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The Baculum In Microtine Rodents Part 1

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The Baculum in Microtine Rodents.

by Sydney Anderson.

INTRODUCTION

Didier (1943, 1954) has described the bacula of several Old World microtines, and other rodents. Argyropulo studied (1933a, 1933b) five species of Cricetinae and _Microtus socialis_. Ognev (1950) ill.u.s.trated numerous species of Eurasian microtines. Hamilton (1946) figured and described the baculum of 11 species of North American microtines. Hibbard and Rinker (1942, 1943) figured the baculum of _Synaptomys cooperi paludis_ and of _Microtus ochrogaster taylori_. Dearden (1958) studied the baculum in two Asiatic species of _Lagurus_, in six subspecies of _Lagurus curtatus_ of North America, and in six other species of microtines of other genera.

The baculum can be preserved easily with standard study skins, and is potentially useful in interpreting relationships on any taxonomic level, and especially in determining the relationships of species within a genus, if used together with other structures.



The anatomical orientation of the baculum needs comment because some confusion exists in the literature, especially concerning the use of the terms ventral and dorsal. The urethra lies on the anatomically ventral side of the p.e.n.i.s, and of the baculum. In the center of the p.e.n.i.s lies a single corpus cavernosum p.e.n.i.s, shown in cross section proximal to the baculum in Figure 1c. Dorsally an artery, thinner walled than the ventral urethra, ends in a somewhat reticulate sinus surrounding primarily the middle part of the baculum within the bulbous glans p.e.n.i.s. The corpus cavernosum p.e.n.i.s (the structure has no median septum, at least distally) terminates with the baculum and is closely knit to it. The site of this bond is evident in the tuberosities and sculpturing of the base of the baculum.

The part of the p.e.n.i.s enclosing the baculum, when not erect, is folded back as shown in Figures 1a and 1b. As a result the anatomically ventral surface faces upwards, or at least posterodorsally. The use of the term ventral in this account refers to the anatomically ventral side, that is to say to the side of the baculum facing the urethra.

The baculum in microtines consists of an elongate stalk, having a laterally, and to a lesser extent dorsoventrally, expanded base and an attenuate distal shaft. Usually, three digitate processes of cartilaginous material in which additional ossifications may occur arise from the terminus of the shaft. The proportions and curvature of the stalk vary as do the proportions of the terminal ossifications to each other and to the stalk. In some species one or more of the digital processes are frequently completely unossified.

[Ill.u.s.tration: FIGURE 1. The baculum in _Microtus ochrogaster_--orientation and variation with age. _a._ Diagram of a sagittal section of the posterior half of a vole, natural size. The p.e.n.i.s, containing the baculum (in black), extends ventrally from a point posterior to the pubic symphysis (stippled), along the body wall, and bends posteriorly at the distal end. _b._ Distal end of p.e.n.i.s ( 2) showing baculum (in black), the urethra (solid lines) adjacent to the baculum, and the corpus cavernosum (broken lines) proximal to the baculum. _c._ Oblique view of the cross section of p.e.n.i.s ( 4) shown in Figure 1 _b_. The thick-walled urethra lies ventral to the curved corpus cavernosum. A thinner-walled blood-vessel lies dorsal to the corpus cavernosum. The anatomically ventral side of the baculum, in the normal non-erect p.e.n.i.s shown, is seen to face dorsally. _d._ Graph showing the relationship between size of baculum, size of animal, and development of digital ossifications. Circles show presence of ossification in stalk only; circles enclosing dots indicate presence of secondary ossification in median process also; large dots indicate the addition of tertiary ossification in one or both of the lateral digitate processes.]

Preserved specimens of _Microtus arvalis_, _Microtus agrestis_, _Microtus orcadensis_, _Microtus nivalis_, _Microtus guentheri_, _Microtus subterraneus_, _Clethrionomys glareolus_, and _Ellobius lutescens_ were provided by Prof. Robert Matthey of Lausanne, Switzerland. J. Knox Jones, Jr. carefully saved the bacula with specimens of _Microtus fortis_ and _Clethrionomys rufoca.n.u.s_ from Korea. Dr. W. B. Quay, Department of Zoology, University of California, supplied specimens of _Synaptomys cooperi_, _Phenacomys intermedius_, and _Microtus oregoni_. Dr. Franklin Sturges and Mr. John W. Goertz, Museum of Natural History, Oregon State College, Corvallis, have provided specimens including bacula of _Clethrionomys occidentalis_, _Microtus oregoni_, and _Microtus townsendii_. Dr. Randolph L. Peterson and Mr. Bristol Foster, Royal Ontario Museum of Zoology, Toronto, Canada, provided specimens of _Phenacomys intermedius_. Dr. J. N. Layne, University of Florida, Gainsville, Florida, presented me with a baculum of _Microtus parvulus_.

I am indebted to all of these persons for their aid, and to various collectors for the Museum of Natural History, who preserved bacula with specimens. Many of these specimens were obtained through the a.s.sistance of the University of Kansas Endowment a.s.sociation and the National Science Foundation.

METHODS

Bacula were obtained from fresh specimens, specimens preserved in alcohol or formalin, and dried study skins. The processing of bacula has been discussed by Hamilton (1946), Friley (1947), White (1951), and Dearden (1958). The methods used to preserve bacula for my study differed some from any of those reported. The terminal part of each p.e.n.i.s including the baculum imbedded in the glans p.e.n.i.s was removed in its entirety and placed in a vial. The catalogue number was kept with each specimen at all times. A two per cent solution of pota.s.sium hydroxide was added. All specimens were examined at least once a day. If tissues other than the glans p.e.n.i.s were present they were removed with forceps when softened usually at the end of one day. Several drops of Alizarin red-S stain in a saturated alcoholic solution were added to the 3 to 5 ccs. of KOH solution in each vial. Solutions were replaced if they became turbid enough to obstruct observation of the clearing p.e.n.i.s. After one day the solution containing stain was removed and replaced with two per cent KOH solution without stain. When the glans became sufficiently cleared that the stained baculum could be seen easily, the solution was replaced by glycerin in which clearing was completed. The time required for the entire process varied from one day to more than two weeks depending on the size of the specimen and on its condition. Fresh specimens clear more rapidly than dried specimens, and those that are dried more rapidly than those that are preserved. A three or four per cent solution of hydroxide will hasten the process, but more frequent observation is required to prevent excessive maceration.

Specimens were then examined in a shallow dish containing glycerin under a binocular microscope. The baculum can be viewed from any desired direction. The method described above leaves the baculum intact within the glans p.e.n.i.s; therefore its orientation can be determined relative to the thick walled urethra and the thin walled dorsal artery that extends onto the dorsal side of the baculum. The ventral curvature of the p.e.n.i.s proximal to the baculum, and the distal extension, characteristic of most species, of the dorsal border of the glans (both shown in Figure 1) are other features aiding in correctly orienting cleared specimens. The digitate processes are not so often injured, lost, or displaced when the method described above is used as they are when the p.e.n.i.s is dissected.

Specimens were stored in glycerin in gla.s.s sh.e.l.l vials having polyethylene stoppers. A small card bearing the name, number, locality, and other data was placed in each vial. A specimen thus enclosed can be kept indefinitely, or removed and mounted in balsam as described by White (1951:631) or in plastic as described by Dearden (1958:541) and thus stored in the vial containing the skull of the specimen.

Drawings were made on millimeter ruled paper while the baculum was viewed under a binocular microscope with a square ruled eyepiece.

Unless otherwise noted all specimens listed are in the University of Kansas Museum of Natural History. Catalogue numbers are cited.

Measurements are accurate to within less than one-tenth of a millimeter.

Proportions as stated in the text are approximations, accurate to within one-twelfth (8.33 per cent). The range of variation is unknown for some species. Mention is made if maturity is known or suspected to differ in specimens being compared.

The development of the baculum has been studied by Callery (1951) in _Mesocricetus auratus_ and by Ruth (1934) in the laboratory rat. In the rat (_Rattus norvegicus_) the bone is of endoblastemal origin being laid down by a condensation of undifferentiated mesenchymal cells. At the distal end of the bone dense fibrous tissue is then differentiated and at the proximal end hyaline cartilage. Growth is by subst.i.tution at the proximal end and by subperiosteal lamellation circ.u.mferentially. A marrow cavity is formed by resorption. In the baculum of the hamster the primary center of ossification is in the stalk, and is present at the age of three days; the secondary centers are in lateral processes and are present at 80 days and enlarge subsequently. A tertiary center, in each median process, may or may not develop later. Maximum development of the baculum is reached late in the reproductive life of the hamster.

The early ossification of the baculum noted in the rat and the hamster occurs in _Microtus_ also. A specimen of _Microtus monta.n.u.s fusus_ (76831, from 5 mi. N, 26 mi. W Saguache, 9600 ft., Saguache County, Colorado) only 74 mm. in total length and weighing only 6.6 grams, had a slender ossified baculum having enlarged ends. This vole was one-half of the average length and less than one-fifth of the average weight of an adult, and of approximately the size at which weaning takes place.

The development of the baculum in _Microtus ochrogaster_ was studied in 32 specimens of various ages. The specimens (between Nos. 74994 and 75074) were collected between August 15 and September 4, 1957, at localities on the Great Plains. These specimens were from breeding populations, as evidenced by pregnancy of females and by large size of testes of males. The length and width of the stalk of the baculum, the presence of digital ossifications, the total length of the animal, and the size of the testes were noted. Variability in length of testes is greatest when voles are from 140 to 150 mm. in total length. s.e.xual maturity is reached rather abruptly when the total length of most individuals is 140 to 150 millimeters. If the baculum likewise underwent more rapid growth at the onset of s.e.xual maturity, greater variability should be evident in the length of the baculum of voles 140 to 150 mm. in total length than in bacula of voles of other sizes. This was the case (see Figure 1d). The baculum does not, however, suddenly reach its maximum maturity.

The primary ossification is in the stalk. The secondary ossification is in the median process except in _Lagurus_ (Dearden, 1958:551) and some individuals of _Neofiber_ (see account on page 258). Tertiary centers of ossification are in the lateral processes. The primary ossification is present at an early age and subsequently increases in size and solidity.

The secondary and tertiary ossifications are progressively more common in older voles. The increase in degree of ossification of all parts continues after s.e.xual maturity is reached. Individual variation and variation with age in the baculum of _Microtus pennsylvanicus_ have been ill.u.s.trated by Hamilton (1946:380). Figures 14, 15, and 17 ill.u.s.trate variation with size, which is correlated with age, and also ill.u.s.trate individual variation. The three bacula are from adult voles having testes that measured 15, 16 and 16 mm. in length, respectively. Each vole was trapped in late June. The total lengths in millimeters of the three voles are 172, 167, and 181; weights are 55, 52.4, and 65.5 grams. I judge that the greater size of the stalk and the better developed base shown in Figure 17 than in Figure 15 are ill.u.s.trative of age variation; the difference in the size of the lateral digitate processes is, in this case, attributable to individual variation. Differences in the distal end of the baculum in Figures 42 and 43, show individual variation also.

Figures 35 and 36 represent two different subspecies; different individuals of _M. mexica.n.u.s mogollonensis_, however, exhibit individual variation of the same degree.

Hall and c.o.c.krum (1953) list 44 species of microtines in North America.

At least twelve of these are insular or local forms perhaps derived from some other species; for example _Microtus coronarius_, an insular form derived from _Microtus longicaudus_; _Microtus provectus_, considered by Chamberlain (1954:587) and by Wheeler (1956:176) as a subspecies of _Microtus pennsylvanicus_; and _Microtus ludovicia.n.u.s_, a close relative of _Microtus ochrogaster_.

All North American genera have been studied. Of the genus _Microtus_ in North America, all subgenera but _Orthriomys_ and all species but the following nine, have been studied: _M. (Orthriomys) umbrosus_, the insular _M. (Stenocranius) abbreviatus_, _M. (Microtus) breweri_, _M.

(Microtus) nesophilus_, _M._

[Ill.u.s.tration: FIGURES 2-13. Bacula of microtines. Unless indicated otherwise views are (_a_) of the dorsum, (_b_) the right side, and (_c_) the proximal end with the dorsal surface upward. Exact localities are given in accounts of species concerned.

2. _Lemmus trimucronatus_, 50678, Point Barrow, Alaska.

3. _Dicrostonyx groenlandicus_, 50539, Porcupine Lake, Brooks Range, Alaska.

4. _Dicrostonyx groenlandicus_, 52524, Point Barrow, Alaska.

5. _Synaptomys cooperi saturatus_, WBQ 3-C-454, 3 mi. S Demotte, Indiana.

6. _Synaptomys cooperi paludis_, 13716, Meade County State Park, Kansas.

7. _Phenacomys intermedius celatus_, SA 2044, Quebec.

8. _Phenacomys intermedius intermedius_, WBQ 3-C-309, 5.4 mi. S Moran, Teton Co., Wyoming.

9. _Clethrionomys rufoca.n.u.s_, 60438, 1 mi. NW Oho-ri, Korea, (_d_) ventral view.

10. _Clethrionomys gapperi_, 42108, 31 mi. N Pinedale, Wyoming.

11. _Clethrionomys rutilus_, 42865, 5 mi. NNE Gulkana, Alaska.

12. _Clethrionomys occidentalis_, FWS 30, Mary's Peak, Benton Co., Oregon.

13. _Clethrionomys glareolus_, 67100, Zermatt, Valais, Switzerland.]

[Ill.u.s.tration: FIGURES 14-25. Bacula of _Microtus_. Unless indicated otherwise views are (_a_) of the dorsum, (_b_) the right side, and (_c_) the proximal end with dorsal surface upward.

14. _M. pennsylvanicus_, 42439, 1 mi. S, 2 mi. E Eagle Nest, Colfax Co., New Mexico; abnormality perhaps owing to injury; dorsal view.

15. _M. pennsylvanicus_, 42306, 5 mi. N, 26 mi. W Saguache, Colorado; dorsal view.

16. _M. pennsylvanicus_, 43043, 20 mi. NE Anchorage, Alaska, ventral view.

17. _M. pennsylvanicus_, 42430, 1 mi. S, 2 mi. E Eagle Nest, New Mexico.

18. _M. agrestis_, 67102, Gryon, Switzerland.

19. _M. monta.n.u.s amosus_, 62241, 1/2 mi. E Soldier Summit, Wasatch Co., Utah.

20. _M. monta.n.u.s na.n.u.s_, 57470, 2 mi. N, 2 mi. W Pocatello, Idaho.

21. _M. monta.n.u.s fusus_, 42307, 5 mi. N, 26 mi. W Saguache, Colorado.

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The Baculum In Microtine Rodents Part 1 summary

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