral to the posterior end of the cloacal region. The homology of these glands in male R. olympicus with the vent gland of Dicamptodon and Ambystoma is based upon similarity of cytology and staining reactions. The location of vent gland orifices in R. olympicus is an autapomorphy for the species, and as such, does little to clarify its phylogenetic relationships (Eldredge and Cracraft, 1980; Hennig, 1966). Aside from the vent gland, much overall similarity exists in the cloacal anatomy of dicamptodontids, ambystomatids, and plethodontids, lending support for a close ancestral relationship among these groups as hypothesized, based upon other characters, by Duellman and Trueb (1986), Estes (1981), Hecht and Edwards (1977), and Milner (1983). Rhyacotriton olympicus, however, possessesrudimentarylateralpelvic glandsand primary and secondary folds of the cloacal tube, features found in dicamptodontids

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and ambystomatids but not in plethodontids (Sever, 1981, 1986). Plethodontidspossess a caudal pelvic gland cluster (Sever, 1986) which is absent in species of Rhyacotriton, Dicamptodon, and Ambystoma. These observations support divergence of the ancestral plethodontid stock from a clade that included the ancestor of species of Rhyacotriton, Dicamptodon, and Ambystoma. Because other characters indicate that the Plethodontidaeis the most recently derived group (Duellman and Trueb, 1986), the pelvic gland anatomy shared by species of Rhyacotriton, Dicamptodon, and Ambystoma may resemble the ancestral state from which that of plethodontids evolved. This hypothesis, however, makes the pelvic gland anatomy of plethodontidsautapomorphousand that of Rhyacotriton, Dicamptodon, and Ambystoma symplesiomorphous,which does not clarify phyletic relations among these genera (Eldredge and Cracraft,1980). The phylogenetic significance of the present findings, therefore, awaits further comparative studies on cloacal structures and their analysis with other morphological charactersof salamanders. Sever (1988) hypothesized that the ancestral function of cloacal glands was production of mating pheromones, and that portions of the ancestral pheromone-producing gland secondarily evolved the function of spermatophoreproduction. In male salamandrids,the dorsal (= abdominal) gland produces mating pheromones (Cedrini and Fasolo, 1971; Malacarne et al., 1984), and Sever (1980) suggested that the vent gland has this function in male plethodontids. Because the vent gland in male R. olympicus does not secrete into the cloaca, a role in pheromone production seems more likely than one in spermatophore formation. The only account of courtshipactivity in R. olympicus is by Arnold (1972), and he observed that males perform a "tail curled upward" behavior in which the tail is raised vertically and the distal tip is rhythmically swung back and forth. Arnold (1972:173) noted that a male in this position ". . . appears from the rear, even in dim light, as a vertical light line (his


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tail) with two light ovals (his vent lobes) near the base of the line on either side." The male may performthe tail curlwhen approachinga female, performingrubbing movementsagainsta female, or simply wheninvestigatinganemptycontainer (Arnold,1972). Futureobservationson the behaviorof male R. olympicus should consider the possiblerole of the vent glands in interindividualcommunication. Thepositionof the vent glandswith respectto the skinis idealforeasyremovalorexperimentalmanipulationwith the gland cluster.

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In M. K. Hecht, P. C. Goody, and B. M. Hecht (Eds.),MajorPatternsin VertebrateEvolution.Plenum Press, New York. HENNIG, W. 1966. Phylogenetic Systematics.University Illinois Press, Urbana. HUMASON, G. L. 1979. Animal Tissue Techniques, 4th ed. W. H. Freeman, San Francisco. KINGSBURY, B. F. 1895. The spermatheca and methods of fertilization in some American newts and salamanders.Trans. Am. Microscop.Soc. 17: 261-305. MALACARNE, G., L. BOTTONI, R. MASSA, AND C. VELLANO. 1984. The abdominalgland of the crested newt: A possible source of courtshippheromones. Preliminary ethological and biochemical data. MonitoreZool. Ital. (N.S.) 18:33-39. MILNER, A. R. 1983. The biogeography of salamanders in the Mesozoic and early Cenozoic: A Acknowledgments.-I thank R. A. Nussbaumfor cladistic-vicariancemodel. Pp. 431-468. In R. W. loan of all but one of the R. olympicus and all of the Sims,J. H. Price, and P. E. S. Whalley (Eds.), EvoDicamptodon. I thank A. Braswellfor the A. talpoilution, Time and Space: The Emergence of the deum, J. Jacoband A. Wynn for the A. jeffersonianBiosphere.Academic Press, London. um, C. D. Sullivan for the A. opacum, and R. Vogt NOBLE, G. K., AND M. K. BRADY. 1933. Observafor the A. laterale. tions on the life historyof the marbledsalamander, Ambystoma opacum Gravenhorst.Zoologica 11: LITERATURE CITED 89-132. SEVER, D. M. 1978. Male cloacal glands of PlethANDERSON, J. A. 1968. Rhyacotriton,R. olympicus. odon cinereus and Plethodon dorsalis (Amphibia: Cat. Am. Amphib. Rept. 68:1-2. Plethodontidae).Herpetologica34:1-20. ARNOLD, S. J. 1972. The Evolution of Courtship . 1980. Cloacal anatomy of male brook salBehaviorin Salamanders.Ph.D. Dissertation,Uniamanders(Eurycea). Herpetologica36:51-60. versity of Michigan, Ann Arbor. . 1981. Cloacal anatomy of male salamanBEHLER, J. L., AND F. W. KING. 1979. The Audubon ders in the families Ambystomatidae,SalamandriSociety Field Guide to North American Reptiles dae and Plethodontidae.Herpetologica37:142-155. and Amphibians.Alfred A. Knopf, New York. . 1983. Cloacal anatomy of male salamanBISHOP, S. C. 1947. Handbookof Salamanders.Corders in the plethodontid subfamily Desmognathinell University Press, Ithaca, New York. nae. Herpetologica39:16-27. CEDRINI, L., AND A. FASOLO. 1971. Olfactory at. 1985. Sexually dimorphic glands of Eutractantsin sex recognitionof the crested newt. An rycea nana, Eurycea neotenes and Typhlomolge electrophysiologicalresearch. Monitore Zool. Ital. rathbuni (Amphibia:Plethodontidae).Herpetolo(N.S.) 5:223-229. gica 41:71-84. COCHRAN, D. M., AND C. J. GoIN. 1970. The New . 1986. Disparate sexual variation among Field Book of Reptiles and Amphibians.G. P. PutGyrinophilus,Pseudotriton and Stereochilus(Amnam's Sons, New York. phibia:Plethodontidae).Herpetologica42:301-323. CONANT, R. 1975. A Field Guide to Reptiles and . 1988. The ventral gland in female salaAmphibiansof Eastern and Central North AmermanderEuryceabislineata (Amphibia:Plethodonica. Houghton Mifflin,Boston. tidae). Copeia 1988: 572-579. DUELLMAN, W. E., AND L. TRUEB. 1986. Biology STEBBINs, R. C. 1954. Amphibiansand Reptiles of of Amphibians.McGraw-Hill,New York. Western North America. McGraw-Hill, New York. ELDREDGE, N., AND J. CRACRAFT. 1980. Phyloge. 1966. A Field Guide to Western Reptiles netic Patternsand the EvolutionaryProcess.Methand Amphibians.Houghton Mifflin,Boston. od and Theory in ComparativeBiology. Columbia TIHEN, J. A. 1958. Commentson the osteology and University Press, New York. phylogeny of ambystomatid salamanders. Bull. ESTES, R. 1981. Handbuch der Palaoherpetologie. Florida State Mus. Bio. Sci. 3:1-50. Teil 2. Gymnophiona,Caudata. G. Fischer, Stuttgart. Accepted: 30 October 1987 HECHT, M. K., AND J. L. EDWARDS. 1977. The Associate Editor: John Iverson methodology of phylogenetic inference. Pp. 3-51.
