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From the * Laboratory of Cellular Biology,
Department of Morphology, Institute of Biological Sciences, Federal University
of Minas Gerais, Belo Horizonte, Brazil; and the
Laboratory of Animal Reproduction, Biological
Sciences Centre, Federal University of Pará, Belém,
Brazil.
| Correspondence to: Dr Luiz Renato de França, Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil 31270-901 (e-mail: lrfranca{at}icb.ufmg.br). |
| Received for publication May 29, 2009; accepted for publication September 10, 2009. |
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Abstract |
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Key words: Testis, spermatogenesis, stereology, spermatogenic efficiency
Knowledge of male reproductive biology and physiology—especially aspects related to spermatogenesis—is fundamental to preventing species from extinction as well as improving species management and enhancing male reproductive capacity in natural and artificial breeding programs (Comizzoli et al, 2000). Although testis structure and organization are very similar in mammals, each species may exhibit particular morpho-functional characteristics, such as those related to phylogenetic aspects and reproductive strategy/behavior (Kerr et al, 2006; Setchell and Breed, 2006).
The total duration of spermatogenesis takes approximately 4.5 cycles and lasts from 30 to 75 days in mammals (França and Russell, 1998; Leal and França, 2006; Hess and França, 2007). Cycle length is generally considered constant for a given species (Clermont, 1972) and is under the control of germ cell genotype (França et al, 1998). Knowledge of spermatogenic cycle length is fundamental for determining spermatogenic efficiency (daily sperm production [DSP] per gram of testis), which is useful for comparisons among species (Hess and França, 2007; Amann, 1962; França et al, 2005; Costa et al, 2008).
There are few reports in the literature concerning the male reproductive biology of the collared peccary. Thus, the main objectives of the present study were to perform a detailed, comprehensive biometrical, histological, and stereological analysis of the testis as well as to estimate spermatogenic cycle length, spermatogenic efficiency, and Sertoli cell efficiency in sexually mature collared peccaries.
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Materials and Methods |
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After orchiectomy, testes were separated from the epididymis and weighed, then cut longitudinally by hand with a razor blade into small fragments. Subsequently, these fragments, taken from different regions of the testis and avoiding areas nearby the mediastinum, were fixed by immersion in 4% to 5% buffered glutaraldehyde for 12 hours. Tissue samples measuring 2 to 3 mm in thickness were routinely processed and embedded in plastic (glycol methacrylate) for histological and stereological analyses.
Thymidine Injections and Tissue Preparation
In order to estimate the duration of spermatogenesis, intratesticular
injections (75 µCi/testis) of tritiated thymidine (thymidine (methyl-3H),
specific activity 82.0 Ci/mmol, Amersham Life Science, Little Chalfont,
Buckinghamshire, England)—a specific marker of cells that are
synthesizing DNA at the moment of injection—were performed prior to
orchiectomy at 3 sites (25 µCi/site) near the epididymal cauda, using a
sterile hypodermic needle. Two time intervals following thymidine injections
were considered (1 hour and 21 days). Tissue samples measuring 2 to 3 mm in
thickness were collected near the site of thymidine injections and were
routinely fixed and embedded as described above.
For the autoradiographic analysis, unstained testis sections (4 µm) were dipped in autoradiographic emulsion (Kodak NTB-2, Eastman Kodak Company, Rochester, New York) at 43°C to 45°C. After drying for approximately 1 hour at 25°C, the testis sections were placed in sealed black boxes and stored in a refrigerator at 4°C for approximately 4 weeks. Subsequently, these testis sections were developed in Kodak D-19 (Eastman Kodak) at 15°C (Bundy, 1995) solution and stained with toluidine blue.
Analyses of these sections were performed by light microscopy to detect the most advanced germ cell type labeled at the different time periods following thymidine injections. Cells were considered labeled when 4 or more grains were present over the nucleus on a low to moderate background.
Sudan III and Sudan Black Staining
For the investigation of the presence of lipids in peccary Leydig cells,
testis sections (5 µm) embedded in paraffin were deparaffinized and
rehydrated in diluted ethanol (100% to 70%). These sections were then immersed
in Sudan III (Chroma, Kongen, Germany) solution and Sudan Black (Sigma
Chemical Co, Sao Paulo, Brazil) solution for 20 minutes in a darkroom
(van Straaten et al,
1978).
Testis Stereology
The volume densities of the testicular tissue components were determined by
light microscopy using a 441-intersection grid placed in the ocular of the
light microscope. Fifteen randomly chosen fields (6615 points) were scored per
testis for each animal at x400 magnification. Seminiferous tubule
diameter and epithelium height were measured at x200 magnification using
an ocular micrometer calibrated with a stage micrometer. Thirty round or
nearly round tubule profiles were chosen randomly and measured for each
animal. Epithelium height was obtained in the same tubules used to determine
tubule diameter. The total length of seminiferous tubules (meters) was
obtained by dividing seminiferous tubule volume by the squared radius of the
tubule times 
(Johnson and Neaves,
1981).
Stages of the Seminiferous Epithelium Cycle
Stages of the cycle in collared peccary were characterized based on the
shape and location of spermatid nuclei, presence of meiotic divisions, and
overall composition of the seminiferous epithelium
(Amann, 1962;
Courot et al, 1970;
Leal and França, 2006).
This method—known as the tubular morphology system—provided 8
stages of the seminiferous epithelium cycle, the limits of which were quite
similar to those reported by Amann
(1962). Because a tubular cross
section could occasionally have more than 1 stage, stage frequencies were
based on the predominant cellular association observed
(Amann, 1962). Relative stage
frequencies were determined from the analysis of 150 seminiferous tubule cross
sections per animal at x400 magnification. Both testes were analyzed for
each animal. The histological sections used were those with better quality and
more tubule cross sections.
Length of the Seminiferous Epithelium Cycle
The duration of the spermatogenic cycle was estimated based on stage
frequencies and the most advanced germ cell type labeled at different times
following thymidine injection. The total duration of spermatogenesis took into
account that approximately 4.5 cycles are necessary for this process to be
completed from type A spermatogonia to spermiation
(Amann and Schanbacher, 1983).
Because primary spermatocytes' nuclear volume grows markedly during meiotic
prophase (França et al,
1995; Neves et al,
2002; Leal and França,
2006), the size of their nuclei was used to determine more
precisely the location of the most advanced labeled germ cell, particularly
when these cells were present in stages showing high frequency.
Cell Counts and Cell Numbers
Germ and Sertoli Cells—
All germ cell nuclei and Sertoli cell nucleoli present in stage 1 of the
cycle were counted in 10 randomly selected round (or nearly round)
seminiferous tubule cross sections for each animal. These counts were
corrected for section thickness and nucleus or nucleolus diameter based on the
method described by Abercrombie
(1946) and modified by Amann
(1962). For this purpose, 10
nuclei or nucleoli diameters were measured (per animal) for each cell type
analyzed. Cell ratios were obtained from the corrected counts obtained in
stage 1.
The total number of Sertoli cells was determined from the corrected counts of Sertoli cell nucleoli per seminiferous tubule cross section and the total length of seminiferous tubules (Hochereau-de-Reviers and Lincoln, 1978). DSP per testis and per gram of testis (spermatogenic efficiency) were obtained according to the following formula: DSP = total number of Sertoli cells per testis x the ratio of round spermatids to Sertoli cells in stage 1 x stage 1 relative frequency (%)/stage 1 duration (d) (França, 1992).
Leydig Cells—
Individual Leydig cell volume was obtained from nucleus volume and the
proportion between nucleus and cytoplasm. Because the Leydig cell nucleus in
the collared peccary is spherical, the nucleus volume was calculated from the
mean nucleus diameter. For this purpose, 30 nuclei with an evident nucleolus
were measured for each animal. Leydig cell nucleus volume was expressed in
µm3 and obtained from the formula 4/3R3, in which
R = nuclear diameter/2. To calculate the proportion between nucleus and
cytoplasm, a 441-point square lattice was placed over the sectioned material
at 400 x magnification and 1000 points over Leydig cells were counted
for each animal. The total number of Leydig cells per testis was estimated
from the individual Leydig cell volume and the volume occupied by Leydig cells
in the testis parenchyma.
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Results |
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TopAbstractMaterials and MethodsResultsDiscussionReferences |
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Stages of the Seminiferous Epithelium Cycle and Relative Stage Frequencies
Based on the criteria used for determination of stages using the tubule
morphology system, 8 stages of the cycle were characterized, as follows
(Figure 2):
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Stage 2— In this stage, spermatid nuclei began elongation and the chromatin of the early elongated spermatids was more condensed than in the previous stage. Primary spermatocytes were in transition from preleptotene to leptotene. Type A spermatogonia were also observed in this stage.
Stage 3— Elongated spermatids first formed bundles with their heads oriented towards the Sertoli cell nuclei, usually located at the base of the tubule. Young primary spermatocytes exhibited characteristics of leptotene cells. At the end of this stage, pachytene spermatocytes transitioned into the diplotene phase of the first meiotic prophase. The nuclei in type A spermatogonia were more frequent and similar in appearance to those seen in the previous stages.
Stage 4— The main characteristic of this stage was the presence of meiotic figures of the first and second divisions. Secondary spermatocytes and early round spermatids were also observed. Zygotene and diplotene spermatocytes were present. Elongated spermatid bundles were located within Sertoli cell crypts at about the middle portion of the seminiferous epithelium. A higher number of type A spermatogonia nuclei were present.
Stage 5— Two generations of spermatids were found in this stage: newly formed round and elongated spermatids. Elongated spermatid bundles were more packed and some were located deep within the epithelium. Type A spermatogonia nuclei were observed at the base of the tubule. Early pachytene spermatocytes were the predominant cell type located between round spermatids and the basal lamina.
Stage 6— The elongated spermatids bundles had moved toward the seminiferous tubule lumen. In comparison to the previous stage, pachytene spermatocyte nuclei were more distant from the basal lamina. Intermediate spermatogonia were found and type A spermatogonia were occasionally present in this stage.
Stage 7— Elongated spermatid bundles had dissociated and spermatid nuclei were located close to the tubular lumen; small residual bodies were also present. Type A and B spermatogonia were found in this stage, and the nuclei of the latter cell type were characterized by a round to ovoid shape and large amount of heterochromatin. Pachytene spermatocytes and round and elongated spermatids were the other germ cell types found in this stage.
Stage 8— The main characteristic of this stage was the location of elongated spermatids just being released at the luminal portion of the seminiferous tubule. Large residual bodies were observed just below elongated spermatids. Overall, the nuclear morphology of the round spermatids, pachytene spermatocytes, and type A and B spermatogonia in this stage were similar to that in the previous stage.
The mean percentage of each of the 8 stages was as follows: stage 1, 16.3% ± 1%; stage 2, 11.1% ± 0.7%; stage 3, 10.8% ± 0.7%; stage 4, 11.3% ± 1%; stage 5, 12% ± 0.9%; stage 6, 12.3% ± 0.9%; stage 7, 8.9% ± 0.7%; and stage 8, 17.3% ± 0.8%. Thus, stages 8 and 1 were the most frequent and stage 7 was the least frequent. The frequencies of the premeiotic (stages 1 to 3), meiotic (stage 4) and postmeiotic (stages 5 to 8) stages were approximately 38%, 11%, and 51%, respectively.
Length of the Seminiferous Epithelium Cycle
The most advanced labeled germ cell types observed at the different time
periods investigated after thymidine injections are displayed in
Table 2 and Figures
3 and
4. Approximately 1 hour after
injection, these cells present at the end of stage 2 (they went through 98% of
this stage) and located in the basal compartment were identified as
preleptotene spermatocytes or cells in the transition from preleptotene to
leptotene (Figure 3A). The most
advanced germ cells labeled 21 days after thymidine injection were round
spermatids at the end of stage 8, and these cells had traversed approximately
90% of this stage (Figure
3B).
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Based on the most advanced labeled germ cell type and stage frequencies, the mean duration of the seminiferous epithelium cycle was estimated as 12.3 ± 0.2 days. The duration of the various stages of the cycle was determined taking into account cycle length and the percentage of occurrence of each stage. As expected, the shortest was stage 7 (1.09 days) and the longest was stage 8 (2.13 days). Because approximately 4.5 cycles are necessary for the spermatogenic process to be completed, the total length of spermatogenesis in the collared peccary was estimated as 55.1 ± 0.7 days.
Testis Stereology
Tables 3 and
4 display the data related to
testis stereology. The meiotic index (measured as the number of round
spermatids produced per pachytene primary spermatocyte) was 3.2 ± 0.1.
This result demonstrated that at least 20% of cell loss occurs during the
meiotic prophase. Sertoli cell efficiency in the collared peccary (estimated
from the number of round spermatids per Sertoli cell) was 11.1 ± 0.7.
The number of Sertoli cells per gram of testis was 28 ± 2 x
106, and this number per testis was 5.8 ± 0.7 x
108. Regarding spermatogenic efficiency, the DSP per gram of testis
and per testis were approximately 23.4 ± 2 x 106 and
4.9 ± 0.6 x 108, respectively. Nucleus volume and size
in Leydig cells were 193 ± 24 and 1170 ± 99 µm3,
respectively. The number of Leydig cells per gram of testis was 120 ±
21 x 106, and 2.5 ± 0.5 x 109 cells
were found per testis.
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Discussion |
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The relative mass of seminiferous tissue determines how much space is devoted to sperm production. In general, species with testes that have a high proportion of seminiferous tubule tissue produce more sperm per unit mass, mainly when this aspect is associated with a higher number of Sertoli cells per testis and a higher number of germ cells per Sertoli cell (Sertoli cell efficiency; França and Russell, 1998; França et al, 2000; Hess and França, 2007; Johnson et al, 2008). Furthermore, germ cell loss (apoptosis), which occurs normally during spermatogenesis, plays an important role in establishing sperm production (Hess and França, 2007). Table 5 compares several important testicle parameters between the collared peccary and both domestic and wild boars. Despite the longer duration of spermatogenesis in the collared peccary, the spermatogenic efficiency found for this species was similar to that cited in the literature for domestic and wild boars. It is likely that the slower germ cell pace in peccaries is compensated by the higher number of Sertoli cells per gram of testis and greater Sertoli cell efficiency in comparison to domestic and wild boars, respectively. Germ cell loss during meiosis is similar in peccaries and domestic pigs.
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Peccaries and pigs belong to the Artiodactyla order and respectively to the Tayassuidae and Suidae families, having diverged approximately 40 million years ago from a common ancestor (Adega et al, 2008). The gonadosomatic index of peccaries is half the value found for domestic pigs. This is perhaps the result of extensive reproductive selection to which most domestic pig breeds have been submitted over the centuries.
Leydig cells are important to quantitatively normal spermatogenesis (Ewing and Zirkin, 1983; Deslypere and Vermeulen, 1984) and other important functional aspects, such as the function of male accessory organs/glands and sexual behavior/strategy (Kerr et al, 2006; Setchell and Breed, 2006). The size and number of Leydig cells per gram of testis are also known to exhibit remarkable variation among different mammalian species (Christensen and Fawcett, 1966; Hess and França, 2007). A number of studies comparing different mammalian species have demonstrated that the amount of testosterone produced is strongly correlated with the bulk of the smooth endoplasmic reticulum and mitochondria in Leydig cells (Haider, 2004; Saraiva et al, 2008). Although Leydig cell size in peccaries may differ from the values observed for domestic and wild boars (França et al, 2005; Almeida et al, 2006), the number per gram of testis in these 3 related species is quite high and situated on the upper level for the mammalian species investigated thus far (Hess and França, 2007). Moreover, the amazingly large number of lipids found in peccary Leydig cells could represent an interesting model for investigating the steroidogenic pathway in mammals. However, we do not know why Leydig cells in peccaries have a peculiar organization and distribution around the lobes of the seminiferous tubules. In an attempt to better understand the organization and cytoarchitecture of the testis in the collared peccary, we are developing longitudinal studies evaluating different testis regions, from the mediastinum/rete testis to the tunica albuginea. Because spermatogonial stem cells are preferentially located in microenvironments called "niches," and this microenvironment is provided in the somatic Sertoli cell, the basement membrane, and cellular components of the intertubular space (Hofmann, 2008), peccaries might represent an interesting model for investigating spermatogonial stem cell niche regulation and Sertoli-Leydig cell interactions.
The frequencies of the 8 stages characterized and grouped in the premeiotic and postmeiotic phases of spermatogenesis are similar in the collared peccary, wild boar, and domestic pigs (Almeida et al, 2006). This observation is in agreement with a number of reports in the literature (França and Russell, 1998; Neves et al, 2002; Almeida et al, 2006; Costa et al, 2008; Leal and França, 2009), suggesting that phylogeny is strongly related to stage frequencies when grouped in premeiotic and postmeiotic phases. Although the morphology of germ cells in peccaries was very similar to those described for domestic (Swierstra, 1968; França and Cardoso, 1998) and wild pigs (Almeida et al, 2006), the germ cell associations in peccaries resembled more those observed for the wild boar. For instance, the most advanced labeled germ cells 1 to 5 hours post–thymidine injection were preleptotene/leptotene, present in stage 1 in the domestic pig (Swierstra, 1968; França and Cardoso, 1998), whereas these labeled cells were located at the end of stage 2 in peccaries (present study) and wild boar (Almeida et al, 2006).
Comprehensive investigations on testis structure and function are essential for comparative studies and a better understanding of reproductive biology, behavior, and strategy. Despite the considerable economic potential of the collared peccary, this species remains poorly investigated. The results of the present study demonstrate that, in spite of its longer spermatogenic cycle length, spermatogenic efficiency in peccaries is similar to that obtained for the previously investigated species of the Suidae family. The results on Sertoli cell efficiency in the collared peccary suggest that this Tayassuidae species has a fairly good potential for increasing its reproductive performance. Therefore, we expect the knowledge generated by the present study to be useful in the near future for improvement programs aimed at the commercial exploitation of this interesting species.
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Acknowledgments |
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Footnotes |
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These authors contributed equally to this article and share
coauthorship. 
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References |
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TopAbstractMaterials and MethodsResultsDiscussionReferences |
|---|
Adega F, Chaves R, Guedes-Pinto H. Suiformes orthologous satellite DNAs as a hallmark of Pecari tajacu and Tayassu pecari (Tayassuidae) evolutionary rearrangements. Micron. 2008; 39: 1281 –1287.[CrossRef][Medline]
Almeida FF, Leal MC, França LR. Testis morphometry, duration
of spermatogenesis, and spermatogenic efficiency in the wild boar (Sus
scrofa scrofa). Biol Reprod. 2006; 75: 792
–799.
Amann RP. Reproductive capacity of dairy bulls. III. The effect of ejaculation frequency, unilateral vasectomy, and age on spermatogenesis. Am J Anat. 1962; 110: 49 –67.[CrossRef][Medline]
Amann RP, Schanbacher BD. Physiology of male reproduction.
J Anim Sci. 1983; 57: 380
–403.
Bodmer RE, Penn JW, Puertas PE, Moya LI, Fang TG. Conserving Amazonian forests through sustainable use of natural resources: interdisciplinary, community-based management of the Reserva Comunal Tamshiyacu-Tahuayo. In: Freese C, ed. Harvesting Wild Species. Baltimore, MD: Johns Hopkins University Press; 1997 : 315–318.
Bundy DC. Photographic emulsions and processing. In: Stumpf WE, Solomon HF, eds. Autoradiography and Correlative Imaging. San Diego, CA: Academic Press; 1995: 49 –57.
Christensen AK, Fawcett DW. The fine structure of testicular interstitial cells in mice. Am J Anat. 1966; 118: 551 –571.[CrossRef][Medline]
Clermont Y. kinetics of spermatogenesis in mammals: seminiferous
epithelium cycle and spermatogonial renew. Physiol
Rev. 1972;52: 198
–236.
Comizzoli P, Mermillod P, Mauget R. Reproductive biotechnologies for endangered mammalian species. Reprod Nutr Dev. 2000; 40: 493 –504.[CrossRef][Medline]
Costa GMJ, Chiarini-Garcia H, Morato RG, Alvarenga RLLS, França LR. Duration of spermatogenesis and daily sperm production in the jaguar (Panthera onca). Theriogenology. 2008; 70: 1136 –1146.[CrossRef][Medline]
Courot M, Hochereau-de Reviers MT, Ortavant R. Spermatogenesis. In: Johnson AD, Gomes WR, Vandemark NL, eds. The Testis. New York, NY: Academic Press; 1970: 339 –432.
Deslypere JP, Vermeulen A. Leydig cell function in normal men:
effect of age, life-style, residence, diet, and activity. J Clin
Endocrinol Metab. 1984;59: 955
–962.
Emmons LH, Feer F. Neotropical Rainforest Mammals: A Field Guide. Chicago, IL: University of Chicago Press; 1997 : 175–185.
Ewing LL, Zirkin B. Leydig cell structure and steroidogenic function. Recent Prog Horm Res. 1983; 39: 599 –635.[Medline]
França LR. Daily sperm production in Piau boars estimated from Sertoli cell population and Sertoli cell index. In: Dieleman SJ, ed. Proceedings of the 12th International Congress on Animal Reproduction and Artificial Insemination. Vol. 4 . Amsterdam, The Netherlands: Elsevier; 1992 : 1716–1718.
França LR, Avelar GF, Almeida FF. Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology. 2005; 63: 300 –318.[CrossRef][Medline]
França LR, Cardoso FM. Duration of spermatogenesis and sperm transit time through the epididymis in the Piau boar. Tissue Cell. 1998;30: 573 –582.[CrossRef][Medline]
França LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD.
Germ cell genotype controls cell cycle during spermatogenesis in the rat.
Biol Reprod. 1998; 59: 1371
–1377.
França LR, Russell LD. The testis of domestic animals. In:
Mart
nez F, Regadera J, eds. Male Reproduction: A
Multidisciplinary Overview. Madrid, Spain: Churchill Livingston; 1998
: 197–219.
França LR, Silva VA, Jr, Chiarini-Garcia H, Garcia SK,
Debeljuk L. Cell proliferation and hormonal changes during postnatal
development of the testis in the pig. Biol Reprod. 2000; 63: 1629
–1636.
França LR, Ye SJ, Ying L, Sandberg M, Russell LD. Morphometry of rat germ cells during spermatogenesis. Anat Rec. 1995;241: 181 –204.[CrossRef][Medline]
Gilbert B. Do not take the javelina lightly. Smithsonian. 1999; 30: 52 –60.
Haider SG. Cell biology of Leydig cells in the testis. Int Rev Cytol. 2004; 233: 181 –241.[Medline]
Hellgren EC, Lochmiller RL, Amoss MS, Jr, Seager SW, Magyar SJ,
Coscarelli KP, Grant WE. Seasonal variation in serum testosterone, testicular
measurement and semen characteristics in the collared peccary (Tayassu
tajacu). J Reprod Fertil. 1989; 85: 677
–686.
Hess RA, França LR. Spermatogenesis. Cycle of the seminiferous epithelium. In: Cheng CY, ed. Molecular Mechanisms in Spermatogenesis. Austin, TX: Landes Bioscience; 2007 : 1–15.
Hochereau-de-Reviers MT, Lincoln GA. Seasonal variation in the
histology of the testis of the red deer, Cervus elephus. J
Reprod Fertil. 1978;54: 209
–213.
Hofmann MC. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol Cell Endocrinol. 2008; 288: 95 –103.[CrossRef][Medline]
Johnson L, Neaves WB. Age-related changes in the Leydig cell population, seminiferous tubules and sperm production in stallions. Biol Reprod. 1981; 24: 703 –712.[Abstract]
Johnson L, Thompson DL Jr, Varner DD. Role of Sertoli cell number and function on regulation of spermatogenesis. Anim Reprod Sci. 2008;105: 23 –51.[CrossRef][Medline]
Kerr JB, Loveland KL, O'Bryan MK, Kretser DM. Cytology of the testis and intrinsic control mechanisms. In: Neill JD, ed. Physiology of Reproduction. Birmingham, AL: Elsevier; 2006 : 827–947.
Leal MC, França LR. The seminiferous epithelium cycle length
in the black tufted-ear marmoset (Callithrix penicillata) is similar
to humans. Biol Reprod. 2006; 74: 616
–624.
Leal MC, França LR. Slow increase of Sertoli cell efficiency and daily sperm production causes delayed establishment of full sexual maturity in the rodent Chinchilla lanigera. Theriogenology. 2009; 71: 509 –518.[CrossRef][Medline]
Low WA, ed. The Influence of Aridity on Reproduction of the Collared Peccary (Dicotyles tajacu) in Texas. Vancouver, Canada: University of British Columbia; 1970 .
Neves ES, Chiarini-Garcia H, França LR. Comparative testis
morphometry and seminiferous epithelium cycle length in donkeys and mules.
Biol Reprod. 2002; 67: 247
–255.
Peres CA. Population status of white-lipped Tayassu pecary and collared peccaries T. tajacu in hunted and unhunted amazonian forests. Biol Conserv. 1996; 77: 115 –123.[CrossRef]
Robinson JG, Redford KH. The use and conservation of wildlife. In: Robinson JG, Redford KH, eds. Neotropical Wildlife Use and Conservation. Chicago, IL: University of Chicago Press; 1991 : 3–5.
Saraiva KL, Silva VA Jr, Torres DO, Donato MA, Peres NG, Souza JR, Peixoto CA. Changes in mouse Leydig cells ultrastructure and testosterone secretion after diethylcarbamazine administration. Micron. 2008;39: 580 –586.[CrossRef][Medline]
Setchell BP, Breed WG. Anatomy, vasculature and innervation of the male reproductive tract. In: Neill JD, ed. Physiology of Reproduction. Birmingham, AL: Elsevier; 2006: 771 –825.
Sowls LK, ed. The Peccaries. Tucson, AZ: The University of Arizona Press; 1984.
Sowls LK, ed. Javelinas and Other Peccaries: Their Biology, Management, and Use. College Station, Texas: Texas A&M University Press; 1997.
Swierstra EE. A comparison of spermatozoa production and
spermatozoa output of Yorkshire and Lacombe boars. J Reprod
Fertil. 1968;17: 459
–469.
van Straaten HW, Ribbers-de Ridder R, Wensing CJ. Early deviations of testicular Leydig cells in the naturally unilateral cryptorchid pig. Biol Reprod. 1978; 19: 171 –176.[Abstract]
Wildt DE. Lions, tigers, and pandas, oh my. J
Androl. 2005;26: 452
–445.
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