HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Jiménez-Severiano, H. Articles by Kinder, J. E. Search for Related Content PubMed PubMed Citation Articles by Jiménez-Severiano, H. Articles by Kinder, J. E.

Season of the year influences testosterone secretion in bulls administered luteinizing hormone¹

H. Jiménez-Severiano^2,*,, J. Quintal-Franco³, V. Vega-Murillo⁴, E. Zanella⁵, M. E. Wehrman⁶, B. R. Lindsey⁷, E. J. Melvin⁸ and J. E. Kinder^9,*,

^* Department of Animal Science, University of Nebraska, Lincoln 68583-0908 and and Department of Animal Sciences, The Ohio State University, Columbus 43210-1095

⁹ Correspondence:
The Ohio State University, 110B Animal Science Building. 2029 Fyffe Road, Columbus, OH 43210-1095 (fax: 614-292-2929; E-mail:
kinder.15{at}osu.edu).

	Abstract

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 
The objective of the present study was to evaluate the secretion of testosterone (T) in bulls in response to the administration of varying doses of bovine LH (bLH) during the four seasons of the year. Five adult bulls (4 yr of age) were treated with an amount of bLH that was estimated to induce a 5 ng/mL amplitude pulse of LH in blood serum on five consecutive days around the spring equinox, summer solstice, fall equinox, and winter solstice. Five hours after this dose, bulls were treated with bLH in amounts that were estimated to induce a 0.25, 0.5, 1, 2, or 4 ng/mL amplitude LH pulse in blood serum in a Latin square design. Blood samples were collected for 5 h after administration of a dose of bLH that was estimated to induce the 5-ng amplitude LH pulse, and for 3 h after administration of the variable doses of bLH, and were then assayed for concentrations of T. Average concentrations and amplitude of T release after doses of bLH that were estimated to induce the 5-ng amplitude LH pulses were greater during the spring and summer than during the winter (P < 0.05). The area under the release curve (AUC) was greater during the spring than during the winter (P < 0.05). During the 3 h after treatment with the variable doses of bLH, T response was affected by dose (P < 0.001) and season (P < 0.001), but there was no dose x season interaction. Testosterone response increased in a dose-dependent fashion for all variables studied. The greatest average concentrations of T and AUC were observed in the spring compared with the fall and winter (P < 0.05). These data support our working hypothesis that testes of bulls are more responsive in releasing T in response to bLH stimulation in the spring and summer compared with the winter; however, there were no changes in sensitivity of the testes to LH during different seasons of the year as indicated by the lack of a dose of bLH x season interaction.

Key Words: Cattle • Male Animals • Seasonal Variation • Testes • Testosterone

	Introduction

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 
Cattle are considered a continuous (nonseasonal) breeding species (Tucker, 1982). Females have estrous cycles and males produce sperm cells and express sexual behavior throughout the year; however, some endocrine and reproductive variables fluctuate in an annual pattern (Tucker, 1982; Randel, 1984). In Holstein bulls, the number of sperm cells per ejaculate is affected by season of year (Everett et al., 1978). Semen quality (Godfrey et al., 1990a) and testis size (Godfrey et al., 1990b) decrease in the winter in Brahman bulls maintained in Texas, and this effect was more pronounced when bulls were relocated to northern latitudes. In a previous study evaluating secretory profiles of LH and testosterone (T) over 24 h during different seasons of the year, mean concentrations of LH were greatest during the spring and least during the winter in male cattle (Stumpf et al., 1993). A seasonal effect has also been reported in intact bulls for amplitude of LH and T pulses and mean concentration of T (Stumpf et al., 1993), as well as for GnRH-stimulated LH and T release (Godfrey et al., 1990a), which suggested a differential sensitivity of testes to gonadotropic stimulation throughout the year (Stumpf et al., 1993). However, it is not clear if the differential seasonal release of T is due to increased LH release during the seasons when the greatest T secretion occurs or if there is varying sensitivity of testes to LH during the seasons of the year when there is increased T. Therefore, the objective of the present study was to evaluate secretion of T in bulls in response to administration of varying doses of bovine LH (bLH) during the four seasons of the year. The working hypothesis was that testes of bulls would be more responsive to bLH as indicated by greater T concentrations in blood during the spring or summer as compared with the fall or winter months of the year as a result of increased sensitivity of the testes to bLH during these seasons of the year.

	Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 
Experimental Animals
The Institutional Animal Care and Use Committee at the University of Nebraska Lincoln approved all protocols and procedures used in this experiment. Five adult bulls of composite breeding (1/4 Hereford, 1/4 Angus, 1/4 Pinzgauer, 1/4 Red Poll) were used in the experiment. The study was conducted at the Beef Physiology Unit, located at the University of Nebraska Agricultural Research and Development Center (41°N latitude). At the beginning of the experiment, bulls averaged 4 yr of age, and BW ranged from 650 to 720 kg. Bulls were maintained on pasture and provided with a mineral supplement throughout the study. Supplemental hay and protein were also provided during the winter months to avoid weight loss. Bulls were brought to an environmentally controlled facility and offered hay and supplemental feed ad libitum only during the treatment and sampling periods. Bulls were weighed before initiation of treatments each season of the year.

Treatments and Experimental Design
Bulls were treated i.v. with purified bLH (teri.bLH.1.; provided by L. E. Reichert Jr., Tucker Endocrine Research Institute, Atlanta, Georgia) dissolved in 5% mannitol around the spring equinox (March 20 to 24), summer solstice (June 19 to 23), fall equinox (September 18 to 22), and winter solstice (December 19 to 23). Bulls were treated with an amount of bLH that was estimated to achieve a pulse of LH with an amplitude of 5 ng/mL in blood serum, starting at 0600 h on five consecutive days each season, in order to stimulate T secretion and synchronize T pulses in all five bulls before treatment with the varying doses of bLH, followed by 5 h of sampling at 1-h intervals. Then, bulls received a dose of bLH (in amounts that were estimated to achieve a pulse of LH with an amplitude of 0.25, 0.5, 1, 2, or 4 ng/mL of blood serum; different each day) at 1100 h, followed by 3 h of sampling at 20-min intervals. The amounts of bLH administered were calculated based on estimated volume of blood serum, taking into consideration the weights of the animals at each of the seasonal treatment periods and their estimated blood serum volume from hematocrit calculations. Amount of blood was estimated to be about 10% of the bulls’ body weight (Frandson and Spurgeon, 1992), and based on hematocrit values, the percentage of serum relative to total blood volume was estimated to be 53%. In a previous study (Stumpf et al., 1993), endogenous LH pulses had durations of less than 4 h at any season of the year, and LH concentrations returned to basal levels less than 5 h after the greatest concentration of the endogenous LH pulse had been achieved in blood serum. The amplitudes of LH pulses chosen for the present study were based on the range in amplitude of LH pulses that had been detected in the previous study (Stumpf et al., 1993). The first day of treatment, the variable dose of bLH was chosen at random for each bull. In the subsequent days, the variable dose was assigned to each bull to ensure that every bull received each of the variable doses on different days. This schedule of treatment was repeated during each season in a multiple Latin square design. Animals were fitted with indwelling jugular catheters (Tygon flexible plastic tubing, 1.27 mm i.d., 2.29 mm o.d.; Norton Performance Plastics, Akron, OH) before starting the bLH administration at each season of the year, and the catheter remained in place throughout the 5-d period of treatment. Blood samples were allowed to clot at room temperature, and then stored at 4°C. Blood samples were centrifuged within 36 h of collection at 1,500 x g for 20 min at 4°C. Serum was then decanted into polypropylene vials and stored at -20°C until assayed for T concentrations.

Testosterone Radioimmunoassay
Concentrations of T were determined in all the samples collected during the experiment. Duplicate 25-µL aliquots of serum were double-extracted with ether and extract residues were resuspended in 600 µL of Tris-buffered saline with 0.1% gelatin (TBS-gel) for assay by a double-antibody RIA, using a microscale method for liquid scintillation counting (Grotjan and Steinberg, 1978). The assay used a sheep T antibody (GDN No. 250; 200 µL of a 1:120,000 dilution) provided by G. Niswender (Colorado State University, Fort Collins), [1,2,6,7-³H (N)] testosterone (24,000 dpm/tube; New England Nuclear, Boston, MA), and donkey anti-sheep -globulin (DSG, 1002; 200 µL of a 1:55 dilution; ImmunoVision, Springdale, AR) as secondary antibody. The standard curve was prepared with T in solution with ethanol (3.6 to 461.4 pg/25 µL), allowed to dry, and resuspended in TBS-gel. The limit of detection was 50 pg/mL. The intra- and interassay CV were less than 10%.

The validation of the RIA for T was as follows. Fifteen different bull serum samples were assayed at 10, 20, and 40 µL. These serial dilutions generated binding inhibition curves that paralleled the T standard curve. Furthermore, the average ratios ± SD and correlations of the T concentrations obtained between the different pairs of volumes were 0.94 ± 0.13 (r = 0.996), 0.99 ± 0.11 (r = 0.99), and 0.93 ± 0.17 (r = 0.995), respectively, for 10 vs. 20 µL, 20 vs. 40 µL, and 10 vs. 40 µL. Three bovine serum samples were used to evaluate recovery of mass. Different amounts of added T were utilized (50, 100, 200, 400, and 800 pM/tube), and the average ± SD recovery from these samples was 97 ± 3.9%.

Statistical Analyses
Variables of response evaluated were average serum T concentration, amplitude of T release after bLH administration, and area under the curve (AUC) of the secretory profile of T after the dose of bLH was administered to induce an estimated pulse amplitude of 5 ng/mL of serum and after the variable doses of bLH. In addition, AUC was analyzed after T concentration at time zero, and all negative values after bLH administration were set to 0 ng/mL. Adjusting the data in this manner did not alter the outcome of the statistical analysis; therefore, only results for actual values are reported. Data were analyzed with the GLM procedure of SAS (SAS Inst., Inc., Cary, NC) for a completely randomized design for variables after the dose of bLH was administered to induce an LH pulse that was estimated to have a 5 ng/mL amplitude in serum, and for a Latin square design for data after the variable dose of bLH, with season and dose as the main factors, and the interaction of season x dose. The two blocking factors were bull and day. The PDIFF option of SAS was used to compare least squares means among seasons or doses. When necessary, variables were log₁₀ (Y+1) transformed so as to be consistent with the assumptions of the analysis of variance.

	Results

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 
Body Weight Changes
No substantial changes in BW occurred between seasons for any particular bull (data not shown). Body weight was maintained across the different seasons of the year, and it usually changed by less than 20 kg among seasons for any particular bull. Furthermore, the small changes in BW did not appear to be related to changes in testosterone secretion in response to various doses of bLH.

Testosterone Response After Dose of Bovine LH Is Estimated to Induce a 5 ng/mL Amplitude LH Pulse in Blood Serum
Season influenced (P < 0.05) T response during the 5 h following administration of the dose of bLH that was estimated to induce a 5 ng/mL amplitude LH pulse in blood serum (Table 1). Average T concentration was greater in spring and summer compared with winter (P < 0.05), and tended to be greater (P = 0.06) in the spring and less (P = 0.09) in the winter compared with the fall. Similarly, amplitude of T release after the dose of bLH estimated to induce a 5 ng/mL amplitude LH pulse was greater (P < 0.05) during the spring and summer compared with the winter and tended (P = 0.08) to be less in winter compared with the fall. The AUC of T profile was greater in the spring (P < 0.05) and tended (P = 0.09) to be greater in the summer compared with the winter. It is noted that during the spring, T concentration was increased before bLH administration (Figure 1) relative to other seasons (P < 0.05), and greater concentrations remained after the return to basal concentrations at 4 or 5 h after the time of bLH administration.

View larger version (22K): [in this window] [in a new window]   Figure 1. Testosterone secretory profile (mean ± SE; n = 5 at each time point) in bulls after administration of bovine LH (bLH) in doses that were estimated to induce a 5 ng/mL amplitude LH pulse in blood serum during different seasons of the year.

The AUC of T profile after variable doses of bLH were administered was influenced by season (P < 0.05; Table 2) and dose (P < 0.001; Table 3), whereas the interaction of season x dose was not significant (P = 0.63), also indicating no changes in sensitivity to bLH. During the 3 h following treatment with variable doses of bLH, AUC of T profile (Table 2) was larger in the spring compared with fall and winter (P < 0.05). The largest AUC of T profile (Table 3) was observed after treatment with the dose of bLH estimated to induce a 4 ng/mL amplitude LH pulse in blood serum (P < 0.05), and the smallest AUC of T profile occurred after treatment with the dose of bLH estimated to induce a 0.25 ng/mL amplitude LH pulse (P < 0.05).

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 
The most important findings in the present study are that T release by the bull testes in response to bLH administration is clearly affected by the season of the year, and this response is shown in a dose-dependent fashion. Physiologically, this indicates that the Leydig cells of the testis are more responsive to LH during those seasons of the year when there is the greatest response to LH. It is important to recognize that the enhanced response to bLH occurred with all doses of the hormone that were administered in a parallel fashion during the spring and summer, when there was an enhanced response to bLH compared with the fall and winter when the response to bLH was less. There was no indication of an enhanced sensitivity to bLH during specific seasons of the year as indicated by the absence of a dose x season interaction for any of the variables of T release that were evaluated after administration of bLH. If there were variations in sensitivity of the testis to bLH during different seasons of the year, the response of T release to bLH would not have been of the parallel nature that it was in the present study across season of the year, and an interaction of dose x season would have occurred.

Even though cattle are not considered to be seasonal breeders, previous studies have reported seasonal changes in some endocrine and reproductive variables in females (Tucker, 1982; Randel, 1984) and males (Everett et al., 1978; Godfrey et al., 1990a; Stumpf et al., 1993). Season of the year influences patterns of LH secretion in gonadectomized beef cows (Day et al., 1986; Stumpf et al., 1988) and bulls (Stumpf et al., 1993), with the greatest mean concentration of LH and pulse amplitude for this hormone being observed at the spring equinox and lesser concentrations at the winter solstice and fall equinox (Day et al., 1986; Stumpf et al., 1988, 1993). A similar effect of season of the year on LH concentration (Welsh et al., 1981) and amplitude of LH pulses (Stumpf et al., 1993) was detected in intact bulls.

In a previous study, there was no difference among seasons in T concentration (Peirce et al., 1987); however, other researchers have reported a seasonal effect on T concentration in intact bulls (Sundby and Tolman, 1978; Gwazdauskas et al., 1980; Stumpf et al., 1993), with the greatest concentrations found in the summer and the least during the winter (Sundby and Tolman, 1978; Stumpf et al., 1993). These results support the data from the present study since average T concentration, T release, and AUC of T release after the dose of bLH estimated to induce the 5 ng/mL amplitude LH pulses in blood serum were greater during the summer and spring as compared with the winter. The greatest values were usually detected in the spring, although the differences in values between the spring and summer were always nonsignificant. During the spring, T concentrations were already elevated before administration of the dose of bLH estimated to induce the 5 ng/mL amplitude LH pulse in blood serum and before the variable doses of bLH. Testosterone release followed the same order as that reported by Stumpf et al. (1993) for T pulse amplitude and for T and estradiol concentrations (i.e., in descending order, summer, spring, fall, and winter). An increased responsiveness of T release from testes after LH release has been reported to occur during the summer and spring because Brahman bulls had a greater AUC of T profile after GnRH administration during these seasons as compared with the winter. This response was observed even though bulls had a greater AUC for LH after GnRH treatment during the winter (Godfrey et al., 1990a). Furthermore, in the same study when GnRH was not administered, the AUC for T was greater in the spring compared with the fall for Brahman and Hereford bulls, with no differences in LH concentration (Godfrey et al., 1990a).

The seasonal fluctuations in T response to bLH in the present study closely paralleled the seasonal changes in testis size (Godfrey et al., 1990b; Stumpf et al., 1993) and semen quality (Godfrey et al., 1990a) in beef bulls, and in semen output and sperm concentration in the ejaculate of Holstein bulls (Everett et al., 1978) reported previously. It appears that the two major functions of the bovine testes, steroidogenesis and spermatogenesis, are influenced by season.

In the present study, bull testes released T in a dose-dependent fashion when bLH was administered in doses that were estimated to induce between 0.25 and 4 ng/mL amplitude LH pulses in blood serum, regardless of the season. This finding is not consistent with previous data, where amplitude of T release is similar after GnRH-induced LH pulses of different amplitudes (D’Occhio and Setchell, 1984; Post et al., 1987). However, in one report, T concentration was maintained above basal values longer after a larger GnRH-induced pulse of LH compared with results seen after smaller pulses (i.e., the total release of T was related to the amplitude of the preceding pulse of LH; Post et al., 1987). Those results agree with the present findings, where the largest AUC of T release occurred after administration of the largest doses of bLH.

The mechanisms governing the increased responsiveness of the testis to LH in the spring and summer are unknown. It is possible that season has an effect on Leydig cell number or on the population of LH receptors in the Leydig cell plasma membrane, which could then mediate this seasonal effect of LH on Leydig cell secretion of T. In this regard, prolactin might have an important role. Plasma concentrations of prolactin in cattle have seasonal fluctuations and are positively correlated with photoperiod (Bourne and Tucker, 1975; Tucker, 1983), with the greatest concentrations found during the spring and summer and lesser concentrations in fall and winter (Peirce et al., 1987; Berardinelli et al., 1992). These results closely parallel the seasonal changes in T response found in the present study and in other previously reported reproductive traits in bulls (Godfrey et al., 1990a,b; Stumpf et al., 1993). Therefore, if prolactin has a role on seasonal reproduction in cattle, this might be more closely related with that found in long-day breeding species (Gerlach and Aurich, 2000). However, prolactin receptors have not been detected in the testicular tissue of bulls, but they have been found in the testes of other species, such as golden hamsters (Klemcke et al., 1990), rats (Zhang et al., 1995), red deer (Jabbour et al., 1998), and sheep (Jabbour and Lincoln, 1999).

In seasonal breeding species, prolactin release is also positively correlated with day length, irrespective of the breeding pattern, and has been found to be an important regulator of seasonal reproduction (Gerlach and Aurich, 2000). Prolactin receptor protein and messenger RNA have been detected in Leydig and germ cells of the ovine testis (Jabbour and Lincoln, 1999; Lincoln et al., 2001), which suggests a role for this hormone in the regulation of steroidogenesis and spermatogenesis. Hamsters maintained under a short photoperiod have lesser concentrations of LH, FSH, and prolactin compared with those maintained under longer photoperiods (Bartke et al., 1985). In this species, prolactin stimulates testicular function by increasing binding of endogenous LH (Bex and Bartke, 1977) and has an important role in stimulating and maintaining a normal population of LH and prolactin receptors in the testes (Klemcke et al., 1984). During the seasonal regression of the testes, the decreased concentration of prolactin is associated with the lower content of testicular receptors for LH, FSH, and prolactin (Bartke et al., 1987). The reduction in LH receptors impairs the capacity of Leydig cells to produce androgens in response to LH in vivo (Bartke et al., 1990) and in vitro (Bartke et al., 1985; Dirami and Cooke, 1998). This is apparently due to a reduced activity of enzymes involved in T biosynthesis, such as the 17-hydroxylase:C_17,20-lyase enzyme complex (Bartke et al., 1985; 1990; Dirami and Cooke, 1998), and lesions in some signal transduction pathways (Dirami and Cooke, 1998).

Prolactin has also been shown to have a season-dependent stimulatory effect on testicular function in the ram by stimulation of T secretion and spermatogenesis (Regisford and Katz, 1993), and a positive effect on the recrudescence of testicular activity in black bears at the end of the hibernation period (Howell-Skalla et al., 2000). Follicle-stimulating hormone also has an important role on testicular steroidogenesis. Interestingly, FSH and prolactin restore the magnitude of the in vitro T production and sensitivity of testis from hypophysectomized hamsters to concentrations comparable to those of intact control animals, apparently through a paracrine effect of Sertoli cell products acting on the Leydig cell receptor population (Klemcke et al., 1990). However, it is not clear how this mechanism might have affected seasonal responsiveness and testosterone secretion in bulls in the present study since FSH concentration does not appear to be affected by season in intact bulls (Stumpf et al., 1993).

In summary, season has an effect on T secretion of bull testes, with increased responsiveness to bLH administration during the seasons when photoperiod is lengthening and decreased responsiveness when photoperiod is shortening. In the present study, there was no indication that there was an enhanced sensitivity to bLH during those seasons of the year when there was enhanced responsiveness to this hormone to induce the release of greater amounts of T from the testis. This lack of variation in sensitivity to bLH across various seasons of the year was indicated by no season x bLH dose interactions for any of the variables of T release that were assessed after administration of bLH. Therefore, the data from the present study support our working hypothesis that testes of the bulls are more responsive to LH during the spring and summer compared with winter months of the year, but there are not changes in sensitivity to this hormone that explain these changes in responsiveness to LH.

	Implications

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 
Even though cattle are considered a continuous-breeding species, the testes of bulls respond differently to luteinizing hormone administration throughout the year. Bull testes have an enhanced responsiveness during those seasons of the year when photoperiod is long compared with seasons where a short photoperiod exists. This differential responsiveness of the bull testes might account for the seasonal fluctuations in some reproductive variables observed in bulls and might implicate differences in their reproductive capacity throughout the year.

	Footnotes

 
¹ Published as paper No. 13938, Journal Ser. Nebraska Agr. Res. Div. Res. and as paper 43-02AS, Ohio Agricultural Research and Development Center, Columbus. Research supported by appropriated funds of the State of Nebraska. The academic programs of H. Jiménez-Severiano, J. Quintal-Franco, and V. Vega-Murillo were supported by the National Council for Science and Technology (CONACYT-Mexico) and the National Institute for Research in Forestry, Agriculture and Livestock (INIFAP-Mexico). We acknowledge M. Miller and K. Pearson for technical assistance with the RIA, K. Moline, J. Bergman, and B. Browelit for their assistance with caring for the bulls, and J. Osborne for assistance in editing and revising the manuscript.

² Current Address: CENID Fisiologia Animal, INIFAP-SAGARPA. Apdo. Postal 2-29, Queretaro, Qro. CP 76020, Mexico.

³ Current Address: INIFAP-CIR Sureste, A.P. 100-D, Suc. Itzimna, Merida, Yucatan, Mexico.

⁴ Current Address: INIFAP-Puebla, Carr. Al Batan No. 7106 Col. El Batan, C.P. 7273 Puebla, Puebla, Mexico.

⁵ Current Address: CNPSA/EMBRAPA, BR 153, km 110, Villa Tamandua-Caixa Postal 21, 89700-000, Concordia-SC, Brazil.

⁶ Current Address: Rocky Mountain Reproductive Services, Inc. P.O. Box 299, Manhattan, MT 59741-0299.

⁷ Current Address: AB Technology, NE 1335 Tree View Dr., Pullman, WA 99163.

⁸ Current Address: Bowman Gray School of Medicine, Wake Forest University, Winston Salem, NC 27106.

Received for publication June 12, 2002. Accepted for publication December 19, 2002.

	Literature Cited

Top Abstract Introduction Materials and Methods Results Discussion Implications Literature Cited

 


Bartke, A., A. G. Amador, V. Chandrashekar, and H. G. Klemcke. 1987. Seasonal differences in testicular receptors and steroidogenesis. J. Steroid Biochem. 27:581–587.[Medline]

Bartke, A., V. Chandrashekar, and A. G. Amador. 1990. Differential effects of short photoperiods on the release of progesterone and testosterone by hamster testes in vitro. J. Biol. Rhythms 5:241–246.[Abstract/Free Full Text]

Bartke, A., K. S. Matt, A. G. Amador, H. G. Klemcke, D. Brown, D. Gonzales, and M. P. Hogan. 1985. Effects of inhibitory and stimulatory photoperiods and sexual maturation on the ability of hamster testes to respond to hCG in vitro. Int. J. Androl. 8:232–242.[Medline]

Berardinelli, J. G., R. W. Godfrey, R. Adair, D. D. Lunstra, D. J. Byerley, H. Cardenas, and R. D. Randel. 1992. Cortisol and prolactin concentrations during three different seasons in relocated Brahman and Hereford bulls. Theriogenology 37:641–654.

Bex, F. J., and A. Bartke. 1977. Testicular LH binding in the hamster: Modification by photoperiod and prolactin. Endocrinology 100:1223–1226.[Abstract/Free Full Text]

Bourne, R. A., and H. A. Tucker. 1975. Serum prolactin and LH responses to photoperiod in bull calves. Endocrinology 97:473–475.[Abstract/Free Full Text]

D’Occhio, M. J., and B. P. Setchell. 1984. Pituitary and testicular responses in sexually mature bulls after intravenous injections of graded doses of LH-releasing hormone. J. Endocrinol. 103:371–376.[Abstract/Free Full Text]

Day, M. L., K. Imakawa, P. L. Pennel, D. D. Zalesky, A. C. Clutter, R. J. Kittok, and J. E. Kinder. 1986. Influence of season and estradiol on secretion of luteinizing hormone in ovariectomized cows. Biol. Reprod. 35:549–553.[Abstract]

Dirami, G., and B. A. Cooke. 1998. Effect of a dopamine agonist on luteinizing hormone receptors, cyclic AMP production and steroidogenesis in rat Leydig cells. Toxicol. Appl. Pharmacol. 150:393–401.[Medline]

Everett, R. W., B. Bean, and R. H. Foote. 1978. Sources of variation of semen output. J. Dairy Sci. 61:90–95.

Frandson, R. D., and T. L. Spurgeon. 1992. Anatomy and Physiology of Farm Animals. 5th ed. Lea and Febiger, Philadelphia.

Gerlach, T., and J. E. Aurich. 2000. Regulation of seasonal reproductive activity in the stallion, ram and hamster. Anim. Reprod. Sci. 58:197–213.[Medline]

Godfrey, R. W., D. D. Lunstra, T. G. Jenkins, J. G. Berardinelli, M. J. Guthrie, D. A. Neuendorff, C. R. Long, and R. D. Randel. 1990a. Effect of season and location on semen quality and serum concentrations of luteinizing hormone and testosterone in Brahman and Hereford bulls. J. Anim. Sci. 68:734–749.[Abstract]

Godfrey, R. W., D. D. Lunstra, T. G. Jenkins, J. G. Berardinelli, D. A. Neuendorff, C. R. Long, and R. D. Randel. 1990b. Effect of location and season on body and testicular growth in Brahman and Hereford bulls. J. Anim. Sci. 68:1520–1529.[Abstract]

Grotjan, H. E., Jr., and E. Steinberg. 1978. A micro-scale method for liquid scintillation counting, applicable to radioimmunoassay for steroids and substances of comparable relative molecular mass. Clin. Chem. 24:1193–1195.[Abstract/Free Full Text]

Gwazdauskas, F. C., J. A. Bame, D. L. Aalseth, W. E. Vinxon, R. G. Saacke, and C. E. Marshall. 1980. Relationship of plasma hormones and semen quality in bulls. Pages 13–20 in Proc. 8th Tech. Conf. Artificial Insemination and Natl. Assoc. Anim. Breeders, Columbia, MO.

Howell-Skalla, L. A., D. Burnick, R. A. Nelson, and J. M. Bahr. 2000. Testicular recrudescence in the male black bear (Ursus americanus): Changes in testicular luteinizing hormone-, follicle-stimulating hormone-, and prolactin-receptor ribonucleic acid abundance and dependency on prolactin. Biol. Reprod. 63:440–447.[Abstract/Free Full Text]

Jabbour, H. N., L. A. Clarke, A. S. McNeilly, M. Edery, and P. A. Kelly. 1998. Is prolactin a gonadotrophic hormone in red deer (Cervus elaphus)? Pattern of expression of the prolactin receptor gene in the testis and epididymis. J. Mol. Endocrinol. 20:175–182.[Abstract]

Jabbour, H. N., and G. A. Lincoln. 1999. Prolactin receptor expression in the testis of the ram: Localisation, functional activation and the influence of gonadotrophins. Mol. Cell. Endocrinol. 148:151–161.[Medline]

Klemcke, H. G., A. G. Amador, and A. Bartke. 1990. Hormonal regulation of testicular prolactin receptors and testosterone synthesis in golden hamsters. Biol. Reprod. 43:162–168.[Abstract]

Klemcke, H. G., A. Bartke, and K. T. Borer. 1984. Regulation of testicular prolactin and luteinizing hormone receptors in golden hamsters. Endocrinology 114:594–603.[Abstract/Free Full Text]

Lincoln, G. A., J. Townsend, and H. N. Jabbour. 2001. Prolactin actions in the sheep testis: a test of the priming hypothesis. Biol. Reprod. 65:936–943.[Abstract/Free Full Text]

Peirce, A. R. J., B. R. Downey, and L. M. Sanford. 1987. Seasonal changes in plasma concentrations of prolactin, LH, FSH, and testosterone in young adult bulls. Anim. Reprod. Sci. 13:165–176.

Post, T. B., M. M. Reich, and B. M. Bindon. 1987. Characterization of LH and testosterone responses to intramuscular injection of GnRH in tropical postpubertal bulls. Theriogenology 27:305–315.

Randel, R. D. 1984. Seasonal effects on female reproductive functions in the bovine (indian breeds). Theriogenology 21:170–185.

Regisford, E. G., and L. S. Katz. 1993. Effects of bromocriptin-induced hypoprolactinemia on gonadotrophin secretion and testicular function in rams (Ovis aries) during two seasons. J. Reprod. Fertil. 99:529–537.[Abstract/Free Full Text]

Stumpf, T. T., M. L. Day, P. L. Wolfe, M. W. Wolfe, A. C. Clutter, R. J. Kittok, and J. E. Kinder. 1988. Feedback of 17ß-estradiol on secretion of luteinizing hormone during different seasons of the year. J. Anim. Sci. 66:447–451.

Stumpf, T. T., M. W. Wolfe, M. S. Roberson, R. J. Kittok, and J. E. Kinder. 1993. Season of the year influences concentration and pattern of gonadotropins and testosterone in circulation of the bovine male. Biol. Reprod. 49:1089–1095.[Abstract]

Sundby, A., and R. Tollman. 1978. Plasma testosterone in bulls: seasonal variation. Acta Vet. Scand. 19:263–268.[Medline]

Tucker, H. A. 1982. Seasonality in cattle. Theriogenology 17:53–59.

Welsh, T. H., R. D. Randel, and B. H. Johnson. 1981. Interrelationship of serum corticosteroids, LH and testosterone in the male bovine. Arch. Androl. 6:141–150.[Medline]

Zhang, F. P., A. Rannikko, J. Toppari, A. Bartke, and I. Huhtaniemi. 1995. Developmental expression of the prolactin receptor gene in rat gonads. J. Endocrinol. 147:497–505.[Abstract/Free Full Text]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Jiménez-Severiano, H. Articles by Kinder, J. E. Search for Related Content PubMed PubMed Citation Articles by Jiménez-Severiano, H. Articles by Kinder, J. E.