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Feb 1, 1999 - The impact of male presence or absence on the timing of the preovulatory LH surge and estrus was studied in 3 experimental groups (n ...

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Stag exposure advances the LH surge and behavioral estrus in Eld's deer hinds after CIDR device synchronization of estrus Article  in  Theriogenology · June 1999 DOI: 10.1016/S0093-691X(99)00077-1 · Source: PubMed





8 authors, including: Dennis Hosack

Lisa Ware

Rio Tinto

Smithsonian Institution





Kendall Mashburn

Catherine Morrow

University of Alaska Fairbanks

Scimitar Scientific Ltd




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STAG EXPOSURE ADVANCES THE LH SURGE AND BEHAVIORAL ESTRUS IN ELD’S DEER HINDS AFTER ClDR DEVICE SYNCHRONIZATION OF ESTRUS D. A. Hosack,iz K. V. Miller,’ L. H. Ware,* K. L. Mashbum,* C. J. Morro~,~ L. R. Williamson,2 R. L. Marchintonr and S. L. Monfort* *School of Forest Resources, University of Georgia, Athens, GA 30602, USA *National Zoological Park, Conservation and Research Center, Smithsonian Institution Front Royal, VA 22630, USA Received for publication: Accepted:

~~~~ 26, 1998 February



ABSTRACT The impact of male presence or absence on the timing of the preovulatory LH surge and estrus was studied in 3 experimental groups (n = 6/group) of Eld’s deer hinds pretreated with intravaginal progesterone-releasing devices (ClDR-type G) as follows: Group 1 = indirect male contact barn; Group 2 = direct male contact barn; and Group 3 = male isolation barn. For all hinds, the duration of the preovulatory LH surge averaged 2.5 f 0.5 h, whereas mean peak preovulatory and basal LH concentrations were 2.9 +_0.2 ng mL-l and 0.27 + 0.03 ng mL-r, respectively. Nine of 12 male-exposed hinds exhibited a preovulatory LH surge within 24 to 32 h postCIDR device withdrawal, whereas 0 of 6 male-isolated hinds exhibited a preovulatory LH surge during the same time period. Onset of behavioral estrus (45.2 * 2.3, 52.7 + 5.7 and 66.3 f 1.8 h, respectively) was significantly advanced (P < 0.05) after CIDR device withdrawal in male exposed hinds (Groups 1 and 2) compared with male isolated hinds (Group 3). These data suggest that stag exposure is important for modulating the timing of the preovulatory LH surge and behavioral estrus after synchronization of estrus with exogenous progestagens. 0 1999 by Elssvier Science

Key words: luteinizing


hormone, cervid, Eld’s deer INTRODUCTION

The influence of male primers on female reproduction has received considerable research attention over the past 35 yr. Most studies have focused on the mechanisms whereby the male effect modulates estrous cyclicity in rodents (6,35,38), goats (7,28,29) and sheep (5, 19,27), whereas little work has been undertaken with nondomesticated species. The present study utilized Eld’s deer (Cervw &li thamin), a species whose basic reproductive biology has been described previously (15,22,23,24,36). Briefly, Eld’s deer are a subtropical species that still inhabit central Myanmar (formerly Burma), with a wild population estimated at fewer than 2,000 individuals (25). Behavioral (36) and endocrine (15,22,23) studies indicate that hinds are seasonally polyestrous, spontaneous ovulators, with onset of estrus occurring in late winter/early spring. Acknowledgments This research was funded bv a Scholarlv Studies Award from the Smithsonian Institution to S. L. Monfort, the Friends of the National Zoo, and the University of Georgia. We especially thank J. L. Brown for technical advice, helpful comments on the manuscript, and providing the PKC-231A antisera. T. Kiser, F. Thompson, and D. Wildt provided valuable suggestions on an earlier draft of this manuscript. We gratefully acknowledge A. S. I. Loudon for providing the RO 716 LH antisera and we thank L. E. Reichert, Jr. for iodination grade LH, and the NIDDK for NlH-LH-S18 standards. We are grateful to M. Bush, L. Bush, S. Murray and L. Tell for veterinary and technical support We are indebted to the many volunteers of the Rivinus Barn Complex for assisting with data collection. Theriogenology 51:1333-1342,1999 Q 1999 by Elsevier Science Inc.

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In the wild, rut occurs during late winter/earlv suring (16.33). and, during this time, normally solitary males are found in-herds (mean si& S-ma&; 8 females) of mix&l sex and age (33). During the nonbreeding season, territories of solitary stags may overlap considerably with those of larger groups of adult hinds and juveniles of both sexes. Eld’s deer stags utilize a “tending-bond” type of mating strategy, whereby the males maintain transient, close proximity to females and defend individual hinds from other stags until mating occurs (15). In captivity, Eld’s deer statrs utilize “latrines” in which thev reueatedlv deoosit fecal nellets and urine (37). In some species ‘;f territorial ungulates (26,30), iatr&es appear-to function’as markers and/or advertise male condition. or status. Latrine use also has been reported in a few cervid species, including muntjac CMunhacus ~QYX&; 8; Muntiam muntiak; 9), red bracket deer m americana; 18), and musk deer (Moschus moschiferus L.; 13; Moschm m, 14). Because Eld’s deer stags consistently use latrines in captivity, we became interested in studying the influence of olfactory communication, resulting from latrine odors, on estrous cyclicity in hinds. In a previous study, we demonstrated that direct or indirect stag contact, or urine alone, increased progestagen metabolite excretion in hinds during the first several estrous cycles of the reproductive season (15). Augmentation of urinary pregnanediol-3a-glucuronide (WG) excretion was expressed as an increase in the magnitude of PdG excretion rather than an increase in the length of the luteal phase. The present study was designed to extend the results of our previous investigations and to determine the impact of indirect male contact versus complete male isolation on the timing of the preovulatory LH surge and behavioral estrus after synchronization of estrus using exogenous progestagens. MATERIALS



Eighteen hand-reared Eld’s deer hinds (2 to 10 yr old; 50 to 90 kg body weight) were housed at the National Zoological Park’s Conservation and Research Center, Front Royal, Virginia (38’ N latitude) between January 1 and June 30. All hinds were exposed to natural fluctuations in photoperiod and ambient temperature, and were fed a diet consisting of alfalfa hay and a commercial ration (12.5% crude protein, 3.8% crude fat, 21.0% crude fiber; Herbivore Maintenance Diet, Agway Inc., C. G., Syracuse, NY, USA) with free access to a mineral block and water. Housing Three separate barn facilities were used for this research. Barn 1 was a double-winged facility that housed both male and female Eld’s deer continuously for 12 yr before the commencement of study. Males were housed in the north wing (n = 12) and females (n = 6) in the south wing, separated by a 25-m central corridor. Before the study, the sexes were not always segregated, and both sexes had been housed in both areas of Barn 1. Females were maintained in visual but not olfactory or auditory isolation from conspecific males in Barn 1. Barn 2, located 100 m north of Barn 1, was constructed 2.5 yr before the study was begun. Females in this barn were maintained in direct visual, olfactory and auditory contact with a mature, vasectomized stag (through a chain-link fence). Barn 3 was a facility located 2 km from the other experimental barns and had not previously housed Eld’s deer. Females in Barn 3 were housed and maintained in complete visual, olfactory and auditory isolation from stags. To avoid the inadvertent transmission of male odors on the clothing of animal handlers during the course of conducting routine husbandry procedures or urine sample collection, females in Barn 3 were tended to before other barns were visited.


Theriogenology Experimental Groups

Hinds were assigned randomly to experimental treatment groups and were separated into groups 4 mo before the start of the study. There were no significant differences (P > 0.1) in age or body weight among groups at the start of the experimental year. Three treatment groups (n = 6/group) were established: indirect, olfactory and auditory communication was possible for Group 1 hinds housed in Barn 1 (indirect male contact barn); Group 2 hinds were provided continuous, direct exposure to a vasectomized stag (through a chain link fence; direct male contact barn) in Barn 2; and Group 3 hinds were maintained in complete isolation from the stag in Barn 3 (male isolation barn). Synchronization

of Estrus

Synchronization of estrus was undertaken from April 4 to May 2 using intravaginal CIDR devices (type G, 0.365 g progesterone; InterAg, Hamilton, New Zealand), as previously described (25). Forty-eight hours before CIDR device withdrawal, each hind was administered 2 mL cloprostenol sodium (Estrumate, Miles Inc., Shawnee Mission, KS, USA; 500 pg, im). For all hinds, CIDR devices were removed 14 d after insertion at 1000 to 1200 h. Jugular cannulae were inserted within 4 h of CIDR device removal, after which the hinds were checked twice daily (at 0700 to 0800 and at 1500 to 1600 h) for overt signs of estrus, including scent marking of observers and/or assuming a humped-back, lordotic stance when manual pressure was applied to the hindquarters (23). Blood Sample Collection Twenty-four hours before intensive serial blood sampling (at the time of CIDR device withdrawal, see below), each hind was sedated with xylazine ([email protected], Mobay Corp., Shawnee, KS, USA; 0.15 mg kg-l, im) and a single intravenous jugular cannula was inserted (through a 12-gauge needle), sutured in place and connected to a 76-cm extension tube as described previously (24). The cannula was constructed of polyethylene tubing (id 0.1143 cm, od 0.1575 cm; [email protected]; Becton Dickinson and Co., Franklin Lakes, NJ, USA)with an 18-gauge luer stub adapter ([email protected],, Becton Dickinson and Co.). An initial blood samole (3 mL sample-l) was collected at the time of cannulation, then every 6 h for the first 24 h’po&nnulation. From 24 to 32 h postcannulation, intensive serial blood samples (3 mL sample-i) were collected every 15 min. From 32 to 70 h post-cannulation, blood sample collection continued at 6-h intervals. Final blood samples were collected at 70 h postcannulation. Blood samples were transferred into heparinized tubes, stored on ice and centrifuged within 2 h; plasma was harvested and stored at -7O’C until assayed. Luteinizing

Hormone Assay

Plasma LH was analyzed using a lzsI double-antibody RIA (22) that employed rabbit antiovine LH antiserum (PKC-231A, J. L. Brown, Conservation and Research Center, Front Royal, VA, USA) as the first antibody, purified ovine LH (LER-1056-C2, L.E. Reichert, Jr. Albany Medical Colleee. Albanv. NY. USA) as the tracer. and ovine LH (NIH-LH-S 18. National Pituitary Pro&&r, Baltimore, MD, USA) as the standard (pooled potency estimate and 95% confidence limit, 1.03 NM-LH-Sl units mg-l and 0.89 - 1.28 NIH-LH-Sl units mg-i, respectively). The LH tracer was made by the following procedure: 5 pg of LH were combined with 1 mCi of Narz51 in an oxidation-reduction reaction involving the use of chloramine-T the reaction was stopped by sodium metabisulfite; the entire radioactive portion was passed through an anion-exchange column; and the eluate was diluted to 25,000 c.p.m. tube’ in an RIA buffer. Assay sensitivity (i.e., 90% of maximum binding) was 0.2 ng r&-l and inter- and intra-assay coefficients of variation were

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