Phyllorhynchus browni

Cadle, John E., 2011, Hemipenial morphology in the North American snake genus Phyllorhynchus (Serpentes: Colubridae), with a review of and comparisons with natricid hemipenes, Zootaxa 3092 (1), pp. 1-25 : 4-7

Phyllorhynchus browni

I discovered two distinct hemipenial morphologies in Phyllorhynchus browni ( Fig. 3 ), the significance of which is presently unknown. Both are similar in the morphology and configuration of the sulcus spermaticus, but differ in terms of overall size, shape, and apical morphology (single vs. bilobed) among other things. I describe each morphology, first the larger bilobed organ of AMNH R-70704, which is more similar to P. decurtatus and which I refer to as “morph I” or “ P. browni I”, then the smaller unilobed organ of CAS 160226 (“morph II” or “ P. browni II ”). These are followed by the retracted organ of CAS 160227. A full exploration of the significance of the differences between morphs I and II is beyond the scope of this paper but Appendix 2 provides ancillary material germane to further investigation.

“ Morph I”, Everted (AMNH 70704. Fig. 3A , left hemipenis). Total length about 14.5 mm, bilobed for about 1.5 mm. A bilobed organ with an overall shape similar to Phyllorhynchus decurtatus ( Fig. 1 ) but with shorter lobes. The base is strongly flexed toward the sulcate side and its narrowness is exaggerated in Fig. 3A because the hemipenis was tied off with thread during fixation; without the artificial constriction the base was probably similar in shape and length to that of P. decurtatus ( Fig. 1 ). Base with some very small spines on the asulcate side, nude or only with widely scattered small spines on the sulcate side.

Sulcus spermaticus centrolineal, with greatly divergent lips distally, one branch of lip tissue going to the inside of each lobe but not fully to the crotch (some damage to the right lip due to a small hole in the apex). Tissue between the divergent lips and the entire apex are nude. Each branch of lip tissue ends short of the tip of its lobe, petering out abruptly before it reaches the point of internal attachment of the retractor muscle. The morphology and relationship between the sulcus lips and apical tissue is similar to that described above for P. decurtatus .

Ornamentation of the hemipenial body (spine size and arrangement and asulcate triangular nude area) generally similar to that of Phyllorhynchus decurtatus but without such distinct bulbous tissue bearing the spines. There are no definitive calyces but distally on the lateral surfaces are a few somewhat reticulating ridges connecting adjacent spines, forming a network. Sulcus spermaticus proximal to its divergent lips bordered by a broad nude area on each side. Distally, these nude areas continue along the lateral sides of the divergent lips but (unlike in CAS 160226 described below) these portions do not appear especially thickened.

Apex entirely nude. On the apex distal to the divergent sulcus lips is a line of whitish tissue on each side extending toward the crotch from a point near the internal attachment of the retractor muscles (the line on the left lobe easily visible in Fig. 3 ; the line on the right lobe is incorporated into the damage on that side). Although superficially having the appearance of ‘lip tissue’ completing the distal edge of a divided sulcus, this white tissue is neither thickened nor raised above the level of the apical tissue. Thus the sulcus spermaticus has a greatly divergent sulcus lips, as in the above-described hemipenis of Phyllorhynchus decurtatus .

“Morph II”, Everted (CAS 160226. Fig. 3B , left hemipenis). Total length about 11.5 mm. Hemipenis unilobed, overall shape slightly bulbous and gradually broadening from base to tip. Short basal section nude and without pockets or lobules. A short area follows that has two or three loosely arranged rows of minute spinules/ papillae (they seem to have some mineralization), followed abruptly by greatly enlarged hooked spines. The hooked spines differ in size and density on the hemipenial body (described below).

Sulcus spermaticus centrolineal until about the level at which the enlarged spines peter out on the sulcate and lateral sides. At that point the sulcus lips flare greatly and the sulcus groove expands and opens into the nude apical tissue. Between the divergent sulcus lips are fine longitudinal ridges, which are probably remnants of folded tissue necessary to permit expansion of the sulcus tip upon eversion of the organ. Starting roughly where the lateral spinose regions impinge on the sulcus tip, the lips of the sulcus are hypertrophied in width and seemingly in thickness. From there the hypertrophied portions extend laterally and distally on the sulcate side of the organ, ending just distal to the spinose areas on the lateral sides; the sulcus lips remain mostly on the sulcate surface of the organ. The edges of the hypertrophied region are strongly defined because the raised tissue stands out above the surrounding surface of the organ; at the expanded sulcus tip, the hypertrophied tissue overhangs the tissue within the expansion. Although the hypertrophied lips have the appearance of being solid, study of a retracted organ (see below) shows that the lips are not solid structures. Instead, they comprise loose tissue that is inflated in the everted organ and their thickened appearance in everted hemipenes is illusory.

Enlarged spines in eight to ten rows on the sulcate and asulcate sides. On the sulcate side the spines occupy a pair of slightly bulbous expansions, one on each side of the sulcus spermaticus; the sulcate spines impinge on the lips of the sulcus for a short distance (thus, no narrow nude strip bordering the sulcus as in P. decurtatus ). Proximally on each lateral side are about four rows of enlarged spines followed distally by a dense patch of small, slen- der, weakly curved short spines; these patches are seen in asulcate view ( Fig. 3B ) just proximal to the narrowing of the apex. That these small spines are mineralized spines rather than soft papillae was confirmed by probing with a fine needle and by subsequent staining with alizarin (see Appendix 2). On the asulcate side spines occupy a pair of bulbous expansions bordering a triangular expanse of nude tissue extending down from the apex to about the widest part of the organ (or about half the length of the organ); in Fig. 3B this nude expanse is largely hidden by the overhanging spinose bulbous expansions. About four rows of very large spines proximal to the nude area; spines relatively straight, hooked at the tip, and project toward the base of the organ.

Apex completely nude and narrowed compared to the distal end of the spinose areas (abrupt transition between the spinose area and the nude apex). No definitive calyces are present. However, distal to the lateral patches of small spines is a very small area containing a few short, somewhat anastomosing low ridges, some of which enclose small depressions.

Retracted (CAS 160227. Fig. 2B , right hemipenis). Hemipenis extends to the end of subcaudal 16 and is distally slightly bilobed. Total length about 25 mm. Major retractor muscle proximally divided for about 2.5 mm.

Sulcus spermaticus in the dorsolateral wall of the organ, distally with divergent lips. Between the divergent lips is a series of longitudinal folds composed of very thin tissue, which apparently expands upon eversion to produce the nude apex. The short lobes in the retracted organ seem to be occupied by the hypertrophied tissue of the sulcus lips.

The hypertrophied distal lips of the sulcus are broad pieces of highly rugose tissue (not solid pads, as they appear to be on the everted organ). However, they do have thickened edges adjacent to the sulcus and all around their periphery (edges away from the sulcus are more prominent than those bordering the sulcus). The rugosities are very dense and irregular, not in any particular pattern.

The elongate bulbous projections on the asulcate side of the everted organ are produced by long flabby spinose folds in the retracted organ. This tissue becomes increasingly rugose and folded distally, with the most distal portions having somewhat anastomosing folds, forming irregular calyx-like structures. The walls of these irregular calyces lack integrity, which explains why the calyx-like structure is not maintained in the everted organ; thus, they are pseudocalyces sensu Myers & Cadle (1994). The nude area between these projections apparent in the everted organ appears, in the retracted organ, as smooth unornamented tissue between the highly corrugated/spinose tissue of the projections. The tissue immediately distal to the small spinose patches on the lateral side is reticulated, fleshy (this forms the anastomosing tissue on the lateral sides of the everted organ at the edge of the apex).

Remarks. Dowling & Duellman (1974–1978: Fig. 112b.9) and Dowling (1975: 199) provided a drawing of a hemipenis of “ Phyllorhynchus ”. The same illustration was later reproduced and identified as P. browni based on AMNH R-92892 by McDiarmid & McCleary (1993: Fig. 3 ) but this specimen is a skeleton and has no associated hemipenis (D. Kizirian, personal communication, September 2010). Later, Dowling (2002: Fig. 4C ) reproduced the same illustration (as P. browni ) and stated that it was an incompletely everted organ based on UMMZ 58386 (not independently verified by me). The published illustration appears similar to the organ of AMNH R-70704 (“morph I”) here described except for the uneverted apex. Dowling (2004: 321 and Fig. 4 ) published a different illustration of a partially everted hemipenis identified as “ Phyllorhynchus ”, completing from memory the outline of “originally-observed lobes”. However, his completed illustration ( Dowling 2004: Fig. 4 ) shows a pair of long, acutely pointed apical lobes unlike the rounded hemipenial lobes of P. decurtatus ( Fig. 1 ) or the much shorter lobes of “ P. browni I”, AMNH R-70704), and completely unlike the unilobed organ of “ P. browni II ”, CAS 160226) ( Fig. 3 ).

The figure in Dowling & Duellman (1974–1978: Fig. 112b.9) seemingly also shows small calyces toward the distal end of the hemipenial body, which are lacking in all everted organs of P. browni I examined. Zaher (1999: 28) also thought these illustrated structures represented calyces, but he also failed to find calyces in the P. browni hemipenis he examined (LSUMZ 37959). However, Cope (1895: Pl. 19, fig. 4; 1900: Plate 17, fig. 4) showed calyces in his illustration of a retracted P. browni hemipenis; these presumably represent the anastomosing folds (pseudocalyces) present in retracted organs, as described above.

Figures

FIGURE 1. Everted hemipenis of Phyllorhynchus decurtatus (CAS 223608) in sulcate (left) and asulcate (right) views. A, detail of the divergent lips of the sulcus spermaticus, one lip passing to each lobe (CAS 223608); B, outer (lateral) surface of the right lobe showing the low ridges passing over the apical tip (CAS 178969).

FIGURE 2. Retracted hemipenes of A, Phyllorhynchus decurtatus (CAS 178969) and B, P. browni (CAS 160227); apical (distal) ends of organs that were slit midventrally and spread flat. R, retractor penis magnus. ss, sulcus spermaticus (lettering placed over the sulcus proximal to the divergent lips). Arrows indicate lips of the sulcus after the point of divergence.

FIGURE 3. Everted hemipenes of Phyllorhynchus browni. A, “Morph I” (AMNH R-70704) in sulcate (left) and asulcate (right) views. The base of AMNH R-70704 is artificially narrowed because it was tied off during preservation; the sulcus lip on the right lobe is damaged near the base of the crotch. B, “Morph II” (CAS 160226) in sulcate and asulcate views.

FIGURE 4. Everted hemipenes of natricids in sulcate view. A, Afronatrix anoscopus (CAS 230205). B, Amphiesma bitaeniatum (CAS 215037) (detail of apex shown in Fig. 5A). C, Natrix tessellata (CAS 183115) (detail of apex shown in Fig. 5D).