THE BIOSTIMULATORY EFFECT OF BULLS ON THE HYPOTHALAMIC- PITUITARY-ADRENAL AND -OVARIAN AXES AND ON TEMPORAL ASPECTS OF RESUMPTION OF OVARIAN CYCLING ACTIVITY IN PRIMIPAROUS, POSTPARTUM, ANESTROUS, SUCKLED, BEEF COWS by Shaun Austin Tauck Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Animal and Range Sciences MONTANA STATE UNIVERSITY Bozeman, Montana November, 2008 ©COPYRIGHT by Shaun Austin Tauck 2008 All Rights Reserved ii APPROVAL of a dissertation submitted by Shaun Austin Tauck This dissertation has been read by each member of the dissertation committee and has been found to be satisfactory regarding content, English usage, format, citation, bibliographic style, and consistency, and is ready for submission to the Division of Graduate Education. Dr. James G. Berardinelli Approved for the Department of Animal and Range Sciences Dr. Bret E. Olson Approved for the Division of Graduate Education Dr. Carl A. Fox iii STATEMENT OF PERMISSION TO USE In presenting this thesis in partial fulfillment of the requirements for a doctoral degree at Montana State University, I agree that the library shall make it available to borrowers under rules of the library. I further agree that copying of this dissertation is allowable only for scholarly purposes, consistent with “fair use” as prescribed in the U.S. Copyright Law. Requests for extensive copying or reproduction of this dissertation should be referred to ProQuest Information and Learning, 300 North Zeeb Road, Ann Arbor, Michigan 48106, to whom I have granted “the exclusive right to reproduce and distribute my dissertation in and from microform along with the non-exclusive right to reproduce and distribute my abstract in any format in whole or in part.” Shaun Austin Tauck November, 2008 iv ACKNOWLEDGEMENTS I would like to thank my parents Mr. and Mrs. Rodney Tauck for their love and encouragement throughout my academic career at Montana State University. Also, I would like to express my sincerest thanks to my major professor, Dr. James G. Berardinelli, for his time, guidance, encouragement of new ideas, patience, constructive criticism, and friendship throughout the course of my graduate training. This study was supported by Award No. 2007-35203-17743, NRI Competitive Grants Program, CSREES, and the USDA, the Montana NSF EpsCOR program, the Montana Agricultural Experiment Station, and is a contributing project to Multistate Research Project, W1112, Reproductive Performance in Domestic Ruminants. I would also like to thank my graduate committee members, Drs. E. Keith Inskeep, Thomas Geary, Andy Roberts, and Charles Paden for their valuable time, assistance, and encouragement during the course of my studies and in the preparation of this dissertation. v TABLE OF CONTENTS 1. INTRODUCTION .........................................................................................................1 2. LITERATURE REVIEW ..............................................................................................5 Postpartum Anestrus ......................................................................................................5 The Effect of Bull Exposure on the Postpartum Anestrous Cow ..................................7 The Mechanism of the Biostimulatory Effect of Bulls ..........................................13 Social Interaction Hypothesis ....................................................................13 Effect of Bull Exposure on the Hypothalamic-Pituitary-Ovarian (HPO) axis .................................................................................................14 Pheromones ..................................................................................................................16 Pheromone Sensory Pathways ...............................................................................17 Odorant Receptor Neuron ..........................................................................17 Vomeronasal Organ ...................................................................................18 Main Olfactory Epithelium ........................................................................19 Accessory Olfactory Bulb (AOB) and Main Olfactory Bulb (MOB) ........20 Pheromonal Transport ............................................................................................21 Perception of Pheromones .....................................................................................26 Summary of Hypothetical Pheromonal Perception and Sensory Pathways...........28 Pheromones in Bovine Reproductive Behavior ...........................................................29 Temporal and Quantal Aspects of the Biostimulatory Effect of Bulls ........................33 Similarities between the Biostimulatory Effect of Bulls and the Male Effect in Sheep and Goats ...........................................................................................................36 Hypothalamic-Pituitary-Adrenal (HPA) Axis and Male Pheromones.........................40 Cortisol Synthesis, Secretion, and General Physiological Effects ...............................41 Interaction between the HPA Axis and HPO Axis ......................................................45 Effect of Suckling and Presence of Offspring on the HPA Axis .................................54 3. STATEMENT OF PROBLEM ....................................................................................57 4. EXPERIMENT 1: ADRENAL INVOLVEMENT IN THE BIOSTIMULATORY EFFECT OF BULLS ...................................................................................................59 Introduction ..................................................................................................................59 Materials and Methods .................................................................................................60 Animals and Treatments ........................................................................................60 Trial 1 .........................................................................................................60 Trial 2 .........................................................................................................60 Animal Housing Areas (Trials 1 and 2) .................................................................61 Bull Exposure (Trial 1) ..........................................................................................62 vi TABLE OF CONTENTS-CONTINUED Bull and Steer Urine Exposure (Trial 2) ................................................................62 Nutrition (Trials 1 and 2) .......................................................................................62 Blood Sampling (Trials 1 and 2) ............................................................................63 Statistical Analyses ................................................................................................64 Results ..........................................................................................................................65 Trial 1 .....................................................................................................................65 Trial 2 .....................................................................................................................67 Discussion ....................................................................................................................69 5. EXPERIMENT 2: CHARACTERISTICS OF TEMPORAL PATTERNS OF CORTISOL AND LUTEINIZING HORMONE IN PRIMIPAROUS, POSTPARTUM, ANESTROUS, SUCKLED, BEEF COWS EXPOSED ACUTELY TO BULLS ...............................................................................................72 Introduction ..................................................................................................................72 Materials and Methods .................................................................................................73 Animals and Treatments ........................................................................................73 Facilities .................................................................................................................73 Nutrition .................................................................................................................74 Intensive Blood Sampling Protocols ......................................................................75 Resumption of Ovarian Cycling Activity ..............................................................75 Cortisol and Luteinizing Hormone (LH) Assays ...................................................76 Characteristics of Temporal Patterns of Cortisol and LH Concentrations ............76 Statistical Analyses ................................................................................................77 Results ..........................................................................................................................77 Adaptation to Handling and Intensive Blood Sampling Protocols ........................77 Characteristics of Temporal Patterns of Cortisol Concentrations, D 2 through D 8 .....................................................................................................79 Characteristics of Temporal Patterns of LH Concentrations, D 2 through D 8 .....................................................................................................80 Relationships between Characteristics of Temporal Patterns of Cortisol and LH Concentrations ........................................................................80