JOURNAL OF MORPHOLOGY 273:1199–1213 (2012


Seasonal Spermatogenic Cycle and Morphology of Germ Cells in the Viviparous Lizard Mabuya brachypoda (Squamata, Scincidae)
Arlette Herna ´ ndez-Franyutti1 and Mari Carmen Uribe2*
´ n Acade ´ mica de Ciencias Biolo ´ gicas, Universidad Jua ´ rez Auto ´ noma Laboratorio: Acuicultura Tropical, Divisio ´ xico de Tabasco, 86039 Villahermosa, Tabasco, Me 2 ´a de la Reproduccio ´ n Animal, Departamento de Biologı ´a Comparada, Facultad Laboratorio: Biologı ´ noma de Me ´ xico, 04510 Me ´ xico D.F. de Ciencias, Universidad Nacional Auto ABSTRACT We describe seasonal variations of the histology of the seminiferous tubules and efferent ducts of the tropical, viviparous skink, Mabuya brachypoda, throughout the year. The specimens were collected monthly, in Nacajuca, Tabasco state, Mexico. The results revealed strong annual variations in testicular volume, stages of the germ cells, and diameter and height of the epithelia of seminiferous tubules and efferent ducts. Recrudescence was detected from November to December, when initial mitotic activity of spermatogonia in the seminiferous tubules were observed, coinciding with the decrease of temperature, photoperiod and rainy season. From January to February, early spermatogenesis continued and early primary and secondary spermatocytes were developing within the seminiferous epithelium. From March through April, numerous spermatids in metamorphosis were observed. Spermiogenesis was completed from May through July, which coincided with an increase in temperature, photoperiod, and rainfall. Regression occurred from August through September when testicular volume and spermatogenic activity decreased. During this time, the seminiferous epithelium decreased in thickness, and germ cell recruitment ceased, only Sertoli cells and spermatogonia were present in the epithelium. Throughout testicular regression spermatocytes and spermatids disappeared and the presence of cellular debris, and scattered spermatozoa were observed in the lumen. The regressed testes presented the total suspension of spermatogenesis. During October, the seminiferous tubules contained only spermatogonia and Sertoli cells, and the size of the lumen was reduced, giving the appearance that it was occluded. In concert with testis development, the efferent ducts were packed with spermatozoa from May through August. The epididymis was devoid of spermatozoa by September. M. brachypoda exhibited a prenuptial pattern, in which spermatogenesis preceded the mating season. The seasonal cycle variations of spermatogenesis in M. brachypoda are the result of a single extended spermiation event, which is characteristic of reptilian species. J. Morphol. 273:1199–1213, 2012. Ó 2012 Wiley Periodicals, Inc. KEY WORDS: spermatogenesis; testicular efferent ducts; viviparous lizard; Mabuya cycle;

spermatogenesis, is as important as the female reproductive cycle in determining the reproductive pattern of a species (Trauth, 1979). Spermatogenesis is an essential process in the biology of reproduction and results in production of haploid spermatozoa from diploid spermatogonial cells. The study of the spermatogenesis requires the recognition and identification of germ cell morphology during their differentiation and their occurrence throughout the seasonal cycle. The differentiation of germ cells involves specific cellular events: mitosis of spermatogonia, meiosis of spermatocytes, and spermiogenesis of spermatids. This process is followed by spermiation, the release of sperm from the seminiferous epithelium (Bakst et al., 2007; Hess and de Franca, 2008). In reptilian sauropsids, as amniotic species, spermatogenesis has special evolutionary interest among vertebrates because germ cell development represents a strategy between the anamniotic clades (fishes and amphibians) and the other amniotic taxa (birds and mammals; Gribbins et al., 2003, 2007, 2008, 2009; Rheubert et al., 2009a,2009b). In the testes of birds and mammals, germ cells are sequentially situated along the seminiferous tubules in a continuous spatial development of spermatogenesis that results in waves of sperm release from specific portions of the tubules during the reproductive cycle (Leblond and Clermont, 1952; Clermont, 1972; Lin
Additional Supporting Information may be found in the online version of this article. *Correspondence to: Mari Carmen Uribe, Departamento de Biolo´a Comparada, Facultad de Ciencias. Circuito Exterior, Ciudad gı ´ noma de Me ´ xico, InsurUniversitaria, Universidad Nacional Auto ´ n Coyoaca ´ n, 04510 Me ´ xico, D.F. Me ´ xico. gentes Sur 3000, Delegacio E-mail: Received 22 January 2012; Revised 4 April 2012; Accepted 13 April 2012 Published online 13 July 2012 in Wiley Online Library ( DOI: 10.1002/jmor.20050

INTRODUCTION The identification and definition of the seasonal changes of the male reproductive cycle, e.g., the

1983. The VIII phases are characterized by: I. spermatozoa in the lumen. mitosis of spermatogonia and no lumen. 2003. 1993. There are no previous descriptions of male reproductive system of M. Vitt and Blackburn. 2009a. dehydrated in a series of graded alcohols (80%. complete regression. Mabuya brachypoda is a viviparous lizard distributed from the southeast of Mexico to Costa Rica in Central America (Webb. IV. b) the females may initiate gestation at a small body size and subsequently grow during gestation (Vitt and Blackburn. VII. 1958). The progressive changes that occurred during the spermiogenesis were divided into seven steps according to Gribbins et al. The eggs attained maximum diameters during June-July.3 mm in diameter) developed. in M.9–1. 9381’ W). In these species. 1990. Me Graph 1). 1991). In contrast.2009b).1200 ´ NDEZ-FRANYUTTI AND M. brachypoda during the annual cycle and to relate these characteristics to the long gestation period of the female reproductive cycle. were collected during 2004. The terms used for the two types of efferent ducts were ductuli efferentes and ductus epididymis as described by Sever (2010).. Guillette and Me ´n-Santa Cruz et al. M.B). from Nacajuca. 2008.. capensis by Flemming (1994). 2003. These species present remarkable reproductive patterns having several unique specializations among lizards: a) the genus Mabuya includes oviparous and viviparous species in Asia and Africa. Vitt and Blackburn. brachypoda (snout-vent length 59–78 mm. Meteorological data. Ramirez-Pinilla et al. Vitt and Blackburn. the analysis of morphological and physiological characteristics of spermatogenesis in reptiles represents a main aspect in the understanding of the evolution of male germ cell development in vertebrates. 1983). A mid ventral incision opened the abdominal cavity. bra´ndez-Franyutti chypoda were documented by Herna et al. Male reproductive activity of Mabuya species has been described as a continuous process by gross analysis of the testes (weight and volume). Uribe et al.C. Macroscopic examination of the oviducts of M. or matrotrophy (when most nutrients for the embryo are transferred from maternal tissues during gestation. 1976. 1996). VI. the tissues were washed in 70% alcohol. Me N. no mitosis of spermatogonia and reduced lumen. the goals of this study are to characterize the morphology of the germ cells during spermatogenesis and determine the changes of the seminiferous epithelia and efferent ducts in M. Guillette and ´ ndez de la Casas-Andreu. However. 1983.. 1994). 2008). and embedded in paraffin. who identified a seasonal process durJournal of Morphology ing which microlecithal eggs (0. 2000. 1982). Asia. Hess and de Franca. 1983) while other species ovulate microlecithal eggs (containing little yolk. capensis (Flemming. The morphological changes of the seminiferous epithelium during the annual cycle were divided into eight phases (I to VIII) according to the classification described by Mayhew and Wright (1970) based on the morphological changes of the seminiferous epithelium in lizards of the genus Uma.. all the species of America are viviparous (Fitch. 1987. Vitt and Blackburn. as in M. This classification focuses on the type of germ cells bordering the tubular lumen during the annual cycle. MATERIAL AND METHODS Male M. 1994. Histological changes in the seminiferous tubules of Mabuya were mentioned only in the study of M.. which is characteristic of the prenuptial pattern (Saint Girons. GribCruz. in the abdominal cavity and con- . 2005). brachypoda are ellipsoid structures (Fig. URIBE A. 1991. 2006). (2009). 1970.. e) therefore. The specimens were euthanized using ether and decapitation. 2007. Some reproductive aspects have been studied in adult females of this species. spermatids in spermiogenesis at luminal margin. 1980) and M. mabouya (Somma and Brooks. c) viviparous species have a long period of gestation (9–12 months. mean monthly maximum and minimum temperatures and pre´ xico. 1983. (2005). and Africa. reptilian spermatogenesis develops a single population of spermatozoa. Villagra bins et al. brachypoda. The ovarian cycle and oogenesis of M. Selected morphometrics such as: diameter and epithelial height of the seminiferous tubules. Digital photomicrographs were taken using an Olympus digital camera model C5050Z coupled to an Olympus CX31 microscope. which is released during a single spermiation event (Mayhew and Wright. 1970. in other species. 1994. there are different levels of lecithotrophy (when most nutrients for the embryo are provided by the yolk). brachypoda. primary spermatocytes at luminal margin. spermatogenesis was defined as a seasonal cycle. some species ovulate macrolecithal eggs (containing abundant yolk. After fixation. 1958. ductuli efferentes. were obtained from the Comision cipitation in Tabasco. heathi (Vitt and Blackburn. undifferentiated spermatids at luminal margin. Species of the genus Mabuya are tropical grass skinks that are distributed in regions of America. and ductus epididymis were measured (N 5 25 per specimen) using a Carl Zeiss Axion Vision Imaging System. 1983. Flemming.. 1983). V. The microlecithal eggs are considered the smallest described thus far in reptiles. Me ´ xico (2004) (Supporting Information Nacional del Agua. and efferent ducts were removed and fixed in alcoholic Bouin’s (8–15 h). the peak of spermatogenesis occurred during spring and early summer. 2009. Histological analysis of the uterus of M. RESULTS The testes of M. VIII. 2005. Maximum and minimum testicular diameters were measured. Hernandez-Franyutti et al. Franca and Godinho. Tabasco. Vitt and Blackburn. early regression with cellular debris in the lumen. 1991. 1991). Tissues were serially sectioned at 6 lm in longitudinal planes and stained with hematoxylin-eosin (Aguilar-Morales et al. 96% and 100%). Testes. HERNA and Jones. 3 ´ xico (18810’ specimens per month). (2006). Rheubert et al. showed the presence of embryos between August and May. but he did not present histological images. 2002). Ferreira et al. II. cleared in xylene. secondary spermatocytes at luminal margin. striata (Simbotwe. III.. Testicular volume was subsequently calculated using the equation for the volume of an ellipsoid (V 5 4/3p (1/2L) (1/2W)2). showed embryos in the uterus. 1A. brachypoda during the annual cycle by Uribe et al. collected between late June to late July by Webb (1958). d) the ovaries develop different types of eggs. Webb. Blackburn. 2009. Consequently. Therefore. N 5 36.

adjacent to the lumen of the seminiferous tubules. brachypoda present annual variations in testicular volume. lumen (*). Testes and epididymis of Mabuya brachypoda during different periods of spermatogenesis. and ductus epididymis (see supporting Information. Table 1). D: 100lm.B). nected to the dorsal wall of the body by the mesorchium. D. 1A. seminiferous epithelium (sep). C. diameter and epithelial height of the seminiferous tubules and diameter and epithelial height of the ductuli efferentes. Adjacent to the testis is the epididymis as a convoluted duct (Fig.SPERMATOGENESIS OF VIVIPAROUS LIZARD Mabuya brachypoda 1201 Fig. The testes of M. Bars 5 A. B: 500lm. Testes and epididymis during phase II of the seminiferous epithelium cycle. The seminiferous epithelium during phase II contains few germinal cells and there are no spermatozoa in the lumen of the seminiferous tubules. The seminiferous tubules of the testes are reduced. Testes and epididymis during phase VI of the seminiferous epithelium cycle. C. Epididymis (E). brachypoda is highly seasonal. which connects to the ductus deferens. B. The phases of the spermatogenic cycle in the testis. 1. A. The reproductive cycle of M. The ductus of the epididymis does not contain spermatozoa. The ductus epididymis encloses abundant spermatozoa. The distal segment is the ductus epididymis. 1A. testes (T). The seminiferous tubules are larger compared to those seen in phase II in the Fig. The seminiferous epithelium during phase VI contains abundant germinal cells and there are late spermatids at the apical end. late spermatids (1St). spermatozoa (Sz). The proximal segment of the epididymis is closest to the testis and is formed by the ductuli efferentes. and the presence of spermatoJournal of Morphology . The efferent ducts consisted of two segments.

The seminiferous epithelium is limited by a basement membrane (Fig. fibroblasts.2 lm average diameter. 2B–E) are located at the base of the seminiferous epithelium. the average cell diameter increases to 23. as well as the diameter and epithelial height of the efferent ducts. are ovoid in shape. After the second meiotic division. The testes contain the seminiferous tubules lined by seminiferous epithelia. Sertoli cells form a permanent epithelium and are distributed around the circumference of the seminiferous tubules (Fig. 2A) that separates the germinal compartment inside the seminiferous tubules. myo-epithelial cells.C) but they were maximal between May and July. There are two types of spermatogonia: spermatogonia A (Fig. densely stained threads. The paired and dense chromosomes become gradually separated but remain united in several sites. are frequently triangular in shape with one or two nucleoli. the chromosomes become more filamentous as the homologous chromosomes pair form.9 lm) compared to the primary spermatocytes. the average cell diameter is smaller than that of the spermatogonia. Next. and telophase I. chromatin condensation. 2J). The morphological changes of the spermatid included formation of the acrosomal system. 2L) are the result of the first meiotic division. during late spermatogenesis (Fig. with an average diameter of 14. Spermatids (Fig. 1B. Secondary spermatocytes are spherical in shape and smaller in average diameter (18. Between November and February. formed by vascularized connective tissue with abundant collagenous fibers. Primary spermatocytes (Fig. The chromatin initiates condensation and the chromosomes appear as thin. c) During the pachytene stage (Fig. diameter and the height of epithelium of the seminiferous tubules. 2B).D. continue through anaphase I (Fig. the spermatocytes have an average diameter of 25. 2F). compared to secondary spermatocytes. The ducts of the epididymis do not contain spermatozoa. Spermatogonia (Fig. they attained an average diameter of 26. bordering the basement membrane. These cells were the rarest of primary spermatocytes. Spermatogonia A have an average diameter of 21lm. and complete cytokinesis to produce the secondary spermatocytes. 2F–K) are spherical cells with a round nucleus. Table 1. Their nucleus and cytoplasm are similar to those seen in the spermatogonia A. 2C–E). Spermatids. Morphology of Germ Cells During the Spermatogenesis Spermatogonia.8 lm. HERNA zoa in the ductus epididymis defined the seasonal changes (Fig.3 lm and are more spherical than the spermatogonia A. supporting Information). and their nuclei are spherical and contain fine granular heterochromatin with one or two dense and round nucleoli. URIBE A. 1C).8 lm. Journal of Morphology have an average diameter of 23. 2M–S).C. The nucleus is spherical and the chromatin consists of fine filaments. and spermatogonia B (Fig. and the ductus epididymis contain abundant spermatozoa.1202 ´ NDEZ-FRANYUTTI AND M. 2A). These spermatocytes were the most abundant among the primary spermatocytes. During the annual cycle they proliferate by mitosis. The spermatogonia B are slightly larger. the spermatocytes are at the maximum diameter for primary spermatocytes.2 lm and condensation of the chromosomes advances. The primary spermatocytes divide forming the spindle and the chromosomes arranged into metaphase I (Fig. 2I). The nucleus undergoes morphological changes during the progression of meiosis I. d) During the diplotene stage (Fig. These epithelia consist of Sertoli cells and germ cells. irregularly distributed all along the chromosomes. The spermatids go through metamorphosis during spermiogenesis. collagen fibers. in early spermatogenesis were minimal (Fig. 2K). 1C.. b) During zygotene (Fig.D). 2M). elongation of the nucleus and . In late spermatogenesis. Secondary spermatocytes (Fig. the seminiferous epithelium of the testicular tubules contains few germinal cells and there are no spermatozoa in the lumina of the seminiferous tubules (Fig. indicating the continuation of meiosis. The interstitial compartment is formed by connective tissue composed of Leydig cells. The paired chromosomes are even thicker and shorter than those seen in zygotene and maintain their intense stained affinity. 1A. several steps of meiotic prophase I were seen: a) during the leptotene stage (Fig. 2H). in their early stages (Fig. the size of the testis. In early spermatogenesis. the seminiferous epithelia of the testicular tubules contain abundant germinal cells and there are spermatids at the apical end. Secondary spermatocytes. Primary spermatocytes. During mitosis the fibers of the spindle were easily observed (Fig. adjacent to the lumen of the seminiferous tubules (Fig. from the interstitial compartment outside the seminiferous tubules. producing a large population of spermatogonia or initiating meiosis and becoming primary spermatocytes. are spherical cells and smaller.e. According to the morphology of the chromosomes. 2E). nerve fibers and lymphatic and blood vessels. i. Sertoli cells have a basal nucleus. its volume.6 lm. Testicular Components The wall of the testis is surrounded externally by the tunica albuginea. the secondary spermatocytes form step 1 spermatids. 1D). 2G). Since secondary spermatocytes are rarely observed it is assumed that rapidly enter the second division of meiosis. attaining a 20. forming chiasmata.

T. 2P). Spermatids in step 5 of spermiogenesis. Spermatid in step 2 of spermiogenesis. Primary spermatocyte in anaphase I of meiosis. the spermatid contained a spherical nucleus with haploid and fine granular chromatin. R. Sertoli cell nuclei (Se). step 1 (1St). Spermatogonium B round in shape and has two dense nucleoli. During the first step (Fig. 2O). O. D. Spermatogonium B during metaphase and a Sertoli cell nucleus. step 6 (6St). Primary spermatocyte in metaphase I (MSc). H. L. Spermatid in step 1 of spermiogenesis. step 7 (7St).SPERMATOGENESIS OF VIVIPAROUS LIZARD Mabuya brachypoda 1203 Fig. Bars 5 5lm. and three (Figs. 2. 2M). C. step 4 (4St). Zygotene spermatocyte (ZSc). Spermatid in step 3 of spermiogenesis. spermatogonium B (SgB). Secondary spermatocytes. step 3 (3St). Pachytene spermatocyte. Spermatids in step 6 of spermiogenesis. steps four (Fig. Primary spermatocyte in metaphase I of meiosis. Spermatozoa (Sz). E. Secondary spermatocytes (SSc). Q. 2N). 2Q). step 5 (5St). spermatids are characterized by elongaJournal of Morphology . and six (Fig. Spermatids in step 7 of spermiogenesis. Spermatid in spermiogenesis. N. M. Spermatids are characterized by the formation of the acrosomal system and the start of chromatin condensation. Diplotene spermatocyte. Sertoli cell nuclei and germ cells during different stages of spermatogenesis in the seminiferous tubules of Mabuya brachypoda. B. (2009). I. K. 2R). Sertoli cell nuclei in the base of a seminiferous tubule. These changes occur gradually through seven steps according to Gribbins et al. five (Fig. Spermatozoa in the lumen of the seminiferous tubule. A. Spermatogonium A is ovoidal in shape. Spermatids in step 4 of spermiogenesis. Zygotene spermatocyte. F. formation of the flagellum. P. steps two (Fig. Spermatogonium B is round in shape. spermatogonium A (SgA). Leptotene spermatocyte. Leptotene spermatocyte (LSc). Pachytene spermatocyte (PSc). G. J. S. step 2 (2St). Primary spermatocyte in anaphase I (ASc). Diplotene spermatocyte (DSc).

Near . Spermatogenesis was completed during this phase.6 6 9. The germinal epithelium formed large columns in which spermatids were located along the lumen.C. Primary spermatocytes in pachytene of prophase I of meiosis were the most abundant type of germ cells identified in this phase. Spermatozoa.9 lm. recrudescence of spermatogenesis was detected undergoing spermatogonia in mitosis (Fig. The lumen of the tubules was mostly occluded. 3A). Meanwhile.4 6 1.B). is characterized by easy visualization of the flagellum protruding into the lumen which suggests the germ cell is near to be released into the lumen.0 lm. Phase VI. 7D). The testes were in this phase during November and December (Fig. The diameter of the seminiferous tubules was 107. Spermatogenesis was synchronous in all the seminiferous tubules. 6A–D). the number of germ cells in the seminiferous epithelium appeared to increase.C). Phase V.2 lm.3 6 1. Occasionally.4 lm. Most of the spermatids showed the initial morphological changes that occur during spermiogenesis. 3A.7 6 1.6 6 17.0 lm. spermatogonia and Sertoli cells.7 lm. including acrosomal development and the initial elongation of the nucleus.4 mm3 (Fig. and some scattered spermatozoa were seen in the lumen of the seminiferous tubules.8 lm. 7A. slightly larger than those seen in the previous stages. the seminiferous epithelium decreased in thickness to 89. 2T).9 6 8.5 mm3 (Fig.5 6 Journal of Morphology 2.5 mm3 (Fig. brachypoda (Fig.6 lm. As a consequence of the mitotic activity of spermatogonia.6 6 2.1 mm3(Fig.2 6 7. The seminiferous epithelium contained. The testes were in phase IV during April at which time the volume of the testes was 47. The seminiferous tubules attained the minimum diameter (77. 3D). they are released into the lumen as spermatozoa. The testes were in phase II during January and February at which time the volume of the testes was 8.6 lm.2 6 4. The diameter of the seminiferous tubules was 271. 5A–D).8 6 2. Phase III. most of spermatocytes and spermatids disappeared. and the flagellum is long and thin. The diameter of the seminiferous tubules attained 306. exclusively. Phase VII.7 lm.6 6 5. During late regression (Fig.2 mm3.1204 ´ NDEZ-FRANYUTTI AND M. meanwhile. 6C.9 6 3.6 6 12.0 mm3 (Fig. similar to that seen in the height of the seminiferous epithelia 122. Phase IV. The lumen is occluded in most of tubules.5 6 16. The diameter of seminiferous tubules was 61. Spermatogonia continued proliferating entering into meiosis and formed abundant primary spermatocytes that were located at the margin of the lumen. Primary spermatocytes were numerous. 3C). 2S). Phase VIII. and the seminiferous epithelium height was 31. Once spermatids complete spermiogenesis (Fig.3 6 1.B). The seminiferous tubules attained their maximum diameter (356. Efferent Ducts The efferent ducts of M. The testes were in phase VI during June and July at which time the volume of the testes was 89.9 6 3. The diameter of the tubules increased to 182. as evidence of early spermiogenesis. At this phase. and the height of the seminiferous epithelium was 94. The testes were in phase V during May at which time the volume of the testes was 75. spermatids were also located at the margin of the tubular lumen.8 lm). 8A–C) are ductuli efferentes and ductus epididymis. 7A. 4A–D). and step seven (Fig. HERNA tion of the nucleus.7 6 6. 7C). The spermatids advanced into late spermiogenesis presenting further elongation of the spermatid nucleus.4 lm. During early regression (Fig. Phase II. and only a few of them had a visible small lumen (Fig. The seminiferous epithelium heights also increased to 61. there were smaller regions with only three or four germ cell layers. Phase I.2 6 10. as the height of the seminiferous epithelium (11.1 6 5. only remaining spermatogonia and Sertoli cells in the seminiferous epithelium.9 lm.6 6 1. Abundant cellular debris. The testes were in phase VII during August at which time the volume of the testes was 52.4 lm). and some spermatids in spermiogenesis. secondary spermatocytes were occasionally seen at the apical end of the seminiferous epithelium. The diameter of the seminiferous tubules was reduced to 312. Annual Changes During the Seminiferous Epithelium Cycle The presence/absence of specific germ cells altered the morphology of the seminiferous epithelium during the annual cycle of Mabuya brachypoda through eight phases (I-VIII). No mitotic activity of the spermatogonia was seen.7 6 5. 3B). The number of primary spermatocytes decreased.D).2 6 5.0 mm3 (Fig. The majority of the seminiferous tubules contained only spermatogonia and Sertoli cells. The testes were in phase VIII during September and October at which time the volume of the testes was 20. URIBE A. the spermatids were very abundant.4 lm). The seminiferous epithelium height was 28. The volume of the testes was 8. but.The seminiferous epithelium contained several layers of spermatids situated along the margin of the lumen. Mature spermatozoa are transported to the efferent ducts. containing spermatogonia. The height of the seminiferous epithelium attained 112. Spermatozoa are elongated.4 lm.7 6 1.5 mm3 (Fig. The testes were in phase III during March at which time the volume of the testes was 12. Numerous spermatids lined the margins of the seminiferous epithelium and spermatozoa were free within the lumen of the tubules (Fig.

8D) that we need to verify their presence at the electron microscope level.9 lm from June through July. Their epithelial height varied from 8. D. spermatogonia A (SgA) spermatogonia B (SgB). Only during the stage VII. The lumen is very small or it is occluded. These ducts had a similar size throughout the reproductive cycle (Table 1. 3. Their minimal and maximal diameters were 17. Spermatogonia in metaphase of mitosis are seen. where the fibers of the spindle are evident.4 lm from January through February. The seminiferous epithelium during phase I contains only Sertoli cells and spermatogonia. Primary spermatocytes are abundant at the center of the tubules. Secondary spermatocytes are seen at the luminal margin of the seminiferous epithelium. 8A–D) were the smallest efferent ducts. primary spermatocytes (1Sc). the ductuli efferentes contained a few spermatozoa. B. at the end of the spermiation and during the early regression of the reproductive cycle in the seminiferous tubules. They were lined by cuboidal epithelium that had large stereocilia bordering the lumen (Fig. and 24. spermatogonia in metaphase of mitosis (arrowheads). Seminiferous tubules during phase II of the cycle show spermatogonia A and B at the base of the seminiferous epithelium. the efferent duct is observed the sexual segment of the kidney.1 6 2.5 6 3. The ductuli efferentes (Fig.5 6 3 lm respectively. The lumen is lightly larger than in the previous phase. Bars 5 12lm. Sertoli cells (Se). seminiferous tubules during phases I.6 6 2. C. Lumen (*). supporting Information). Mabuya brachypoda. Journal of Morphology .SPERMATOGENESIS OF VIVIPAROUS LIZARD Mabuya brachypoda 1205 Fig. Seminiferous tubules during phase III of the cycle. The lumen is clearly larger than in the previous phase. A. II and III of the cycle.1 lm to 10.

and was larger than the ductuli efferentes. during the phases V to VII when masses of spermatozoa were in the lumen. Spermatids before metamorphosis at the luminal margin of the seminiferous epithelium. B. The diameter of the ductus epididymis and the height of the epithelial cells changed during the reproductive cycle.1206 ´ NDEZ-FRANYUTTI AND M. Spermatids (St). From . seminiferous tubules during phase IV of the cycle. Mabuya brachypoda. HERNA Fig. C. D.1 lm in January-February. spermatids in early metamorphosis (eSt). lumen (*). maximum lumen was 226.E) was distal to the ductuli efferentes.2 lm from JanuaryFebruary to 33.0 6 3. C: 30lm. The ductus epididymis (Fig. URIBE A. A. B: 10lm. Abundant spermatids during early metamorphosis are seen at the luminal margin of the seminiferous epithelium. 4. The lumen is seen. Bars 5 A: 20lm. and it hypertrophies during June-July. The ductus epididymis was lined by columnar epithelium (Fig. 8E). The height of the epithelium varied from 9.1 6 1. Some of them present early metamorphosis. Minimum lumen size was measured as 67. 8A–C. D: 20lm.2 Journal of Morphology lm between June through August.3 6 15.0 lm during June-July.C.8 6 8.

A–D. C: 20lm. 8E). B: 10lm. DISCUSSION The results of our study are in agreement with earlier studies of reptilian sauropsids by Trauth (1979). columns (co). Mabuya brachypoda males exhibit a strong seasonal cycle of spermatogenesis. Spermatogenic recrudescence was detected from November to Journal of Morphology . May through August. the cytoplasm of the epithelial cells contained abundant secretory granules (Fig. seminiferous tubules during phase V of the cycle.SPERMATOGENESIS OF VIVIPAROUS LIZARD Mabuya brachypoda 1207 Fig. Mabuya brachypoda. Spermatids in middle metamorphosis (mSt) and late metamorphosis (lSt). D: 10lm. 5. Spermatids during middle metamorphosis and late metamorphosis are seen at the luminal margin of the seminiferous epithelium. The seminiferous epithelium presents columns extended to the lumen. lumen (*). Bars 5 A: 40lm. Histological analysis of Mabuya brachypoda shows the precise time and duration of reproductive activity and reflects upon the environmental factors that may affect the cyclical changes of the reproductive system.

C. Abundant spermatozoa during spermiation are observed in the lumen of the seminiferous tubules. when mitotic activity of spermatogonia and development of a central lumina in the seminiferous tubules were observed.1208 ´ NDEZ-FRANYUTTI AND M. lumen (*). primary and secondary spermatocytes developed. Mabuya brachypoda. photoperiod and rainy season occurred.C. B. From March through April. During these months. Bars 5 10lm. D. Late spermatids (lSt). The seminiferous epithelium presents columns extended to the lumen. URIBE A. Late spermatids are seen at the luminal margin of the seminiferous epithelium. From January to February. and the beginning of the rainy season. HERNA Fig. when the increases in temperature. seminiferous tubules during phase VI of the cycle. spermatozoa (Sz). the seminiferous tubules contained abundant spermatozoa. photoperiod. coinciding with the decrease of temperature. 6. numerous Journal of Morphology spermatids in various stages of spermiogenesis were apparent in the apical layers of the seminiferous tubules. December. and the maxi- . A. Spermiogenesis was completed from June through July.

C. lumen (*). Bar 5 12lm. mal testicular volume was detected. During middle regression. B: Bar 5 10lm. reduction of the seminiferous epithelium (thick arrows). Spermatogonia. Sertoli cells (Se). the seminiferous tubules contained only a few spermatocytes. in phase VII of the cycle. A: Bar 5 20lm. spermatozoa (Sz). seminiferous tubules during phases VII and VIII of the cycle. few spermatozoa (arrow head). having only three or four cell layers composed of spermatogonia. During complete regression. only spermatogonia and Sertoli cells are seen in the seminiferous epithelium. D. in phase VII of the cycle. During early regression. Seminiferous tubules of Mabuya brachypoda in late regression. occasionally some spermatocytes and some remaining spermatids and spermatozoa. spermatogonia (Sg). the seminiferous epithelium is reduced to spermatogonia and Sertoli cells and abundant cellular debris (cd) in the lumen of the tubule are seen. Testicular regression occurred from August through September when testicular volume and spermatogenic activity decreased.SPERMATOGENESIS OF VIVIPAROUS LIZARD Mabuya brachypoda 1209 Fig. Bar 5 12lm. ProgresJournal of Morphology . B. A. the reduction of the seminiferous epithelium is evident. spermatids and spermatozoa are seen. The lumen is very small or it is occluded. in phase VIII of the cycle. Few spermatozoa are seen in the lumen of the seminiferous tubule. the spermatids in metamorphosis had diminished and the seminiferous epithelium decreased in thickness. 7. Mabuya brachypoda. Cellular debris (cd). spermatids (St).

during late spermatogenesis in phase VI of the seminiferous epithelium cycle. sexual segment of the kidney (SK). Bars 5 A: 500lm. Detail of Fig. abundant cellular debris. Epididymis of Mabuya brachypoda.C. D. Epididymis. stroma (S). The stroma surrounds the ductuli efferentes. 8C. The ductuli efferentes of the efferent ducts have not spermatozoa. 8. The testis is observed near the epididymis. testis and sexual segment of the kidney. B. D: 10lm. The ductus epididymis has a large columnar epithelium and contains abundant spermatozoa. The ductuli efferentes have not spermatozoa. The stroma (S) surrounds the ductus epididymis. C. epididymis (E).1210 ´ NDEZ-FRANYUTTI AND M. During October. E: 20lm. testis (T). and the ductus epididymis contains abundant spermatozoa. The ductuli efferentes have a cuboidal epithelium with large stereocilia in the apical end. in phase II of the seminiferous epithelium cycle. 8C. C: 500lm. B: 100lm. with the advance of the regression. and some scattered spermatozoa were seen Journal of Morphology in the lumen of the seminiferous tubules. stereocilia (arrowhead). HERNA Fig. Epididymis and sexual segment of the kidney. ductus epididymis (Dep). A. the seminiferous tubules contained only spermatogonia and Sertoli . URIBE A. E. the spermatocytes and spermatids disappeared and the presence of hyaline material. spermatozoa (Sz). Stroma of connective tissue surrounds the efferent ducts. sively. during early spermatogenesis. The regressed testes defined the total suspension of spermatogenesis. Ductuli efferentes (dep). Detail of Fig.

corresponding to a prenuptial pattern. 2006. brachypoda indicates synchrony in the reproductive cycles of both sexes. and the lumen became completely occluded. both events. the germ cells commence meiosis while moving into the seminiferous epithelium from the base to the lumen and are subsequently released into the lumen at spermiation. When spermiation occurs. 1970. de la Cruz et al. Later. in temperate species. 2009). 2005. 2008). from where they travel to the deferent ducts. 1984. Leblond and Clermont (1952) recognized in the rat the cellular associations that occur along the seminiferous epithelium during the spermatogenic phases. 1988. Hess and Franca. 2010). the testes of M. and amphibians (Uribe et al. In contrast.. 1987). spermatogenesis in some tropical species has been described both as a continuous (Licht. Unlike reptilian sauropsids.. Rheubert et al. the cysts open and release spermatozoa into the tubules or lobules. 1990. as M. Ramı Ferreira et al. Gribbins et al.. 2010).. spermatogenesis and mating are temporally separated. occurring at different times of the year. and Seminatrix pygaea (Gribbins. 1987. 2009. Opheodrys aestivus (Aldridge et al. during the annual reproductive cycle.. 2011). is reminiscent to that described in anamniotic taxa (fishes and amphibians).SPERMATOGENESIS OF VIVIPAROUS LIZARD Mabuya brachypoda 1211 cells. and M. Gribbins et al. Gribbins et al.. as it was described by Saint-Girons (1982) and Licht (1984). 2007. During spermatogenesis. Uribe. 1987). coincides with that of ´ ndezseveral species of reptiles. Separate hormonal patterns may exist. Ferreira 1984. 2009). In the postnuptial pattern. throughout the year. germ cells undergo the events of mitosis. 1987). brachypoda evidences that the males reached the maximum level of spermatogenic activity. and this is known as ‘‘dissociated pattern’’ of reproduction (Whittier and Crews.2009b). 2009). indicated the sea- sonality of the testicular cycle. there is a synchronous development of a single population of germ cells during spermatogenesis followed by a single spermiation event. 2011) compared the spermatogenesis in several reptilian sauropsids considering that the spermatogenic strategy in reptiles. females were in early vitellogenesis during May through July. The synchrony of gametogenic cycles of males and females was seen in other species of the genus Mabuya. 1983). 2010). a similar pattern to that described in temperate species. capensis (Flemming.. The seasonal morphological changes of the testis in M.. According to this report. Villagra 1994. heathi (Vitt and Blackburn. ´ndez-Gallegos et al. usually have a prenuptial pattern of reproduction.. birds and mammals). and the germ cells are not within spermatocysts.. Gribbins. 2003. in contrast. 1994. Aldridge et al.. brachypoda... Gribbins. Gribbins (2010. Cruz et al. 2009). if seasonal it was triggered either by the rainy season or the photoperiod (Fitch. in a chronological uniformity. 2008.. brachypoda.. brachypoda coincided with those reported for ovarian seasonality of this species (HernandezFranyutti et al. spermatogenesis and mating. Similar reptilian spermatogenic seasonality was documented primarily. in all amniotic taxa (sauropsids. The testis of fishes (Grier and Uribe. wherein all of the seminiferous tubules have similar stages of spermatogenesis. 2009). in birds and mammals there is a successive order of spermatogenic phases along the seminiferous epithelium which occurs in a wave of cyclic cell division and sperm development (Lin and Jones. 2008)... 1990). as the spermatozoa are produced after the completion of the mating season and stored in the male ducts until the following mating season. 2009. Meanwhile. The concurrence of gametogenesis between males and females of M. During the reproductive season. called the ‘‘associated pattern’’ (Whittier and Crews. seminiferous epithelium formed by Sertoli cells and germ cells. 1994). Hess and Franca. are initiated by the same hormonal condition. and ovulation occurred during July through August. and it was indicated that spermiation occurred during the warmer months of the year (Licht. 2010. Ogielska and Bartmanska. The germ cells are in different stages of spermatogenesis (Leblond and Clermont. alligators (Gribbins et al. releasing sperm in a single event. a turtle (Gribbins et al. The cysts are formed when spermatogonia are enclosed by Sertoli cells. Other lizards were documented as having prenuptial spermatogenesis. 2002. 1987) and M. 1984. In all of these species. 1994). such as lizards (Me ´n-Santa Cruz et al. capensis (Flemming. which have synchronous spermatogenesis along the lengths of tubules. have a postnuptial pattern. Spermatogenic activity in M. brachypoda have Sertoli cells and spermatogonia as a permanent seminiferous epithelium. meiosis and spermiogenesis as a single cohort. The observation of the VIII phases of the annual spermatogenic cycle in the seminiferous epithelium of M. before mating. the seminiferous epithelium contains Sertoli cells associated with layers of germ cells. 1994. In the prenuptial pattern. Lizards. Villagra ´rez-Bautista et al. including Barisia imbricata (Guillette and Casas-Andreu. Ochotorena et al. The histological analysis of testes and epididymis of M. 1990.. Licht. Gribbins. or as seasonal. the testes contain seminiferous tubules that are lined by permanent. contains tubules or lobules where the germinal cells develop in a cyst or spermatocyst. in both birds and mammals. Herna et al. multiples species of snakes as Thamnophis sirtalis parietalis (Krohmer et al. 1952.. based in the classification used by Mayhew and Wright (1970). 2009a.. Within the cysts. 2005). 2006) and a snake (Gribbins et al. the seminiferous epitheJournal of Morphology . ´ n-Santa Guillette and Casas-Andreu. As described in several species of reptilian sauropsids by Gribbins (2010.

The sexual segment of the kidney is a distal portion of the nephron of squamates. Morphological and histochemical characterization of the seminiferous epithelial and Leydig cells of the turkey. Mabuya capensis (Sauria: Scincidae) from South Africa. Biol Reprod 68:1554–1561. Anim Reprod Sci 97:303– 313. Journal of Morphology ACKNOWLEDGMENTS The authors thank Marcela E. and there is a single spermiation event. Mills EM. reptiles represent a dynamic of spermatogenesis between the anamniotes fishes and amphibians. 1982). 2007. hamster. coinciding with our observations in M. . 2010. Mesure et al. ‘‘Las Manual general de te Prensas de Ciencias’’ Facultad de Ciencias. and the amniotes birds and mammals.F. Scincidae). and spermatogenesis involves the activities of germ cells within and between successive generations to produce cellular associations of the seminiferous epithelium. Nacional Auto Aldridge RD. Me ´ xico.. such as mouse. the functions of these ducts include reabsorption of luminal fluid and active secretion.C. Sever. TX. Cytological evaluation of spermatogenesis in the Redeared Slider. 1993). Franca LR. pp 319–412. which are essentially similar to those described in mammals. Rheubert et al. Sauria. J Herpetol 28:334–341. provide essential aspects for the understanding of the evolution of male reproduction in vertebrates. URIBE A. Me ´ xico. and daily sperm production in domestic cats (Felis catus).F. Ultrastructural examination of spermiogenesis within the testis of the ground skink. Herpetol Monogr 14:371–377. In: Herna ´ ndez de la Cruz F. Testis morphometry. Me ´ xico. Gribbins KM. Blackburn DG. Me ´ ndez Sa ´ nchez JF. 2004. Ferreira et al. and Jose ´ ndez Go ´ mez for the excellent digital preparation na of histological figures and Edgar Abraham Lozano ˜ ndez Vidal for the asMendoza and Ulises HernA sistance in the preparation of the Supporting Information Graph. and in birds as the Japanese quail (Lin and Jones. ´ n Nacional del Agua. New Life Publications. Cytological evaluation of the germ cell development strategy within the testis of the American Alligator. 1987). 2005. 2010). Kinetics of spermatogenesis in mammals: Seminiferous epithelium cycle and spermatogonial renewal. Salinas-Rosales P. Bakst MR. Brillard JP. Viviparous Fishes. Ferreira et al. In: Cheng Y. Gobierno de Me ´ xico. Reptilian Spermatogenesis. Jones and Lin. 1991. seminiferous epithelium cycle length. including the cell types and the dynamics of the seminiferous epithelium cycle and features of the duct system in reptiles. in the ductus epididymis. Aguilar-Morales M. 1987. ram. Several studies described annual changes in the epididymis of reptilian sauropsids (Mayhew and Wright. Temperate Reptilian Spermatogenesis: A ´ nNew Amniotic Mode of Germ Cell Development. Gist DH. (1991). spermatogenesis. Mesure et al. in particular. Gribbins KM. As a consequence. 1972. 2003. In: Uribe MC and Grier HJ. Seasonal changes in testicular and epididymal histology of the tropical lizard. Histologie compare de l’epididyme et de ses secretions chez les reptiles (lezards et serpents). A Histological and Ultrastructural Perspective. Homestead. the functional strategy for germ cell development in reptilian sauropsids is synchronized within the seminiferous epithelium along the lengths of the tubules. 2002. Reproductive cycles of lizards and snakes.1212 ´ NDEZ-FRANYUTTI AND M. Godinho CL. D. Acta ZoolStockholm 87:59–69. domestic cat (Franca and Godinho. 2003). lucio Gribbins KM. 1990. Amphibia-Reptilia 11:165–172. 1994. editors. 1972). Dolder H. Greenhow J. (2009) and Sever (2010) consider the importance of analyzing the morphological changes of the epididymis and its secretions in the interpretation of its role in the maturation of the spermatozoa.. Flemming AF. Physiol Rev 52:198–236. 1970.. Blackburn DG. HERNA lium cycle was studied in several species of mammals. 2005). Classification of the reproductive patterns of amniotes. Ravet et al. Gribbins KM. 1996. Aguilar-Morales ´ n for help in histological ´a-Alarco and Adriana Garcı processing. 2010.. Akuffo V. guinea pig. 2003. Sever and Hopkins. dez Gallegos O. Congdon J. Coutin ´ cnicas histolo ´ gicas y citoquı ´micas. Fitch HS. Scincella laterale (Squamata. Gribbins KM. Rheubert et al. and suggested that the function of the glycoproteins in the epididymal secretions perhaps produce an environment for sperm storage and/or maturation. 2009. 1970. pp 250–269.. Gist DH. Dufaure and Saint-Girons. 2007. monkey (Clermont. and is observed near the testis and epididymis. 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