A Comparative Osteological Study of Two Species of Colubridae: (Pituophis and Thamnophis) Robert E

Brigham Young University Science Bulletin, Biological Series

Volume 8 | Number 3 Article 1

12-1966 A comparative osteological study of two species of Colubridae: (Pituophis and Thamnophis) Robert E. Bullock Lethbridge College, Lethbridge, Alberta, Canada

Wilmer W. Tanner Department of Zoology and Entomology, Brigham Young University, Provo, Utah

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Recommended Citation Bullock, Robert E. and Tanner, Wilmer W. (1966) "A comparative osteological study of two species of Colubridae: (Pituophis and Thamnophis)," Brigham Young University Science Bulletin, Biological Series: Vol. 8 : No. 3 , Article 1. Available at: https://scholarsarchive.byu.edu/byuscib/vol8/iss3/1

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Science Bulletin -^^OWP^ zc

UNIVERSITY A COMPARATIVE OSTEOLOGICAL STUDY OF TWO SPECIES OF COLUBRIDAE (PITUOPHIS AND THAMNOPHIS)

ROBERT E. BULLOCK

and

WILMER W. TANNER

BIOLOGICAL SERIES — VOLUME VIII, NUMBER 3

^y DECEMBER, 1966

I BRIGHAM YOUNG UNIVERSITY SCIENCE BULLETIN BIOLOGICAL SERIES

Editor: Dorald M. Allred, Department of Zoology and Entomology, Brigham Young University, Provo, Utah

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Bacteriology J. V. Beck, C. Lynn HArwAUD, Zoology

W. Derby Lavs^s, Agronomy

Howard C. Stutz, Botany

WiLMER W. Tanner, Zoology, Chairman of the Board

David L. Hanks, Botany

Ex officio Members:

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Science Bulletin

A COMPARATIVE OSTEOLOGICAL STUDY OF TWO SPECIES OF COLUBRIDAE (PITUOPHIS AMD THAMNOPHIS)

ROBERT E. BULLOCK

and

WILMER W. TANNER

BIOLOGICAL SERIES — VOLUME VIII, NUMBER 3

DECEMBER, 1966 TABLE OF CONTENTS

Page

INTRODUCTION 1 MATERIALS AND METHODS 2 VERTEBRAL COLUMN 3 Atlas 7 Axis 7 First Thoracic Vertebra 7 Other Thoracic Vertebrae 9 Lumbar Vertebrae 9 Anterior Caudal Vertebrae 9 Middle Caudal Vertebrae 13 Posterior Caudal Vertebrae 13 Ribs 13 SKULL 15 Premaxilla 15 Nasals 15 Septomaxillae 15 Vomers 15 Frontals 15 Prefrontals 17 Parietals 17 Postorbitals 17 Supraoccipital 17

Prootics - 17 Exoccipitals 19 Basioccipital 19 Basisphenoid 19 MaxiUae 19 Ectopterygoids 19 Palatines 19 Pterygoids 21 Supratemporals 21 Quadrates 21

Mandible ^ 21 Stapes 22 Hyoid Apparatus 22 OSTEOLOGICAL COMPARISONS 22 Vertebral Column 22

Skull .. 23 DISCUSSION 25 SUMMARY AND CONCLUSIONS 27 LITERATURE CITED 28 ABBREVIATIONS USED IN PLATES 28 LIST OF FIGURES

Figure Page

1. Atlas 4

2. Axis 5 3. First Thoracic and Thoracic Vertebrae 6 4. Thoracic and Lumbar Vertebrae 8

5. Anterior Caudal Vertebra 10

6. Middle Caudal Vertebra 11

7. Posterior Caudal Vertebra and Rib 12

8. Skull, Dorsal View 14

9. Skull, Lateral View 16 10. Skull, Ventral View 18 11. Hyoid Apparatus, Mandible, and Cranium 20 A COMPARATIVE OSTEOLOGICAL STUDY OF TWO SPECIES OF COLUBRIDAE {PITUOPHIS AND THAMNOPHIS)

Robert E. Bullock' and Wilmer W. Tanner-

INTRODUCTION

Snake anatomy has been genei-ally neglected. relative abundance. One of them (P. catenifer)

Although some early writers recorded observa- cxjnstricts its prey. other T. radix ) The ( swallows tions on the anatomy of snakes, no attempt has it alive. This difference in mode of feeding may been made to undertake a comprehensive study, be responsible for some structural modifications. and Cole (1944) has rightfully referred to this Although it is not the purpose of this study section of vertebrate anatomy as an "almost vir- directly to resolve any phylogenetic or ta.xonomic

gin field." Snakes deserve more intensive in- problems, it is hoped that it will encourage other vestigation because of the considerable number anatomical studies of reptiles, add to our present of adaptations demonstrated by them, their understanding of homologies, and indicate im- peculiar types of locomotion, and methods of portant internal phylogenetic and taxonomic feeding. It is important to comprehend their structures as suggested by Robinson and Tanner anatomical specializations if we are to under- (1962). stand the evolutionary trends among modern Although no previous investigator has studied reptiles. It also is evident that comparative de- the osteology of the two species included in this scriptions of serpents, thus far based mainly on study, the general gross anatomy of various external characteristics, need to be supplemented other snakes has been known for a long time. by accounts of their internal anatomy. Ahrenfeldt (1955) stated that as far back as 1573 there were some fragmentary accounts of The purpose of this study is threefold: snake anatomy published in Europe, but Cole

(1) To work out in detail the osteology of ( 1944 ) mentioned that it was not until 1683 that two common members of the family the first workmanlike and relatively accurate Colubridae. description of serpent anatomy was made by (2) To compare the bones and bone struc- Edward Tyson on a "Timber Rattlesnake" said tures of the two species in order to de- to have been collected in the West Indies.

Owen ( gave one of the first termine their anatomical similarities and 1866 ) detailed differences, and to use these comparisons accounts of the osteology and myology of snakes in determining the different speciahza- based on his work with the species Crotalus tions that have been made by two com- horridtis, Pijthon tigris. Boa constrictor, Naja mon serpents. tripudians, and Deirodon scaber. Although Owen's work on this section of the vertebrates (3) To relate the structural differences of is a general account by our standards, in his these genera, as far as possible, to some time it was a major contribution to this area of of the other generic groups previously anatomy. Another work dealing with reported. snake anatomy is a laboratory dissecting guide by Kel- Our original intent was also to include the licott (1898) for the genus Heterodon. Unfor- myology of the head, neck, and anterior tnmk tunately, the descriptions lack detail and are region (first 10 vertebrae). This proved to be a therefore somewhat superficial and in many major effort in itself, and such a report will ap- areas incomplete. pear separately at a later date. Huxley (1871), Gegenbaur (1878), Hoffman The gopher snake, Pituophis catenifer Blain- (1890), Sedgwick (1905), Wiedersheim and N'ille, and the plains garter snake, Thamnophis Parker (1907), VVilliston (192,5), Kingsley radix (Baird and Girard), were chosen for this (1917), Goodrich (1930), and Versluys (1937) study because of their moderately large size and were some of the early textbook writers who

^Lethbridge College. Lethbridge, AJberta, Canad ^Department of Zoology and Entomology, Brigha Young University, Provo, Utah. Brigham Young University Science Bulletin dealt with the subject of snake osteology. Most describes and compares the development of the of these writers restricted their studies to the cranial muscles and associated skeletal structures skull of serpents, and on occasion included one in forms ranging from the fishes to the mam- or more generalized vertebrae. Romer's "Osteo- mals. Haas (1930) and Cowan and Hick (1951) logy of the Reptiles" (1956) deals only briefly also dealt with the musculature of snakes, but with serpents, but does bring some of the termi- included skeletal structures as well. Albright and nology and many of the homologies up to date. Nelson ( 19.59 ) dealt with the cranial osteology Two volumes by Ludicke (1962, 1964) de- and the musculature of the colubrid snake voted entirely to the anatomy of serpents deal Elaphe obsolcta quadrivittata. rather extensively with the developmental and Perhaps more osteology has been done with adult anatomy of several species of snakes, in- venomous species, particularly with the teeth cluding a few colubrid species. Many of the (fangs) and sk-ull. The work of Klauber (1956: descriptions and comparisons in these works are 712-743) is a good example. of a general nature and, therefore, are of limited We made no major attempt here to e.xhaust value in making comparisons with the colubrid the references which may refer to snake anat- species involved in this study. omy. Those referred to above represent some of Sood (1941, 1948) published two papers the more important works that we have seen. dealing with the vertebral column of serpents. We were greatly surprised when we found rela-

The first is concerned with the caudal vertebrae tively few studies dealing with either of the two of the sandsnake, Eryx johnii (Russell), and common colubrid genera Pittiophis and Tham- illustrates many unique peculiarities in its verte- nophis. bral anatomv. The second studv includes both Our prime concern, therefore, is to provide minute and gross vertebral anatomy for several detailed descriptions and drawings which wiU other Asian species. set forth the skeletal anatomy as we found it in An extensive work by Edgeworth (1935) these genera.

MATERIALS AND METHODS

This comparative study utilized the species on a fine mesh screen and a jet of water was Pituophls catenifer deserticola Stejneger and used to clear away the remaining tissue. Some Thamnophw radix haydeni Kennicott. The four- of the bones were bleached in a 3% solution of teen specimens of P. c. deserticola used were hvdrogen peroxide for ten to twelve hours. collected in Grand, Kane, Utah, San Juan, Gar- Most of the articulated skeletons were pre- field, and Uintah Counties, Utah. The twelve pared from fresh material. The fresh, skinned, specimens of T. r. haydeni came from Warner and eviscerated snake was placed in a 25% County, Alberta, Canada. However, two speci- solution of ammonium hydroxide for one week, mens of P. catenifer sayi Schlegel from Medicine then boiled for t^vo to ten minutes until the

Hat, Alberta, Canada, two T. elegans vagrans tissues were loose but the ligaments still intact. Baird and Girard from Utah County, Utah, and A small jet of water was used to clear the soft four T. sirtalis parietalis Say from Salt Lake tissue from the vertebral column. This jet proved County, Utah, were also dissected and studied. to be too harsh on the more delicate and loosely These additional species are similar within their connected bones of the skull. To remove the respective genera; therefore, a description of deeper skull muscles it was necessary to use these is not included. forceps under a stereoscopic microscope. This The skeletons were prepared in several dif- latter method was essential in preparing skulls ferent ways, depending on whether fresh or without distortion or loss of small bones. preserved snakes were used, and upon the de- A few snakes preserved in alcohol were gree of articulation required. Disarticulated utilized in the preparation of skeletal material. skeletons were prepared from fresh material by These were cleaned by placing them for two bacterial action. The snake was skinned, evis- days in a solution of two ounces of trisodium cerated, and plac-ed in a container with enough phosphate to each quart of water. Tlie material water to cover the specimen so as to accelerate was then boiled in water for varying lengths of the decomposition process. After a few days in time, the time determined by the type of skeletal hot weather, the macerated material was placed preparation desired. Soaking the preserved OsPEOLOGv OF Snakes material in concentrated ammonium livdroxide and Ludicke (1962, 1964). The terminology for instead of trisodium phosphate before boihng the skull structures used herein was adopted proved to be almost as satisfactory. chiefly from Romer (19.56), and the terminology Specimens were studied and drawings made for the vertebral column from Sood ( 1941, to scale with the aid of a hand micrometer. 1948). Literature dealing with the complete osseous The two snakes studied are anatomically skeleton of the snake is fragmentary and limited. similar; therefore, to avoid unnecessary repeti- Because the literature to date, as far as we were tion a complete description of P. catenifer was able to ascertain, reveals no account of the prepared, but T. radix is discussed only in con- osteology of either P. catenifer or T. radix, the homologies were worked out and derived from nection with comparative structures that differ work done by Owen (1866), Kellicott (1898), in the two forms. Tlie plates were prepared with Romer (19.56). Sood (1941, 1948), and the more sufficient detail to aid in the comparisons of recent works by Albright and Nelson (19.59), similar structures in the two species.

VERTEBRAL COLUMN

In P. catenifer as in other snakes, the verte- C. Lumbar Subregion, consisting of the brae are numerous and procoelous, with ball and vertebrae situated between the thor- socket articulations wliich allow free movement. acic subregion and the caudal region. All of the vertebrae articulate with ribs except The hypapophyses are reduced in the atlas, axis, first thoracic, and caudals. The size or completely lacking in this successive vertebrae not only articulate by the area. usual pre- and post-zygapophyses and by the II. The Caudal Region procoelous centra, but also by additional articu- A. Anterior Caudal Subregion, situated lations such as the zygosphenes and zygantra. immediately behind the precaudal The division of the ophidian vertebral col- vertebrae. Vertebrae are provided umn into well-marked regions is less distinct with both fi.xed and articulating bi- than it is in other higher vertebrates. Owen furcated ribs called processi costo- (1866), Sedgwick (1905), Reynolds (1913), transversii or lymphapophyses. Williston (1925), and others considered the column to be made up of two regions—a pre- B. Middle Caudal Subregion, containing caudal region, and a caudal region. fixed ribs which are unforked and differing from the posterior caudal Five regions were distinguished by Roche-

) subregion in the absence of haema- brune ( 1881 —the cervical, thoracic, pelvic, pophyses. sacral, and cocygeal. Although these regions can be distinguished one from another, the differ- C. Posterior Caudal Subregion compris- ences are slight and variable. Because this classi- ing vertebrae with a pair of flat, fication was somewhat superficial and could not platelike haemapophyses on the ven- be regarded as ecjuivalent to the regions of the tral aspect of their centra. This area vertebral column of other vertebrates, it was shows a gradual reduction in the size presumably not adopted by later workers. and development of the vertebrae and vertebral processes from anterior Sood (1941, 1948) retained the division to posterior until they are repre- which separated the column into two regions sented near the end of the tail by (precaudal and caudal), but distinguished sev- extremely short vertebrae with al- eral subregions of each as follows: most wholly vestigial processes. I. Tlie Precaudal Region Because the division of the vertebral column A. Cervical Subregion, composed of the as outlined by Sood is in general use, the pre- first two vertebrae, atlas, and axis. ceding vertebral classification will generally be B. Thoracic Subregion, consisting of all followed; however, a few modifications have

the vertebrae that follow the axis and been made in order to adapt it to the species in- bear prominent hypapophyses. volved in this study. Bhigham Young University Science Bulletin

A.INT.F.

A.NEU.F.

A.NEU.F

Fig. 1. Atla-s. Pituophii catenifer, A-D, 9X: A, anterior; B, posterior; C, dorsal; D, lateral. Tliumiiophis radix, E-H, 15X: E, anterior; F. posterior; G, dorsal; H, lateral. Osteology of Snakes

N.S.

ZE. Bricham Young University Science Bulletin

PRZ.F

lateral; C-D, thoracic vertebra: Fig. 3. Pituophts catenifer, A-D, 7X: A-B, first thoracic vertebra: A, dorsal; B, dorsal; F, lateral; G-H, C, anterior; D, poiposterior. Thamnophis radix, E-H, 9X: E-F, first thoracic vertebra: E, thoracic vertebra: G. anterior; H, posterior. Osteology of Snakes

nected to the main centrum and the anterior Fig. 1-A, B, C and D hypapophvsis by a broad, curved suture. The apex of the odontoid has a rounded process The first cervical vertebrae or atlas differs which extends through the odontoid cavity of widely from the general vertebral pattern. It the atlas and rests lightly upon the basioccipital is a relatively narrow ring composed of tliree portion of the occipital condyle. lateral separate bones fused together by means of su- The articular surfaces of the process are c-onvex are tures. Tlie two lateral neural arches or neura- and received between articulate with the pophyses join dorsally as the sagittal neural su- and posteromesial neural arch facets of the atlas. ture; thev form a pair of neurocentral sutures The neural arch of the axis develops an elon- at their ventral borders where they unite with gate, posteriorly-projecting, ribless, transverse the intercentrum. Tliere is no neural spine, but process from each side of its base, a partially a nidimentary dorsal crest is developed. The developed zygosphene from the anterior dorso- centrum of the atlas actually coalesces with that lateral border of each side, and a moderately of the axis leaving the atlas without a true cen- long, posteriorlv-projecting neural spine from its trum, its place being taken by the autogenous coalesced dorsal surface. hypapophysis (Owen, 1866). Romer (1956) The posterolateral expansions of the neural arch form the zvgantrum stated that the atlas has been robbed by the a.xis internally and the postzygapophyses externally. of its centnmi, but has retained its intercentnmi. Anteriorly the intercentrum presents a concave The postzygapophyses contain flat, oval-shaped facets pointing ventrolaterallv the articular surface which articulates with the from expand- surfaces, whereas the has basioccipital tubercle of the occipital condyle. ed zygantrum two similarly articulating surfaces excavated Posteriorly a similar surface adjoins the ventral shaped from the inner surface of these expansions, surface of the odontoid process, as well as the same which point in a dorsomesial direction. post- interior facet of the anterior hypapophysis of the The zygapophyses articulate with the prezygapo- axis. Posteroventrally the intercentrum develops physes of the first thoracic vertebra while the a small conical hypapophysis. zygentral facets articulate with the zygosphenal The base of each neural arch half possesses thoracic vertebra. an anteromesial, concave articular surface which surfaces of the same receives the exoccipital tubercle of the occipital There are two hvpapophyses developed on condyle, and a posteromesial surface which ar- the ventral surface of the axis. The anterior one ticulates with the dorsal and lateral convex por- is sutured to the ventral border of the odontoid tions of the odontoid process. Each neural arch process as well as the anterior border of the pos- half carries a short postzygapophysis from the terior hypapophysis. It is somewhat triangular lateral border of its dorsoposterior region, and in shape with its curved dorsal suture represent- from its ventrolateral border a short conical ing the base of the triangle, and its apex point- transverse process points posteriorlv. The neural ing ventrally. The anterior vertical border con- canal is formed by the dorsal expansion of the tains an elongate, oval facet which articulates neural arch, while the smaller ventrally located with the intercentrum of the atlas. The posterior condylar or odontoid canal is formed between hypapophysis is an elongate spinelike process the mesial concave articular surfaces of the arch developed on the midventral aspect of the cen- and the dorsal surface of the intercentrum. The trum which points obliquely posterior. two canals are partially separated by a tough transverse ligament extending from the dorso- FIBST THORACIC VERTEBRA mesial border of one neiu-al arch half facet to the Fig. 3-A and B other. The intervertebral foramina are formed The first thoracic vertebra lacks free ribs and when the notches in the posteroventral edges is also otherwise modified. It differs from the of the neural ring of the atlas come in contact other thoracic vertebrae in possessing a rather with the anteroventral neural ring notches of elongate, transverse process much like that of the the adjacent axis. axis, a fairly long, narrow, posteriorly-pointing, AXIS bladelike neural spine, and in the absence of Fig. 2-A, B, C and D articular surfaces for the attachment of ribs. The The axis has a very stout and elongate cen- transverse process of these vertebrae is consid- trum which protrudes anteriorly, forming the ered by Romer ( 19.56 ) to be partially composed odontoid process, and terminates posteriorly as of short fused ribs. He therefore states that they a ball-like articulating condyle. The odontoid can be referred to as "cervical" vertebrae. Other process is a separate cone-shaped bone con- structures developed on this first thoracic verte- Brigham Young Univebsity Science Bulletin

vertebra, 6X: Fig. 4. Pituophis catenifer, A-D: A-B, thoracic vertebra, 7X: A, dorsal; B, lateral; C-D, lumbar lateral. lumbar C, dorsal; D, lateriil. Thamrwphis radix, E-H: E-F, thoracic vertebra, 9X: E, dorsal; F, G-H, vertebra, 7X: G, dorsal; H, lateral. )

Osteology of Snakes bra are similar to the other more typical verte- the neural arch of the preceding vertebra. The brae of tliis subregion and are discussed in c-on- zygosphenal surfaces are adapted to articulate nection with them. with those of the zygantra. The postzygapophyses and zygantra of the OTHER THORACIC VERTEBRAE thoracic vertebrae are very similar to those of Figs. 3-C and D, 4-A and B the axis except for their being slightly larger and more horizontally placed. The typical thoracic vertebrae are strong and The neiu-al spine is of moderate height, blocklike, being wider than they are long. Tlie placed about equidistant in its anteroposterior number of these vertebrae varied from fifty to extent on the vertebra, and is laterally com- in the specimens of P. catenifer fifty-three pressed and tnmcate. studied, but averaged approximately fifty-t\vo in There are typically two sets of foramina in number. Tlie centrum is not round, but ratlier the vertebral column—the intervertebral and the compressed dorsoventrally. Its anterior face intravertebral (Sood, 1948). Tlie intervertebral bears a concavity, the vertebrae being procelous. foramina have already been mentioned in con- Tlie socket faces a little ventrad from the greater nection with the atlas and a.xis, but they are prominence of the upper border; the prominent found along the entire column between con- ball terminates the back part of the centrum tiguous vertebrae. When viewed laterally each rather more obliquely, its aspect facing some- foramen is composed of two apertures—a dorso- what upward. Ventrally the centrum bears an lateral, superior inters'ertebral foramen and a elongate median hypapophysis e.vtending pos- ventrolateral, inferior intervertebral foramen. teroventrally, and terminating slightly posterior The zygapophysial articulation separates the to the condyle of the centrum. Tlie transverse single intervertebral foramen into its superior processes are short, bilobed structures arising and inferior external apertures. A feature not from the anterolateral portions of the centrum, noted previously is the presence of several pairs and extending ventrally in an obliquelv posterior of intravertebral foramina in addition to the pair direction. The major portion of each transverse of minute apertures situated ventrally in the process is covered by the rib articular surface. middle of each centrum on either side of the The dorsal lobe of each process is a convex sur- median longitudinal line. These additional in- face, whereas the ventral area is flattened and travertebral foramina are located as follows: even slightly concave. The area of the transverse a foramen on the dorsal surface of the proximal process which extends ventrally and anteriorly portion of each metapophysis, a foramen in the below the level of the centrum is referred to as middle of the base of each lateral wall of the the parapophysis. neural arch, a foramen or pair of foramina on The neural arches are broad, swollen struc- each side of the anterior central articular socket, tures facilitating the arrangement of the zygapo- and several pairs of minute foramina on the physes, whose nearly horizontal articular sur- roughened ridge dorsal to each postzygapo- faces are placed far apart from each other at a physis. These foramina are found not only in level not far above the floor of the jaeural canal. the thoracic vertebrae, but arc common to most The oval, transversally elongate facet of each vertebrae in all of the subregions. prezygapophysis is supported by a lateral process arising from the dorsal aspect of the trans- LUMBAR VERTEBRAE verse process, and is facing dorsad. Sood ( 1948 Fig. 4-C and D noticed that each prezygapophysis supported a lateral projection pointing outwardlv and The lumbar vertebrae vary in number from slightly forward, serving as a point of attach- 183 to 187 in the specimens studied. These ver- ment for muscles, and seemed to correspond to tebrae lack hv-papophyses, but possess a small, the metapophysis of mammals. rudimentary mid-ventral ridge. Most vertebrae A wedge-shaped process, the zygosphene, is iire slightly larger and heavier than those of the developed from the anterior border of the biuse thoracic subregion, but with the exception of of the neural spine and bears two smooth, oval, lacking hypapophyses, they are morphologically flat articular surfaces. These zygosphenal facets very similar. extend from the ventral apex of the wedge ANTERIOR CAUDAL VERTEBRAE (sloping dorsolaterally ) to its dorsolateral bor- Fig. 5-A. B, C and D ders. This wedge Ls received into the cavity (zygantrum) containing the zygantral facets, In general structure these five or six vertebrae wliich is excavated in the posterior ex-j^ansion of resemble those of the precaudal series. The Bhigham Young University Science Bulletin

POZ.F.

C. dorsal; D, lateral. Fig. 5. Anterior caudal vertebra, 6X. Pituophk Mtenifer, A-D: A, anterior; B, posterior; Thamnophis radix, E-H: E, anterior; F, posterior; G, dorsal; H. lateral. Osteology of Snakes 11

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CO.PR

^'^' 1«'^- A' ^"t^™--^ B. dorsal; C, lateral; LerJl"Z^%hT'''7-^'°J-^'^-^°''''"°'^^"'^''^'^^^^lateral, D, rib, 5X. Thamrwphis radix, posterior caudal vertebra, E-G, 12X; E, anterior; F, dorsal; G, lateral. Osteology of Snakes 13 region can be distinguislied, however, by the ab- subregion the vertebrae lack haemapophyses, sence of free ribs and tlie presence of fused or both colubrid snakes involved in this study articulating bifurcated ribs called lymphapo- possessed them. Tlie possession of haemapophyses. In the younger specimens studied the physes by middle caudals makes it rather diffi- lymphapophyses of the first anterior caudal ver- cult to distinguish between the last few verte- tebra articulate with the body of the vertebra, brae of this group and the first few vertebrae of as do the preceding ribs of the lumbar verte- the posterior caudal subregion. brae. In the majority of the older and more mature specimens the articulating surfaces were POSTERIOR CAUDAL VERTEBRAE somewhat fused, and in most incidences the Fig. 7-A, B and C lymphapophyses were not free to move in the The number of vertebrae involved in this same manner as articulating ribs. In a few of the subregion vary greatly from specimen to speci- mature specimens the only evidence of the pre- men; however, an average range is fifty-five to vious articulation is a groove aroimd the base of sixty-five. These vertebrae are similar in general the lymphapophyses. The lymphapophyses of pattern to the middle caudals, but they gradual- the remaining vertebrae of this subregion do not ly diminish in size until the last few are rudi- articulate or demonstrate any superficial indica- mentary. Their processes also show a gradual tion of such. reduction in size until they are almost vestigial structures These bifurcated (lymphapo- near the tip of the tail. physes) are associated with muscle attachment Although the demarcation between these as well as with the large lymph hearts on either vertebrae and the middle caudal group is some- flank; the divided processes extend outward, what arbitrary, it is possible to separate the two dorsal and ventral to the hearts. Tlie more ven- areas by the length and direction of the fixed tral branch is an elongate hornlike process ribs (transverse processes) as well as the struc- pointing posteroventrally. Tlie dorsal branch is ture of the haemapophyses. In this latter caudal much shorter and arcs in a ventrolateral direc- group the transverse processes point aiitero- tion. The dorsal and ventral branches of these ventrally; the fixed ribs of the middle caudals vertebrae, however, do show some degree of point either ventrally or posteroventrally, and morphological modification from vertebra to are longer. The apices of the haemapophyses ap- vertebra and from specimen to specimen. Both proach each other mesially until they almost branches show continuity in becoming reduced touch in the anterior portion of the posterior in size as they progress posteriorly. The dorsal caudals, whereas they are farther apart and branch is reduced to the point of becoming non- more rudimentary in the middle caudals of the existent in the middle caudal subregion, but the majority of the specimens studied. About midventral branch remains in its reduced form way along the posterior caudals, the haema- throughout the remaining caudal region. The pophyses undergo a transition whereby they pro- first one or two vertebrae of this subregion have ject almost straight downward in a posteroven- developed a small ridgelike hypapophysis, but tral direction with little or no inward curve, re- are devoid of haemapophyses. In P. catenifer, maining rather vddely separated at their distal however, the last few vertebrae of tliis section ends. possess a pair of flat, platelike, curved haemapophyses projecting ventrallv from the posterior part of each centrum. These structures are con- Fig. 7-D sidered to be chevrons by Romer (1956), and All of the precaudal vertebrae, except the serially homologous with the hypapophyses of atlas, a.xis, and first thoracic, articulate with a the precaudals. pair of vertebral ribs pleurapophyses ) . ribs ( The There was no apparent indication of sexual in the middle of the body are longer and heavier dimorphism in the vertebrae of this (cloacal) than the first and last few pairs. Tliey are terete, area. curved, pointed, and are so articulated that they move freely in an anteroposterior plane. Each MIDDLE CAUDAL VERTEBRAE articulates with the anterior edge of the cen- Fig. 6-A, B, C and D trum, the head being connected with the bilobed These three or four vertebrae differ from transverse process. Although the rib head is

the anterior caudals in possessing unforked, fixed single, the articular surface is divided into a ribs which are relatively long and only moder- flattened ventral portion and an adjacent dorsal ately curved. Although in Sood's criteria for this cupped area. Tlie rib head does not develop a Young University Science Bulletin 14 Brigham

EC. PO. PAL. SM.PR.

Fig. 8. Skull, dorsal. A, Pituophis catenifer, 4X. B, Thamnophis radix, 5X. Osteology of Snakes 15 true capitiilum or tubt'rciilum as is characteristic a posterodorsally-directed costal process for the

of higher vertebrates. Distal to the head there is attachment of muscle fibers.

SKULL

Tlie skull of P. catcnifcr is well ossified and maxillae form the floor of the internal nares. the bones are dense; the cranium is relatively Tliey are in contact dorsally with the nasals, long and broad, and the brain cavity extends anteriorly with the premaxillae, ventrally with Ix'tween the orbits. The apparent large size of the vomers, and posteriorly with the frontals.

the head is partially due to the arrangement of The septoma.xillae lie close together near the the supratemporals, cjuadrates, and mandibular mid-dorsal line, but do not suture. Their posterior structures. Tlie bones making up the skull are ex-tremities turn ventrad and come in contact for the most p;irt loosely articulated, thus making with the frontals. A pair of horizontal winglike possible a greater flexibility in the mouth region. processes extend laterally from about the middle of each bone, become narrow, and turn dorsally PREM AXILLA until they almost touch the descending dorso- Figs. 8-A, 9-A. 10-A lateral borders of the nasals.

The premaxilla is a single, small median bone which terminates the snout. Its anterior surface Figs. 8-A, 9-A, 10-A is an inverted Y-shaped ridge, the prongs of which extend in a ventrolateral direction. Tlie The edentulous vomers are connected to the dorsal process of the ridge curves posteriorly and ventral surfaces of the septomaxillae; at this wedges between the anterior portion of the t^vo union they fomi a pair of hollow, spherical nasals. From the ventral crotch of the "Y" there vomeronasal organs which open by paired ori- is a horizontal platelike process, terminally bi- fices into the buccal cavity. The inner margins furcated, ex-tending posteriorly. Its dorsal surface of the vomers do not suture, but are joined to articulates with the ventral surfaces of the an- adjacent elements only by connective tissue. terior septomaxillary processes, thus forming the Each vomer has three vertically-flattened pro- roof of the anterior portion of the mouth. Tlie cesses extending from its flat mesial border—an prema.villa does not bear teeth. anterior process connected to the septomaxilla, a posterior process connected to the mesial surface of the posteroventral process of the nasal Figs. 8-A, 9-A, 10-A and the posterior process of the septomaxilla, From a dorsal view the articulated nasals and a larger posteroventral process with a large appear as an ov^alshaped structure between the triangular fenestra occupying most of its area. premaxilla and the frontals, and are loosely con- The posteroventral process does not articulate nected to them by connective tissue. The nasals with any skull structures, but is connected by separate anteriorly to form an interspace, which connective tissue to other adjacent elements. receives the dorsal process of the premaxilla, but remain connec-ted posteriorly, forming a FRONTALS

pointed process which is received into the an- Figs. 8-A, 9-A, 10-A terior cleft between the two frontals. Dorsally The frontals are highly developed and form the nasals do not articulate with the frontals. The a complete enclosure for the anterior portion of nasals sheath the nasal cavities dorsolaterally, the brain. Tliey remain separate, but are joined and form a double median septum between mesially by the sagittal suture. The dorsal sur- them. This vertical septum extends postero\'en- face of each frontal is flat, subquadrate, longer trallv as a process which comes in contact with than broad, and there is a groove in each, parallel the fused anteroventral borders of the frontals. with the indented orbital edge. This groove is The posterior portion of the septum is in contact perforated with several supraorbital foramina in with the dorsal surface of the septoma.xillae. the adult forms. In younger snakes some of these foramina are not completely formed, but are SEPTOMAXILLAE mere indentations from the orbital margin. The Figs. 8-A, 9-A. 10-A anterolateral edge has a small, depressed articu- The elongate, horizontal, platelike septo- lar surfac-e to which the prefrontal is loosely at- Brigham Young University Science Bulletin

SOC. PR SM.PR.

Fig. 9. SkuU, lateral. A. Pituophis catcnifcr, 4X. B, TJwwnoplm radix, 5X. Osteology of Snakes 17 tached. The lateral surface, considered to be the posterodorsal surface of each orbit is expanded orbitosphenoidal plate of the frontal, joins the laterally by the parietal into a flattened lobe- dorsolateral margin of the frontal at an acute like process, the lateral border of which articu- angle, thus forming a major portion of the mesial lates with the curved mesial surface of the post- wall of the orbit. Ventrallv the descending walls orbital. A smaller coneshaped process, ventral to rest upon the presphenoidal prolongation of the the lobelike process, articulates dorsally with basisphenoid, completing the orbital septum and the posteroventral border of the postorbital. cranial floor. Each wall is notched posteroven- About midway down the coalesced sagittal sut- trally where it sutures with the anterior wall of ure, there are two small parietal foramina im- the parietal, thus forming the anterior jx)rtion of mediately lateral to the midline. each orbital or optic foramen. Through these foramina pass the optic nerves, eye-muscle POSTORBITALS nerves, and blood vessels. Anteriorly, where the Figs. 8-A, 9-A, 11-C frontals contact the nasals and septomaxillae, The small postorbitals, considered to be post- two large canals or ethmoid foramina, to facili- frontals by Owen (1866) and Kellicott (1898), tate the passage of olfactory nerves, are formed are narrow, elongate flattened bones which ar- by way of a vertiaxl, median double lamina (one ticulate with the anterolateral surfaces of the from each frontal). parietal, and form the dorsoposterior boundary PREFRONTALS of each orbit. A strong ligament connects the posterior part of each postorbital with the an- Figs. 8-A, 9-A, 10-A terodorsal surface of the ectopterygoids. Although some early workers considered the lacrimals to be present in snakes, Romer (1956) SUPRAOCCIPITAL stated that "lacrimals are absent; a foramen or Figs. 8-A, 9-A, 11-C groove for the lacrimal duct is present in the prefrontal." According to Gregory (1913), the The small butterfly-shaped supraoccipital is medially placed and unites anteriorly with the prefrontal of reptiles is not homologous with the lacrimal of mammals. parietal, laterally with the prootics, and posteriorly with the exoccipitals. It forms the roof From a lateral view each prefrontal is an irregular cone-shaped structure with a laterally of the posterior part of the brain cavity, and is compressed anterior process (forming the apex internally ex-panded from its lateral wings to of the cone) extending laterally to the posterior form the dorsal portion of each oHc capsule. The portion of the nasal, septomaxilla, and vomer. lambdoidal ridge or nuchal crest is prominent, The prefrontals loosely articulate with the and extends obliquely posterolaterally down anterolateral surfaces of the frontals, forming each side of the posterior portion of the cranium. crest diminishes the anterior edge of each orbit. A rather large Each lateral branch of the in size near the exoccipital articulation, b t con- lacrimal foramen or duct is located on the ventral tinues as a rather sharp ridge along the anterior border of each prefrontal near its articulation with the dorsal surface of the maxilla. border of the exoccipital, terminating at the posterior border of the fenestra ovalis. Dorsally a short median longitudinal ridge extends posteriorly, ending where the mid-dorsal suture Figs. 8-A, 9-A, 11-C joins the exoccipitals. Posteriorly the frontals articulate with the fused (coalesced) parietals, there being some degree of motility between the frontals and the Figs. 8-A, 9-A, 11-C parietal. The parietal is the largest of the cranial elements and forms the greater part of the Each prootic is an irregular quadrate-shaped braincase roof, but like the frontals, extends far bone forming the anterior part of the internal down either side of the brain, reaching ventrally otic capsule and the jx)sterolateral wall of the to the basisphenoid and forming the posterior braincase. It is bordered by the parietal an- portion of each orbit. The posterolateral borders teriorly, supraoccipital dorsally, exoccipital pos- of the parietal suture with the prootics. The tri- teriorly, and the basisphenoid and basioccipital angular-shaped, dorsal surface has its narrow ventrally. The anterior half of each fenestra apex attached to the supraoccipital posteriorly. ovalis is formed by the prootic; the exoccipital Dorsally a V-shaped pair of crests converge pos- completes the fenestra posteriorly. The foramen teriorly near the supraoccipital articulation. The is basically for the passage of the trigeminus, but Brigham Young University Science Bulletin

BO.HYP.

Fig. 10. Skull, ventral. A, Pituophis catenifer, 4X. B, Tliamnophis radix, 5X. Osteology of Snakes 19

also carries some facial nerve fibers. It is divided surfaces. Paired carotid foramina pierce the bone externally into two openings, both anterior to laterally to each process to enter the pituitary the fenestra ovalLs. The posterior foramen is fossa. This fossa is seen ventrally as a convex larger than the anterior one, and has a lateral area, and is the floor of the sella turcica in which proct*ss projecting posteriorly from its anterior the pituitary gland lies. A pair of foramina also border, therefore partially obscuring the open- pierce the posterolateral borders of this bone. ing. Other smaller foramina pierce each prootic, The narrow elongate parasphenoidal portion carrying cranial nerve fibers. of the basisphenoid extends anteriorly into the rostrum area, and becomes the floor of the orbit EXOCCIPITALS and optic foramen. A median longitudinal Fig.s. 8-A, 9-A, 10-A, U-C groove extends the entire length of the ventral The exoccipital bones form the posterolateral surface, whereas a dorsomesial keel is wedged between the ventral connection f walls of the braincase as well as part of its of the rentals. roof. They are joined together by a mid-dorsal suture, connected to the supraoccipital and pro- MAXILLAE otics anteriorly, and resting upon the basioc- Figs. 8-A, 9-A, 10-A cipital ventrally. The opisthotics are fused with Each maxilla is a short, curved bar that con- the exoccipitals, the combined bone thus sur- forms to the shape of the head. On the mesial rounding the jugular foramen and extending border, about midway, there is a small horizon- forward to form the [X)sterior border of the tal dorsoposteriorly-pointing process that articu- fenestra ovalis (Romer, 19.56). This jugular lates with the ventral surface of the prefrontal. foramen, which is internally subdivided into two The posterior end of the maxilla is broadened or more smaller aspects, is just posterior to the somewhat, and is received by the flattened club- fenestra ovalis, and is used for the passage of shaped ventral surface of the ectopterygoid. the ninth and tenth cranial nerves. Posteriorly Each maxilla bears sockets for about fifteen or the exoccipitals form the entire dorsoventrally- sixteen curved teeth, but not all of the sockets compressed, oval foramen magnum, except for contain rigidly fixed teeth; therefore, some a small ventral portion of the occipital condyle. are usually lost in the preparation of the skull. Posteroventrally the exoccipitals terminate as a In P. catenifer about every other tooth on the pair of articulating tubercles which form the maxillae, as well as the other tooth-bearing lateral portions of the crescent-shaped occiptal structures , was only loosely lodged in the condyle. grooves and could be removed very easily. The BASIOCCIPITAL maxillae are connected by fibrous tissue to the premaxillae, and not by an osseous articulation Figs. 9-A, 10-A, 11-C as in most vertebrates. The basioccipital is a pentagonal-shaped bone forming the floor of the posterior part of ECTOPTEBYGOroS the brain ca\'itA'. The ventral surface has a low, Figs. 8-A, 9-A, 10-A sagittal ridge with a laterally depressed area on The ectopterygoids, which were sometimes either side. Posteriorly a midventral tubercle referred to as the transpalatines by earlier work- forms the ventral portion of the occipital con- ers such as Kellicott (1898) and Wiedersheim dyle, thus completing the foramen magnum. The and Parker (1907), are small club-shaped, flat basioccipital is bordered laterally bv the exoc- bones connecting the maxillae to the pterygoid, cipitals, and is joined anteroventraliy with the and overlying each at its ends. Each flattened basisphenoid. spatulatelike anterior process is notched ante- BASISPHENOID riorly where it ligamentously articulates with the Figs. 9-A, 10-A maxilla, and an elongate, posterior end articulates with the dorsolateral groove in In the skull of adult serpents, the basisphen- the pterygoid which runs parallel with the curved contour of oid is applied without a suture anteriorly to tliis bone for its entire length. The ectoptery- the elongate parasphenoid, forming a single goids do not bear teeth. bone. The basisphenoidal portion of the bone is a flat, hexagonal plate, bounded dorsally at its PALATINES margins by prootic and parietal walls, and posteriorly by the basioccipital. A pair of prominent Figs. 9-A, 10-A transverse processes extend obliquely and ante- Tlie palatines are short bars placed anteriorly riorly toward the midline from its ventrolateral to the pterygoids, and mesially to the ma.xillae, Brigham Young University Science Bulletin

SOC. FO.M. OT.C.

BR.COR.

BO. HYP.

Fig. 11. Pituophis catenifer, A-C: A, hyoid apparatus, ventral, 4X; B. mandible, medial, 5X; C. cranium, po.sterior. 5X. D, Thamtiophis radix, cranium, posterior, 9X. Osteology of Snakes each bearing nine or ten teeth. The posterior sagittal plane, whereas its concave distal articu- end of each pahitine articulates with the ante- lating surface is extended transversely to form rior end of the pterygoid. About midway each an intercondyloid fossa for mandibular articu- palatine possesses a broad, flattened, horizontal, lation. About midway down the mesial side of median process with apex directed anteriorly, each quadrate there is a small, rectangular, and a similar but narrower lateral process ar- raised process which articulates with the distal ticulating with the ventral border of the pre- end of the stapes. frontal. The palatines are connected by fibrous MANDIBLE connective tissue to the snout elements. Figs. 8-A, 9-A, 10-A, 11-B

mandible is composed of two jaw bones PTERYGOIDS The which lack a firm anterior symphysis, but are Figs. 8-A, 9-A, 10-A connected by an elastic ligament anteriorly,

Each pter)'goid is a curved, flattened bar and is held together posteriorly to the symphysis extending from the palatine posterolaterally to by the transverse muscles. Each jaw bone is the angle of the mandible. Anteriorly it narrows long, curved anteromesially, and is separable and forms a loose articulation with the posterior into two major bones in the adult snake; how- end of the palatine. From this articulation a ever, the splenial and angular bones can some- row of eight to twelve teeth extends posteriorly times be separated in addition to these two along the medial border, ex'tending about mid- major elements. The longer pro.ximal part of way. The pterygoid receives the ectopterygoid each jaw is composed of angular, prearticular, into an elongated, dorsolateral groove. Posterior- articular, surangular, and splenial aspects, and ly the pterygoid narrows into a slender, curved is without teeth. Although the splenial and an- process that re.iches the base of the c|uadrate as gular are the only bones that can be separated well as the mandible. from this proximal portion of the jaw, the other bones are coalesced and form the following SUPRATEMPORALS areas: the articular and prearticular form the Figs. 8-A, 9-A, lO-A mandibular condyle area; the surangular ex- dorsomesial crest near The supratemporals are not true squamosals pands into a longitudinal the condyle, a deep lateral groove is formed at as some of the earlier writers indicated (Romer, the base of the crest, and the inferior dental 1956). Owen (1866) referred to them as mas- foramen opens at the bottom of the groove. The toids, but this terminology has been dropped in splenial angular bones are triangular shaped favor of the more applicable term (supra- and with their bases together and their apices point- temporal) used in this paper. The problem of ing anteriorly posteriorly from their mid- the homologies of the scjuamosal, supratemporal, and ventral location on the mesial surface of the jaw. etc., is, however, far from being solved in the The apex of the splenial points anteriorly; and various reptile groups, as pointed out by Jollie to the reduction in its size, the anterior (1960). owing part of the meckelian canal becomes an open Each supratemporal is a short, harrow, flat- anterior to the tened bone connecting the posterolateral dorsal mesial groove in the dentary just part of the skull with the proximal end of the splenial. Bogert ) uses the term postarticular quadrate. Anteriorly each supratemporal over- ( 1943 referring the process of the articular lays a portion of the parietal, prootic, supra- when to that extends posteriorly from the mandibular occipital, and exoccipital, and is attached to articulation with the quadrate. His was these cranial elements by fibrous connective work with the cobra and other elapids. tissue. The two bones are almost parallel to each The dentary forms the anterolateral portion other, converging only sbghtly as they extend of the jaw, contains a row of sixteen to posteriorly. and eighteen of the usual hooked or recurved teeth. QUADRATES It is short, curved, pointed anteriorly, and bifur- Figs. 8-A, 9-A, 10-A cated posteriorly on the lateral surface, thus

Each quadrate is a strong, rectangular bone; articulating with the anterior projection of the its proximal surface articulates with the postero- proximal portion of the jaw. This contact be-

lateral border of the supratemporal, and its dis- tween the two bones is not a close one; there-

tal, notched, condylar surface with that of the fore, it gives a degree of flexibility to the jaw.

mandibular condyle. Its proximal surface is The mental foramen is located near the middle twisted to become obliquely aligned along the of the lateral surface of the dentary. Bbigham Young University Science Bulletin

STAPES hyobranchial ) attached to the midventral raphe

Figs. 8-A, 9-A between the lower jaws; each rodlike branchial cornu e-vtends posteriorly along the lateral bor- Each stapes (columella) is a delicate, slender of the elongate tongue, being inserted into der, rodlike stylus connecting the otic capsule, the base of one of the elongate retractor muscles. by way of the fenestra ovalis, to the rectangular Suj^erficial, ventral cranial muscles are attached articular surface of the quadrate. Its pro.ximal to the basihyobranchial and the anterior portion end is enlarged to forni a footplate that fits of each comu. The hyoid apparatus is not at- into the foramen. The stapes is believed to tached to any of the skull elements as it is in transmit sound vibrations from the various jaw most other vertebrates, but lies imbedded in the bones to the otic capsule. muscle and fascia of the intermandibular region. The tongue, along with its posteriorly con- tinuing retractor muscles, is more than twice as HYOID APP.\RATUS long as the skull. The hyoid apparatus, there- Fig. 11-A fore, is modified into a very long structure in

The hyoid apparatus is a cartilagenoiis, V- this species even though it is a rather delicate shaped structure with its vertex or base (basi- organ.

OSTEOLOGICAL COMPARISONS

The two species considered in this study vertical process extending ventrad from the (Pituophis cafenifer and Thamnophis radix) ventral portion of the intercentrum. show many osteological similarities. There are, The major differences in the axis of the two however, a few significant structural differences species are found in the anterior and posterior existing between them. Some of these differ- hypapophyses. In T. radix the axis (Fig. 2-E, ences appear to be highly correlated with the F, G and H) develops a stout, hatchet-shaped, special adaptations made by the two species in anterior hypapophysis (Fig. 2-H) with its an- becoming more compatible with their specific terior articular facet placed vertically on its environments and food habits; however, there anterior border, whereas the previously-men- are many minor structural differences that would tioned, wedge-shaped, anterior hypapophysis of seem to be nonadaptive, or perhaps they ma\' P. catenifer (Fig. 2-D) possesses a narrower have other effects of survival value not apparent posteroventrally situated facet. The posterior to the authors. Only those differences which hyjiapophysis of T. radix (Fig. 2-H) is not as appear to be of sufficient magnitude to be com- spineUke or tapered as in the other species, pared, and perhaps have some bearing on the but is more trapezoid in shape with its ventral adaptation of these two species, will be dis- margin being somewhat truncate. cussed. Some of the less obvious differences existing A complete set of osteological illustrations in these vertebrae are the pro[X>rtionally narrow- for Thamnophis radix, corresponding to those of er odontoid process (Fig. 2-G), the more pos- Pituophis catenifer, has been included and will teriorly placed, dorsoventral odontoid suture be referred to in the course of the compara- (Fig. 2-G and H), and the greater anteriorly tive discussion. projecting portion of the neural spine (Fig. 2-H) in T. radix. VERTEBRAL COLUMN In T. radix the first thoracic vertebra (Fig.

Precaudal Vertebrae 3-E and F) lacks free ribs, just as it does in P. The atlas of T. radix (Fig. 1-E, F, G, and H) catenifer. The fixed ribs or transverse processes, is proportionately broader along the sagittal, however, are short, and extend posteriorly in

neural suture line ( Fig. 1-G and H ) than in both species. In the majority of the specimens P. catenifer (Fig.l-C and D), but its dorso- studied, the transverse processes of the first posterior projections containing the postzygapo- thoracic vertebrae were a little thicker at the physes are not as prominent. The hypapophysLs base, and less spinelike in T. radix (Fig. 3-F). of the atlas of T. radix (Fig. 1-H) does not This species also differs from P. catenifer in that

point posteroventrally as it does in P. catenifer the neural spine is narrower and slightly longer

( Fig. 1-D ) , but instead is represented as a small (Fig. 3-F), the anterior zygapophyses are placed ,

Osteology of Snakes 23 more mesially and are partially covered by the not attain as great a length proportionally, sweep zygosphenes when viewed dorsally ( Fig. 3-E ) back posteriorly, or curve as much ventrally at and there is a complete lack of metapophyses. its apex. The neural spine is also narrower and The other thoracic or typical t'loracic ver- projects more posteriorly (Fig. 5-H) in T. radix. tebrae show few noticeable differences between There are three or four vertebrae belonging the two species. It can be observed, however, to the middle caudal subregion in T. radix ( Fig. that in T. radix these twenty-two or twenty- 6-E, F, G and H), the same number as was three thoracic vertebrae ( Figs. '3-G and H; 4-E found to be present in P. catenifer. These verte- and F) develop proportionally smaller metapo- brae are similar in the two species, but there are phvses but larger transverse proc-esses (Fig. 3-G noticeable differences in their fixed ribs (trans- and H). The dorsal convex portion of the transverse processes ) and haemapophyses. In T. radix verse prcK-ess, bilobed rib, articular surface pro- the fixed ribs curve posteroventrally (Fig. 6-G) jects more laterally (Fig. 4-E and F), and the instead of anteroventrally ( Fig. 6-C ) as they do facets of the anterior zygapophyses are tilted in P. catenifer. The haemapophyses of this slightly more oblicjuely dorsad (Fig. 3-G) in species are more delicate in structure, not as T. radix than those of P. catenifer (Fig. 3-C). widely arched from each other at their midpoint The lumbar vertebrae of T. radix (Fig. 4-G (Fig. 6-E and F), and they project more pos- and H) retain relatively large hypapophyses teriorly (Fig. 6-G and H) than in P. catenifer. (Fig. 4-H), whereas the hypapophyses of P. The vertebrae of the posterior cauda sub- catenifer (Fig. 4-D) are lacking in this region, region of T. radix (Fig. 7-E, F and G) vary and are represented only by rudimentary mid- greatly in number from sjxjcimen to specimen ventral ridges. The presence of hypapophyses on just as in P. catenifer; however, an average the lumbar vertebrae of T. radix makes it very would fall somewhere between fifty and sixty difficult to distinguish the first few vertebrae of (an average of about five less than in P. cateni- this subregion from the last two or three thor- fer). For the most part, the same interspecific

acics. However, there is a decisive reduction in differences found in the middle caudal vertebrae the length of the hypapophyses extending over are carried over into the posterior subregion;

three or four vertebrae, making it jx>ssible to however, the neural spine slopes more obliquely

distinguish between the two vertebral areas anteriorly ( Fig. 7-G ) , and the transverse pro- with a relative degree of consistency. In T. radix cesses curve more anteriorly at their apices and

there is an average of approximately 136 or 137 are more pointed and less foothke (Fig. 7-G) lumbar vertebrae, compared to 185 or 186 found in T. radix. in P. catenifer. The lumbar vertebrae of T. radix There were no noticeable differences in the (Fig. 4-G and H) develop transverse processes ribs of the two species except for size. Tham- much like those of the thoracic vertebrae. The nophis radix, being the smaller serpent, de- dorsal rib facets are placed more dorsally (Fig. veloped proportionately smaller ribs. 4-H), and are more prominent laterally (Fig. 4-G) than in P. catenifer. In tliis species the ventral apex of each transverse process (para-

pophysis ) is devoid of a rib articular surface, and The skulls of both species are composed of thus forms an anteroventrally projecting process similar bones and bone structures; however, similar to those found on the thoracic vertebrae there are a few morphological and size relation- of botli species (Fig. 4-B and F). ship differences that do exist. The most apparent of these differences and those thought to be of Caudal Vertebrae some significance will be discussed. A dorsal The anterior caudal vertebrae of T. radix view of the skull of T. radix (Fig. 8-B), a (Fig. 5-E, F, G and H) number five or six in lateral view (Fig. 9-B), a ventral view (Fig. 10- the specimens studied. In addition to their total B), and a posterior view of the cranium (Fig. number being essentially the same as in P. 11-D) have been included to facihtate the com- catenifer, they also develop a ridgehke hypapo- parative discussion. first or physis (Fig. 5-E and F) on the one two The premaxilla of T. radix is more com- vertebrae of this subregion, and rather rudi- pressed dorsoventrally, having a distinct depres- mentary haemapophyses on the remaining three sion or fossa about midway along its dorsal or four. The dorsal branch of the lymphapo- surface (Fig. 9-B) in contrast to the ridgelike

physis does not arc as much ventrally in T. radix process in P. catenifer ( Fig. 9-A ) . This postero- (Fig. 5-E and F), and the ventral branch does dorsal process does not extend dorsally to wedge 24 Brigham Young University Science Bulletin

between the anterior portions of the nasals as it The basioccipital of T. radix develops a does in P. catcnifer. prominent, median, crestlike process or hypapo- The septomaxillae are heavier and more ex- physis (Fig. 11-D) for the attacliment of ventral tensive in T. radix. They cover a greater pro- neck muscles; this structure is not found on the portion of the ventrallv-attached vomers in this basioccipital of P. catcnifer. species, and the lateral winglike processes are From a dorsal view (Fig. 8) the size of the proportionately broader and turn posterodorsal- po,steromesial notch in the dorsal surface of each ly (Fig. 9-B) instead of anterodorsally (Fig. 9- exoccipital, where each sutures in the midline, A) as they do in P. catcnifer. The elongate, flat is greater in the case of T. radix (Fig. 8-B). anterior processes from the septoma.xillae are Both the quadrate and the supratemporal less tapered and more horizontally situated in are proportionately heavier and broader (Figs. T. radix. S-B, 9-B) in T. radix. Tliev do, however,

Although tlie frontals and prefrontals are occupy approximately the same position in both more rigidly attached in T. radix, there are no species. significant differences in these bones in a com- The maxillae, ectopterygoids and palatines parison of the two species. The parietal and (Fig. 10-A and B) are similar structurally in postorbitals, however, show a major structural the two species, but there is a difference in the

modification in T. radix. The parietal is narrow- number of teeth on the tooth-bearing structures

er proportionately, develops more prominent ( maxillae and palatines ) . The maxillae of T. dorsolateral crests, and lacks the small, paired radix bear about twenty-two or twenty-three

foramina on its dorsal surface (Fig. 8-B). In P. curved teeth as compared to the fifteen or six- catcnifer the parietal foramina (Fig. 8-A) are teen in P. catcnifer; the palatines bear about quite prominent. eighteen teeth as compared to the nine or ten teeth developed in P. catcnifer. The large, flat- In comparing the length of each parietal tened, median process of the palatine is directed with its width, it was found that in T. radix the more dorsally in T. radix, and in most cases the parietals were 1.1 times as wide as they were dorsal apex of this process arches mesially, ter- long, whereas in P. catcnifer they were 1.3 minating in a ventral direction. times as broad as long. The pterygoids (Fig. 10-A and B) are pro- The postorbitals of T. radix are not just portionately broader, their longitudinal ventral narrow, elongate bones attached to the antero- grooves deeper, and the number of teeth is lateral margins of the parietals as they are in greater in T. radix. This species bears about P. catcnifer (Figs. 9-A, 11-C). b'lt thev ex- twenty-seven or twenty-eight teeth (more than tend ventrally, coming in contact with the dorsal twice as many as found in P. catcnifer) in a surfaces of the anterior spatulate processes of longitudinal median row which extends almost the ectopterygoids (Figs. 9-B, 11-D). twice as far posteriorly as it does in P. catenifer. Some of the less obvious differences of the The pterygoid is abruptly curved laterally at its bones comprising the braincase are the narrow- posterior end, making the mandibular articulation er basisphenoid (Fig. 10-B) in the case of in T. radix; whereas in P. catcnifer the entire T. radix, with its transverse processes more pos- bone is gradually curved laterally until it articu- teriorly situated and extending laterally (perpen- lates posteriorly with the angle of the jaw. dicular to the midline) instead of obliquely and The mandible of T. radix is curved a Httle posterolaterally as in P. catcnifer (Fig. 10-A). more mesially at its middle dentary articulation The posteroventral surface of this bone presents (Fig. 10-B), and it contains from twenty-eight a convexity instead of a concavity as it does in to tliLrtv teeth on the dentary portion, or about P. catcnifer. In T. radix the prootics have a twice as many as previously recorded for P. prominent crest running longitudinally along catenifer. Both species have splenial and angu- their lateral borders just dorsal to the large lar bones that can be separated from the an- prootic foramina. This crest is somewhat hidden teromesial border of the proximal half of the by the lateral border of the supratemporal. The jaw bone (Fig. 11-B). lateral process which projects posteriorly, par- Although the shape and structure of the tially obscuring the opening to the posterior hyoid apparatus (Fig. 11-A) is very similar in prootic foramen, is not present in T. radix. the two species, it is proportionately longer in Therefore, the foramen appears round, from a T. radix, being appro.ximately 2.2 times longer

lateral view (Fig. 9-B), instead of kidney- than its mandible. In P. catenifer the hyoid is shaped (Fig. 9-A) as in P. catcnifer. only approximately 1.4 times longer than the .

Osteology of Snakes 25

mandible. Both specit's, however, develop a nated as the basihyobranchial. The specimens of rather large and functional hvoid apparatus. T. radix used in this study, however, did not According to Albright and Nel.son (1959), possess this anterior protuberance. Elaphe ohsoleta has a hyoid apparatus about Although Cowan and Hick (1951) did not twice the length of its skull. discuss the osteology of the hyoid apparatus of

Smith and Wanier (194S) figured a series Thamnophis siitalis as such, they indicated its of ophidian hyobranchia and included the genus structure by figures and descriptions concern- Pituophi.s, but not Thamnuphis. Their Fig. 1-R ing the hyoid musculature. According to these of Pituophii- is similar to our Fig. 11-A, but dif- authors the basihyal (basihyobranchial) por-

fers in that it is smoothly rounded anteriorly, tion of the hyoid of T. sirtalis is smoothly whereas we find Pituophis to exhibit a small rounded anteriorly, and does not possess an an- anterior protuberance which we have desig- terior protuberance.

DISCUSSION

From the foregoing comparisons it is evident Because of the close adherence of the atlas that there are osteological differences existing to the cranial elements and the difficulty in-

in the two species. In order to provide a com- volved in separating it from the skull intact, it

plete comparison of the differences it would be may be that some of the above statements are necessary to correlate and compare as many of not based on sufficiently meticulous dissection these interspecific differences as possible with to be complete. Possibly the true atlas has been other serpent groups (particularly colubrids) in overlooked in some cases, and has not been in- order to arrive at some osteological continuity cluded as part of the anterior vertebrae. A de- in the species studied, and to postulate some tailed study of many different genera would be

reasons for these differences. This is obviously necessary in order to determine the extent of the beyond the scope of this study. There are, how- ribless first thoracic vertebrae in the various ever, a few osteological differences that can be types of colubrid snakes. discussed, and these will be considered insofar The presence of metapophyses on the first as our data will permit. thoracic vertebra of P. catenifer, along with their greater The ribless condition of the first thoracic development on the other thoracic vertebrae, vertebrae, as demonstrated by P. catenifer and seems to indicate a more extensive area T. radix, has not been reported in the species for the attachment of lateral trunk muscles, giv- studied by the majority ing this constriction species an advantage in both of workers ( op. cit. ) strength Owen (1866) stated that the ribs commence in and motility in the neck and anterior trunk the cobra, as they do in other serpents, at the region. third vertebra from the head. Kellicott (1898) Tltatnnophis radix, being the smaller of the mentioned short transverse processes in connec- two species, has fewer precaudal vertebrae, but tion with the heads of the ribs as being present the proportionate number of the various types on all of the body vertebrae ( not including atlas of vertebrae in this region vary in the two and axis ) in Heterodon. A general statement was species (Table 1). There is a decrease of ap- made by Gadow (1901) concerning snakes, in proximately 48 (26%) lumbar and 28 (29%) which he states that "all the vertebrae, except thoracic vertebrae in T. radix when compared to the atlas, carry ribs." Albright and Nelson P. catenifer. It is evident from the above data (1959) reported short ribs on vertebrae 3 and that the larger snake (P. catenifer) owes much 4 of Elaphe, the first full-length rib being on of its greater precaudal body length to the great- the fifth vertebra. Ludicke (1962), on the other er number of lumbar vertebrae, but proportion- hand, reported that all of the vertebrae, with the ately or percentage-wise, there is an addition of exception of the atlas, can bear free ribs, but about twice as many thoracic vertebrae as com- the axis and the first two "cervical" or thoracic pared to the lumbar. vertebrae may also lack ribs in some species. Owen (1866) stated that hypapophyses are The latter statement appears to coincide more developed on the first seventy-four of 253 body fully with the findings of our study in which vertebrae in Python tigris, the first sixty anterior the first thoracic vertebra was lacking free ribs. l)ody vertebrae (305 total, counting caudals) in Brigham Young University Science Bulletin

Table 1. A comparison of the number of vertebrae in each of the vertebral regions and subregions of fourteen Pituophis catenifer and twelve Thamnophis radix. Both male and female specimens are included. )

Osteology of Snakes 27

row postorbitals approach but do not articulate ker ( 1907 ) , Gadow ( 1901 ) , and more recently with the upper jaw structures. Such an osseous by Edmund (1960), to mention a few. Almost connection is also lacking in Heterodon. all reptiles are polyphyodont ( number of denti- Tlie proportionately heavier and broader tions indefinite), but in some cases such as (juadrate and supratemporal in the case of T. Typhlopidae, certain teeth are not replaced and radix seems to c-oincide with the previously others undergo reduction (Wiedersheim and stated conjecture concerning rigidity in the jaw Parker, 1907). structures necessary for the feeding habit of this The greater number of teeth found on all species. of the tooth-bearing structures in T. radix ( Table According to Kellicott (1898) the basiocci- 2) seems to give this species an advantage in pital hv'papophysis, which is present in T. radix grasping and retaining struggling prey such as but missing in P. catenifer, is also lacking in frogs, toads, fish, grasshoppers, mammals, and Heterodon. Owen (18.54) stated that the python other regularly eaten animals. Tliis adaptation has a prominent hypapophvsis with a recurved to the nonconstrictor habit of food-getting was point, and that the rattlesnake also develops a noted previously in connection with the post- long, strong, recurved hypapophvsis from its orbitals, quadrates, and supratemporals. basioccipital which acts as a point of insertion The proportionately narrower posterior por- for the powerful ventral neck muscles, by which tion of the skull, due mainly to the narrower the downward stroke of the head is performed parietal, has possibly resulted from selection for in the act of inflicting a wound. more streamlined forms, in the case of T. radix, In both species studied, there were occasional which would have an advantage for life in the specimens which demonstrated an abnormally swampy areas where diving and swimming be- large number of teeth on some of their toothed come an integral part of its life. structures. It was noted that the bases of the extra teeth were lined up along the sides of the Table 2. A comparison of the number of teeth de- teeth in the normal tooth row, one tooth being veloped on die various tooth-bearing structures of fourteen Pituophis catenifer and twelve Thamnophis radix. firmly fi.\ed in the socket, and the more medially placed tooth being only connected to the bone Average Number of Teeth by fascia. It appeared as if the loosely connected

( Ranges in Parentheses teeth were being replaced by the firmly fixed Tooth-bearing Structures P. catenifer T. radix ones, thus maintaining a complete set of functional teeth at all times. This observation, per- Maxilla taining to the continual replacement of teeth in serpents, was noted in the works of West (1898), Kingsley (1917), Wiedersheim and Par- 28 Bricham Young University Science Bulletin cranium and its component bones, (8) the shape hypapophyses, (12) the number of maxillary, and character of the septomaxillary process, (9) pterygoid, and mandibular teeth, ( 13 ) the rela- the existence or lack of paired parietal foramina, tive size and character of the supratemporal,

(10) the shape and extent of the postorbitals, quadrate, and mandible, and ( 14 ) the relative (11) the presence or absence of basioccipital size of the hyoid apparatus.

LITERATURE CITED

Ahrenfeldt, R. H. 1955. Two Briti.sh anatomical Kellicott, D. S. 1898, The dissection of the Ophidi;in. studies on American reptiles (1650-1750) II. Ed- Gen. Biol. Supply House, Chicago. Kingslcy, S. 1917. of comparative anatomy ward Tyson: Comparative anatomy of the timber J. Outline rattle,snaike. Herpetologica, 2(l):49-69. of vertebrates. P. Blakiston, Philadelphia. Albright, R. C, and E. M. Nelson. 1959. Craniiil Klauber, L. M. 1956. Ratdesnakes. Univ. California kinetics of the generalized colubrid snake Elaphii Press, Los Angeles, 2:710-1476.

obsoleta qtiadrivittata. I. Descriptive morphology, Ludicke, M. 1962. Ordnung der Khisse Reptiha, Serpentes. Handbuch der Zoologie, 1-128. and II. Functional morphology. J. Morph., 105(2): 7(5):

193-492. . 1964. Ordnung der Klasse Reptilia. Ser-

Bogert, C. M. 194.3. Dentitional phenomena in cobras pentes. Handbuch der Zoologie, 7(6) : 129-298. and other elapids with notes on adaptive modifica- Mookerjee, H. K., and G. M. Das. 1932. Occurrence

tions. Bull. Amer. Mus. Nat. Hist., 8 1 ( 3 ) : 285-360. of a paired parietal bone in a snake. Nature, 130: Brongersma, L. D. 1938. On the presence or absence 629. of hypapophyses under the posterior precaudal ver- Owen, R. 1854. The principal forms of the skeleton tebrae in some snakes. Zool. Meded. Leiden, 20: and of the teeth. Blanchard and Lae, Philadelphia,

240-242. , 1866, The anatomy of vertebrates, Long- F. 1944. history of comparative anatomy. man, Green and Co,, London, 1:53-57, Cole, J. A Macmillan, London. Reynolds, S. H, 1913, The vertebrate .skeleton. Uni-

Cowan, I., and W. Hick. 1951. A comparative study versity Press, Cambridge. of the myology of the head region in three species Robison, G. W., and W. W. Tanner, 1962. A com- of Thamnophis. Trans. Roy. Soc. Canada, ser. 3, parative study of the species of the genus Crota-

45(3). phi/tus Holbrook ( Iguanidae ) , Brigham Young Uni- Edgeworth, F. H. 1935. The cranial muscles of ver- versity Sci, Bull,, Biol, Series, 2(1):1-31, tebrates. Univ. Cambridge Press, Cambridge. Rochebrune, A, F, 1881, Memoire .sur les vertebres Edmund, A. G. 1962. Se{juence and rate of tooth (Paris), 17:185-229. des ophidiens, J, Anat, Physiol. replacement in the Crocodilia. Life Sciences Divi- Romer, A. S. 1956. Osteology of the reptiles. Univ. sion Contribution 56, Toronto. — Chicago Press, Ilhnois. Gadow, H. 1901. Amphibians and reptiles. Macmil- Sedgwick. A. 1905. A student's text-book of zoology. lan, London. Swan Sonnenschein and Co., Ltd., London, v, 2, Gegenbaur, C. 1878. Elements of comparative anatomy. Macmillan, London. Sood, M. S. 1941. The caudal vertebrae of Erijx 14:390- Goodrich, E. S. 1930. Studies on the structure and jolmii (Russel). Proc. Indian Acad. Sci., development of vertebrates. Macmillan, London. 394.

Gregory, W. K. 1913. Homology of the "lacrimal" . 1948. The anatomy of the vertebral column and the "alisphenoid" in the recent and fossil rep- in serpents. Proc. Indian Acad. Sci., 28:1-26. tiles. Bull. Geol. Soc. Amer., 24:241-246. Versluys, 1937. Kranium und visceralskeUett der J. kopfskelett und die haut- Haas, G. 1930. Ueber das Reptilien, In Bolk et al. Handbuch der verg- muskulatiu- der Typlilopiden und Glauconiiden. leichenden anatomic der WirbelHer, 4:780-7, Zool. J;ihrb., Abt. Anat., 52:1-94, 95-218, 347-404. West, G, S, 1898, Tooth succession, Linn, Soc, Hoffman, C. K. 1890. Reptilien. In Bronn's Kla.ssen J. 26:517-526. und Ordmmgen des Tier Reich, 6(3) :1420-1465. Wiedersheim, R,, and N. Parker. 1907. Compara- Hu.\ley. T. H. 1871. A manual of anatomy of verte- W. tive of vertebrates. Macmillan, London. animals. and A. Churchill, London. anatomy brated J. Jollie, M. T. 1960. The head skeleton of the hzard. Williston, S, W. 1925. The osteology of the reptiles. Acta Zoologica, 41:1-64. Harvard Univ. Press, Cambridge.

ABBREVIATIONS USED IN PLATES Osteology of Snakes 29

LP.D.B. l)Tnp]iapophysis dorsal branch. D. dentary. LP.V.B. lymphapophysis ventral branch. D.F. dental foramen. MET. metapophysis. EC. ectopterygoid. N.C.S. neiiro-central suture. EO. exoccipital. NEU. neurapophysis. FO.M. foramen magnum. N.S. neural spine. FOV. foramen (fenestra) ovalis. N.SU. neural suture. FR. frontal. O.CL. odontoid canal. J.F. jugular foramen. O.PR. odontoid process. M. ma.villa. PARP. parapopliysis. ME.F. mechelian foramen, canal or P. HYP. posterior hypapophysis. groove, P.INT.F. posterior intercentral facet. NAS. nasal. POZ. postzygapophysis. o.c. occipital condyle, POZ.F. postzygapophysial facet. OP.F. optic foramen, PRZ. prezygapophysis. OT.C. otic capsule, PRZ.F. prezygapophysial facet. PAL. palatine, RB.F. rib facet. PAR. parietal, RB.H. rib head. PARA. parasphenoid. SH. shaft. PAR.F. parietal foramen, T.PR. transverse process. PER. prefrontal, ZE. zygosphene. PM. premaxilla. ZE.F. zygosphenal facet. PO. postorbital. ZM. zygantrum. PR. prootic. ZM.F. zygantral facet. PRA. prearticular. PT. pterygoid, QU. quadrate, SA. surangular. A. angular. SM. septoma.xilla. AR. articular. SM.PR. septomaxillary process, BH. basihyobranchial. SOC. supraoccipital. BO. basioccipital. SP. splenial. BO.HYP. basioccipital hypapophysis. ST. stapes. BO.T.PR. basioccipital transverse process. SUP. supratemporal. BR.COR. branchial comu. vo. vomer, B.S. basisphenoid. V. fifth cranial nerve.