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Streams of a career in research: “It was a wonderful journey, this career of mine”

Streams of a career in research: “It was a wonderful journey, this career of mine” James G. Berardinelli Department of Animal and Range Sciences, Montana State University, Bozeman, MT 599717 © The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which per- mits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Transl. Anim. Sci. 2019.3:1617–1626 doi: 10.1093/tas/txz105 cows; 3) fertility of heifers and postpartum cows STREAMS OF A CAREER exposed to bulls during estrous synchronization The first question a reader might ask is, “what protocols that incorporate a controlled internal does he mean by streams of research?” Well, a drug-releasing device; and, 4) developing the use research stream may be defined as a series of re- of nuclear magnetic resonant spectroscopy of lated experiments or articles on one topic, each small molecular weight metabolites to identify progressing to dig deeper, especially to discover critical interactions of metabolites and metabolic new or unique information or to reach a new or hormones involved with reproductive endocrine more profound understanding: the best stream function, disease, and behavior of domestic and is programmatic and systematic, progressing wild ruminant species. There were many other from a hypothesis or conceptual mechanism, to “streamlets” in my career that were exceptionally fundamental, quantitative research. Ultimately, interesting and productive; however, I do not have this stream may lead to an application. A vi- the space to discuss these topics in this article. brant stream does not end [adapted from Peng The following narrative represents the chron- (2010) and the Cambridge Academic Content icles of “STREAM 1,” namely, the biostimula- Dictionary (2019)]. I hope this is made clear to the tory effect of bulls on postpartum, primiparous, reader by the end of this monograph. anovular, suckled beef cows. The long-term goal This journey is based on the premise/assump- of “Stream 1” was to determine the physiological tion that by understanding the variation in bio- mechanism(s) and pheromonal pathways by logical processes, we might be able to discover the which the biostimulatory effect of bulls acceler- underlying biological mechanisms that will allow ates the reproductive neuroendocrine–endocrine us to improve the efficiency and sustainability of cascade that culminates in resumption of ovula- the biological system that we are studying, espe- tory cycles in postpartum, anovulatory, suckled cially for economically important species. The cows. My hope was to develop technologies based major streams of research in my career included 1) upon the fundamental mechanism(s) involved physiological mechanism(s) whereby the biostim- with the biostimulatory effect of bulls that would ulatory effect of bulls accelerates resumption of increase reproductive efficiency of cow–calf op- cycling activity and improves fertility in heifers erations by providing management strategies that and in primiparous, postpartum, suckled beef were low cost, were time and labor saving, yielded cows; 2) factors that influence fertility at puberty consistent results and returns, and were easily ap- in heifers and ewe lambs, and at the resumption plicable, socially acceptable, and sustainable. of ovulatory cycles in postpartum, suckled beef STREAM 1: PUTTING IN (1974 TO 1979) Corresponding author: jgb@montana.edu Received June 6, 2019. As a young M.S. student in 1974, under Accepted July 25, 2019. the supervision of Dr. E. K. Inskeep, I got my 1617 1618 Berardinelli introduction to phenomenon of “biostimulation,” Technical Committee, W112, especially Drs. Ron although this word had yet to be coined in the Randall, Bob Short, Bob Staigmiller, Bob Bellows, literature. The term “biostimulation” originally Terry Nett, and Dennis Hallford. And, there are appeared in the literature in 1983 to refer to any many more collaborators on this committee that I stimulatory effect of a male on estrus and ovula- lack the space to mention but I would like to thank. tion in females through genital stimulation, prim- They were a tremendous resource and an invaluable ing pheromones, or other less defined external cues. network over the past 37 years. However, there are cases where females may have So, my “paddling” continued with one of the a biostimulatory effect on males or on other con- objectives of the W112 at the time, which was to specific females; thus, this term is not mutually ex- determine those factors that limit reproductive per- clusive for a given sex in mammals (Chenoweth, formance of beef heifers and postpartum, anestrous 1983). One could say that most of my career cen- cows. My first attempt at WVU to use mature bulls tered around this “biostimulatory effect” of males to accelerate the onset of puberty in heifers proved on anestrous or anovular females. disheartening; however, I reasoned that those By this time, it was known that the presence of negative results might have been caused by small an adult male reduced the age at puberty in female numbers of heifers and limited exposure periods. mice and gilts, and hastened the onset of the breeding Perhaps, heifers needed to be exposed to bulls for season in sheep and goats (for review, see Rekwot et longer than 30 d. Dr. Mark Roberson, then an MS al., 2001). So, we (actually, Dr. Inskeep) asked the student, and I tested this hypothesis by starting question, does the presence of a mature bull for 21 d bull exposure at 200 d of age on 100 prepubertal accelerate age at puberty in beef heifers? The answer heifers. Again, we found that bull exposure of beef to this question was NO, the presence of a bull, under heifers for 152 d did not accelerate age at puberty these conditions, did not influence age at puberty in (Roberson et al., 1987). We concluded that bull ex- beef heifers (Berardinelli et al., 1978). We then asked, posure of prepubertal beef heifers to long-term ex- if we “primed” heifers with progesterone (P4) and posure of bulls did not influence the occurrence of increased the exposure period to 30 d, would com- puberty under these conditions. Another “tip of the bining this treatment with the presence of bulls accel- canoe.” However, as we will see in the discussion of erate age at puberty in prepubertal heifers? Again, the postpartum, anovular cows, conditions matter! answer was NO; this combination did not appear to While I was working on the effect of bull on accelerate age at puberty in heifers (Berardinelli et al., heifers, I read an article from Nebraska indicating 1978). Thus, my first experience with biostimulation that resumption of estrous cycles was advanced by was certainly not positive. But I had learned much exposing mature, multiparous cows to bulls during about how to do science, gained vital experience in the early postpartum period (Zalesky et al., 1984). learning field and laboratory techniques, under - Ah, here is a case where a clear biostimulatory ef- standing the value of statistics, and learning how to fect occurs in cattle. As I dug into the literature, I write in a scientific manner during this 5-yr period at failed to find a single article regarding effects of bull West Virginia University (WVU). I was learning how exposure on primiparous suckled, anovular beef to paddle a canoe. cows, and Zalesky et al. (1984) made no mention of the physiological mechanisms by which bulls might influence postpartum reproductive function of STREAM 1: INTO THE MAIN CHANNEL suckled cows. Luckily, and thanks to Dr. Richard (1981 TO 2001) (Butch) Whitman, there was a management change I began my academic career by joining the fac- in 1985 involving first-calf cows in our herd. They ulty of Montana State University in the Department would now be housed and maintained on the farm of Animal and Range Sciences in 1981 as an as- in Bozeman. This was vitally important for it al- sistant professor. This required me to develop a lowed me direct and easy access to this type of cow, modern laboratory (for the time) from scratch and and with some effort, I could manipulate the facil- establish a research program in reproductive physi- ities to isolate groups of cows and bulls from one ology and endocrinology. These were no easy tasks another. In hindsight, it was like I could stop “pad- at the time. However, I had a very good mentor dling” and use a motor on this journey. and collaborator in Dr. Peter Burfening, whom I Our first experiment involved exposing first- thank for all his support and encouragement dur- calf, suckled cows to bulls continuously, starting 3 ing my career. As important as he was in shaping d after calving to determine whether this type of my career were the members of the Western Section exposure would alter postpartum interval to estrus, Translate basic science to industry innovation Streams of a career in research 1619 and patterns of luteinizing hormone (LH) con- 15-min intervals every third day for 18 d. Sampling centrations. More importantly, we thought to get from BEI cows began 2 h before introduction of a a glimpse of a mechanism by taking serial, 15-min bull every other day. We found that mean LH and blood samples for 6 h at weekly intervals starting LH pulse frequency increased within the 6-h sam- 10 d after initial exposure of cows to bulls for assay pling period in both NEBE and BEI cows to bulls of LH. Our hypothesis was that characteristics of compared to NE cows. Surprisingly, even though pulsatile patterns of LH would increase sooner in LH pulse frequency increased with intermittent cows exposed to bulls (BE) than in cows not ex- 2-h exposure every third day, these cows did not re- posed to bulls (NE). Results of two trials clearly spond to the biostimulatory effect, i.e., interval to demonstrated that the presence of bulls accelerated resumption of ovulatory activity did not occur any resumption of ovulatory cycles in primiparous, sooner than that in NE cows. suckled beef cows. However, characteristics of LH On the basis of these data and the hypoth- patterns in weekly sample did not indicate that the esis that increased LH secretion plays a significant presence of bulls altered temporal pattern of LH role in the resumption of ovarian cycling activity, (Custer et al., 1990). This result did not seem to one might conclude that bulls effect a reduction in fit the consensus hypothesis that in order to accel- postpartum interval to ovulation by increasing LH erate resumption of ovulatory cycles in anovular secretion acutely and chronically after exposure. females, any stimulus(i) should affect the hypothal- However, cows that were intermittently exposed amic–pituitary axis to increase GnRH and in turn to bulls did not exhibit estrus and ovulation any increase pulse frequency of LH, which stimulates sooner than cows isolated from bulls. One interpret- final stages of follicular development, estradiol in- ation of these results is that immediate exposure to crease, and ovulation. Perhaps the timing of sam- bulls induces a pheromonally activated trigger (sig- pling was insufficient to determine if the presence naling type) that induces a hypothalamic release of of bulls altered this axis and LH patterns. GnRH and subsequent acute release of LH, specif- At this point, we thought two important issues ically an increase in pulse frequency. However, this had to be addressed to gain some insight into this type of stimulation (conditions) does not result in physiological mechanism. The first was whether cows the induction of ovarian cycling activity. We pos- needed to be exposed continuously to bulls “soon” tulated that there must either be exteroceptive cues after calving to obtain a biostimulatory response, and other than pheromones or that there is some type the second was whether continuous, 24-h exposure, of “re-enforcement mechanism” associated directly was required to elicit a biostimulatory response. Dr. with the physical presence of the bull involved in Dave Fernandez was a graduate student of mine at the biostimulatory effect of bulls on postpartum the time that tackled these difficult issues. First, we cows (Fernandez et al., 1996). This was a dilemma exposed of primiparous, suckled beef cows to mature that needed attention in order to understand this bulls in the first 30 days after calving (BE/NE), ex- mechanism. posed them beginning 30 d after calving (NE/BE), or Before we tackled this dilemma and to gain a exposed them continuously starting 3 d after calving more profound understanding of the biostimu- (BE). We found that postpartum intervals to resump- latory effect of bulls it was vital to precisely nail tion of ovarian cyclic activity did not differ among down the temporal development of the response of BE, BE/NE, and NE/BE cows, but they were 15.4 d postpartum anovular cows to the biostimulatory ef- shorter than for NE cows (Fernandez et al., 1993). fect of bulls. The question to be answered was are We now knew that we could obtain a biostimulatory primiparous, anovular, suckled cows more sensitive effect of bulls by exposing cows continuously 30 d to the biostimulatory effect of bulls when exposure after calving that was the same as continuous ex- to bulls occurs at progressively longer intervals posure beginning 3 d after calving. after calving? To answer this question, we exposed We then exposed cows to a bull initially on day primiparous, anovular, suckled cows to bulls at 15, 30 after calving (NEBE), exposed cows to a bull for 35, or 55 d after calving. Evaluation of the cumu- 2 h every third day beginning on day 30 after calving lative 10-d distribution of percentages of cows that (intermittent exposure; BEI), or did not expose resumed ovulatory activity among cows exposed to cows to a bull (NE). More importantly, this design bulls beginning 15, 35, and 55 d after calving indi- gave us the opportunity to collect serial blood sam- cated that cows become responsive to the biostimu- ples from cows to evaluate temporal LH patterns latory effect of bulls about 35 to 40 d after calving acutely and chronically after exposing cows to bull. and sensitivity increases as time after calving in- Blood samples were obtained over a 6-h period at creases (Fig. 1; Berardinelli and Joshi, 2005). Translate basic science to industry innovation 1620 Berardinelli BE15 NE15 80 BE35 NE35 BE55 NE55 Insensitive period Sensitive period 0-10 11-20 21-30 31-40 41-50 51-60 Days after calving Interval (d) Figure 2. Relative hypothetical sensitivity of primiparous, anovu- Figure 1. Cumulative percentages of primiparous, suckled beef lar, suckled beef cows to the biostimulatory effect (BSE) of bulls after cows exposed to presence of a bull (BE) or not exposed to a bull (NE) calving (day 0). on either days 15, 35, or 55 after calving that resumed ovarian cycling activity. Interaction Χ = 18.6, df = 10; P < 0.05. This was an important finding that impacts the Please note that we think that insensitive to sen- effectiveness of the biostimulatory effect of bulls dur- sitive periods can slide left or right depending on ing early postpartum anestrus of cows. We would the influences of other major factors that affect the have recognized this earlier if I would have examined length of postpartum anestrus in suckled cows. the differential in intervals to resumption of ovula- Around 2000, it became apparent to my labora- tory activity between cows exposed to bulls starting 3 tory that a critical feature of the biostimulatory ef- d after calving compared to cows exposed on day 30 fect of bulls was missing, that was, what might it after calving (Fernandez et al., 1996). The differen- be and what is its source? We and most investiga- tial was much shorter for cows exposed beginning on tors at the time assumed or speculated that bulls day 30 after calving than for cows exposed 3 d after produce a primer pheromone that acts via an ol- calving! Nevertheless, the question then became what factory pathway to evoke this response (for review, is it about those first 35 d after calving that dampens see Rekwot et al., 2001). Thus, we investigated the or attenuates the biostimulatory effect of bulls? hypothesis that the biostimulatory effect of bulls is The answer to this question may be the fol- mediated by exteroceptive stimuli of bulls in a series lowing. This corresponds to the period during of three experiments. The first experiment tested which inhibitory influences on LH secretion, such the hypothesis that exposing postpartum, anovular as increased sensitivity to the negative feedback of suckled cows to excretory products of bull for 12 estradiol, the maternal cow–calf bond, and lacta- h daily would evoke the same biostimulatory re- tional stimuli are still very high. Possible explan- sponse as continuously exposing cows to the phys- ations for this observation are either there is no ical presence of bulls. Indeed, we found that interval pheromonal mechanism in cows during this period to resumption of ovulatory activity and the propor- to respond to bulls and they developed them espe- tions of cows that resumed ovulatory activity were cially for this time in their reproductive life cycle shorter and greater, respectively, for cows exposed (not likely), or the pheromonal mechanism is pres- to a bull continuously or cows exposed to the ex- ent but the negative effects that suppress LH release cretory products of bulls for 12 h daily compared have the same inhibitory effect on the pheromonal with those metrics of cows not exposed to a bull or system that mediates the biostimulatory effects of excretory products of bulls. More importantly, the bulls (highly likely). If the latter is the case, then the temporal responses for the proportions of cows cyc- apparent “insensitive period” is related to the inten- ling at 10-d intervals after exposure to a bull or the sity of stimulation. Increasing the “intensity” (dose excretory products of bulls were identical (Fig. 3; or duration of exposure) should induce a response Berardinelli and Joshi, 2005). to the biostimulatory effect of bulls. If the former These data clearly indicate that excretory prod- is true, then no level of intensity of bull biostimula- ucts (urine, feces, or mucus/saliva) of bulls hastened tion will evoke a response. Nevertheless, cows begin the resumption of ovulatory activity in postpartum, to become responsive to the biostimulatory effect anovular, suckled cows. Therefore, the biostim- of bulls about 35 to 40 d after calving, and it ap- ulatory mechanism appears to be mediated by a pears that sensitivity increases as time after calving pheromone(s) present in their excretory products increases (Berardinelli and Joshi, 2005). An illustra- and does not appear to be reenforced by the phys- tion of this conceptualization in presented in Fig. 2. ical presence of bulls. This was an extraordinary Translate basic science to industry innovation Cumulative % Relative sensitivity to BSE Streams of a career in research 1621 Figure 3. Cumulative percentages of first-calf restricted suckled Figure 4. Percentages of first-calf suckled cows exposed to ma- beef cows exposed continuously to presence of a bull (BE), exposed ture bull urine (BUE) or exposed to steer urine (SUE) that resumed to excretory products of bulls (EPB), not exposed to a bull (NE), or ovarian cycling activity by the beginning of the estrus synchronization exposed to excretory products of cows (EPC) that resumed ovarian protocol. Bars with common letters do not differ, P = 0.25, X = 1.3, cycling activity in 10-d intervals from day 0 to end of the experiment. df = 1. The blue-shaded area represents points that do not differ (P > 0.10) among BE, EPB, and EPC cows. activity (Berardinelli et al., 2010). We concluded discovery at the time. But, could we nail down a that continuous or 12-h exposure of postpartum, specific excretory product that would be a major anovular, suckled cows to bull urine does not carrier for such a pheromone? allow for a pheromonally induced activation of Perhaps we could as Baruah and Kanchev the hypothalamus–pituitary–ovarian (HPO) axis (1993) reported that bull urine sprayed into the to stimulate the cascade resulting in resumption of nasal passages of dairy cows 7 d after calving in- ovulatory activity. creased systemic LH and follicle stimulating hor- However, these results do not preclude the pos- mone concentrations within 70 min of exposure, sibility that bull urine contains a biostimulatory and we knew that other reproductively active pheromone(s), but may indicate that the “mode” pheromones in mammals are carried in urine. We (frequency, amplitude, duration) of pheromonal asked the question: does exposing cows to mature stimulation may be an important factor that deter- bull urine mimic the biostimulatory effect of bulls mines the biostimulatory effect of bulls on resump- to reduce the postpartum interval to ovulatory ac- tion of luteal activity in postpartum, suckled beef tivity in primiparous, anovular suckled cows? In an cows. Too much for too long each day may “desen- elegant experiment by Tauck et al. (2006), we tested sitize” or overly stress the HPO axis, whereas too the hypothesis that continuous exposure (24 h) of little or too short a duration of exposure may be cows to bull urine would accelerate resumption of insufficient to be recognized as stimuli to generate ovulatory activity. Urine from bulls and steers was a response by the HPO axis of primiparous, anovu- delivered continuously to cows by means of an in- lar, suckled cows. genious, controlled urine deliver device. We found That this might be the case can be inferred from that interval from urine exposure and proportions an experiment involving fenceline contact between of cows that resumed ovulatory activity did not bulls and cows. We found that exposing cows to differ between BUE- and SUE-exposed cows after direct fenceline contact (BEFL) with bulls penned 64 d of exposure (Fig. 4). This was a disconcerting within their pen accelerated resumption of ovula- result. However, we reasoned that perhaps 24-h ex- tory activity compared with cows not exposed to posure of cows to bull urine, under these conditions bulls (NE). However, the biostimulatory response (again, conditions) in some manner, actually “de- of cows exposed to fenceline contact was not as dra- sensitized,” downregulated, or otherwise stressed matic as that for cows exposed to the physical pres- the physiological system(s) that sense and perceive ence of bulls (Fig. 5; Berardinelli and Tauck, 2007). a urinary pheromone by cows. To test whether this Although these data indicate qualitatively that might be the case, we exposed primiparous suckled intensity of the biostimulatory effect of bulls is an cows to mature bull urine or saline by constant drip important factor to consider in this effect, they did for 12-h daily onto straw-bedding, and then placed not yield insight regarding the quantity and dur- cows into these areas for 12-h daily. Again, 12-h ation of exposure necessary to evoke a response. As exposure to straw-bedding containing bull urine I stated previously, these are critical variables that did not affect interval to resumption of ovulatory we had yet to measure. Nevertheless, we think that Translate basic science to industry innovation 1622 Berardinelli Figure 6. Linear regression of interval from the start of bull ex- posure (D 0) to resumption of ovulatory activity on hours of daily ex- Figure 5. Cumulative frequency distribution of the percentages of posure for primiparous, postpartum, anovular, suckled cows exposed primiparous, anovular cows exposed to close physical contact with ma- to bulls for 0, 6, or 12 h. Y-intercept (b0) = 42.2 d; slope (b1) = 1.01 d/h ture bulls (BE) or not exposed to bulls (NE) for 35 d and exposed to (P < 0.05); R = 0.18. fenceline contact with bulls (BEFL) or not exposed to bulls (NE) for 42 d. collectively, these data indicated that there is a min- Integrating the results of our “stream of re- imum and maximum intensity to the pheromonally search” to this point, we developed the concept that mediated effect of bulls, if the pheromone is carried cows respond to bull-pheromonal “stimulation and by urine. relaxation cycles” in a dose-dependent manner. This The next critical question that we asked was does type of cyclic presentation of stimuli may be a critical the response of cows to the biostimulatory effect of component of the pheromonal mechanisms by which bulls involve a duration of exposure component? the biostimulatory effect of bulls accelerates resump- Fernandez et al. (1996) reported that interval from tion of ovulatory activity. However, it appeared to calving to resumption of ovulatory activity was not us, that in some way, there was some type of reen- accelerated in cows exposed to bulls for 2 h every third forcement mechanism or agent related to dosage, in- day for 18 d beginning 33 d after calving. However, tensity, and duration of the mechanism involved a length of postpartum anestrus was reduced in cows pheromonally mediated biostimulatory effect of bull. exposed to the excretory products of bulls for 12 h This idea led us to the following question: what daily (Berardinelli and Joshi, 2005). With these re- physiological factor(s) might act as a “triggering” sults in mind, we tested the hypothesis that duration and (or) “re-enforcing” agent for the putative phero- of bull exposure and interval to resumption of ovula- monal mechanism to stimulate resumption of ovu- tory activity ovulatory in primiparous, anovular, suck- latory activity? In rodents, there appeared to be a led cows exposed to bulls for 0, 6, or 12 h daily would clear functional relationship between the hypothal- progressively accelerate resumption of ovulatory ac- amic–pituitary–adrenal (HPA) axis and induced tivity in anovular, suckled primiparous cows. Indeed, pheromonal activation or inhibition of female re- the results of this experiment showed that the number productive events (Mora and Sánchez-Criado, of hours of daily bull exposure required to accelerate 2004). Might there be the same relationship in the resumption of ovulatory in postpartum, anovular, bovine? To answer this question, we evaluated cor- suckled cows decreases in a linear manner (Tauck tisol concentrations in blood samples obtained at et al., 2010a; Fig. 6). Thus, the duration of bull-pher- 3-d intervals from cows exposed continuously to omone stimuli that cows perceive each day is related bull urine (BUE) and cows exposed to the physical to how soon after exposure primiparous, postpartum, presence of bulls (BE) starting 35 d after calving anestrous, suckled cows respond to this stimulus and (Tauck et al., 2007). Remember, interval to resump- undergo the physiological changes necessary to re- tion of ovulatory activity for BUE cows did not sume ovulatory activity. The dose-dependent manner differ from that in SUE cows, but BE cows resumed by which pheromones produced by bulls accelerated cycling much sooner that NE cows (Tauck et al., resumption of ovulatory activity in postpartum, ano- 2007). Surprisingly, systemic cortisol concentra- vular, suckled cows may explain disparate reports in tions in BE cows increased significantly within 9 d the literature concerning fenceline contact and inter- after exposure, and the difference in cortisol concen- mittent exposure of cows to bulls. trations was maintained throughout the exposure Translate basic science to industry innovation Streams of a career in research 1623 period compared to those of NE cows, and all BE characteristics of temporal patterns of both LH cows resumed cycling activity! In contrast to these and cortisol by increasing LH pulse frequency and results, cortisol concentrations in BUE cows clearly decreasing cortisol pulse frequency. Interestingly, follow the same temporal pattern as that of SUE in cows exposed to bulls, as amplitude and fre- cows over the exposure period, and BUE cows had quency of cortisol pulses decreased, amplitudes of the same interval to resumption of ovulatory ac- LH pulses increased, and frequency of LH pulses tivity as SUE cows. We suggested that these data tended to increase (Tauck et al., 2010b). Thus, the indicated a strong possibility that activation of the physiological mechanism of the biostimulatory ef- HPA axis might be intimately, but subtlety, involved fect of bulls may initially involve modification of with the pheromonally mediated biostimulatory ef- the HPA axis, and these changes may facilitate ac- fect of bull (Tauck et al., 2007). tivation of the HPO axis and resumption of ovula- To gain insight into this possibility, we evalu- tory cycles in postpartum, anovular, suckled cows ated characteristics of temporal patterns of cortisol (Tauck, 2008). Our interpretations of these results and LH in postpartum, anovular, suckled beef cows are graphically presented in Fig. 7. after acute exposure to bulls. Our hypothesis was Finally, in this stream, there is “the rest of the that acute exposure of cows to bulls for 5 h daily story.” For resumption of ovulatory activity to occur over a 9-d period would increase cortisol concen- in postpartum, anovular suckled cows, changes in trations, and in turn, increase mean and frequency LH pulse frequency related to ovarian follicular of LH concentrations like that which would trigger development, maturation of dominant follicles the neuroendocrine–endocrine ovulatory cascade. (DFs), and ovulation are required. Therefore, it was We reported that exposing postpartum, anovu- reasonable to postulate that as the physical pres- lar, suckled cows to bull in this manner altered ence of bulls to cows increases pulse frequency of Effect of Anestrous Factors Effect of Pheromones of Bulls (Cow-calf bond, lactation, nutrition, Frequency Duration Smoothness etc.) 7 7 5 5 4 4 1 1 060120 180240 300360 060120 180240 300360 Time, min Time, min Cortisol on LH secretion Cortisol on LH secretion LH pulse frequency 1.5 1.5 1 1 0.5 0.5 0 0 060120 180240 300360 060120 180240 300360 Time, min Time, min Figure 7. Graphic representation of the effect of factors that influence length of postpartum anestrus and the biostimulatory effect of bulls on the hypothalamic–pituitary–adrenal axis of postpartum, anovulatory, suckled beef cows. Translate basic science to industry innovation LH, ng/mL Cortisol, ng/mL LH, ng/mL Cortisol, ng/mL 1624 Berardinelli LH in postpartum cows, the biostimulatory effect mechanism with the following illustration (Fig. 9) and of bulls may influence follicular wave dynamics of interpretation. exposed cows. Indeed, in the studies by Wilkinson Bulls produce an androgen-dependent phero- (2009), it was reported that exposing cows to bulls mone that is carried from the blood to the urine altered follicular growth and developmental pat- by major urinary protein (MUP), α-2u globulin, terns by decreasing the number of follicular waves albumin, or a combination thereof. This phero- and increasing mean follicle diameter before re- mone is excreted in urine, feces, cutaneous se- sumption of ovulatory activity (Fig. 8). We inter- cretions, or a combination of these excretory preted these results to mean that the biostimulatory products. Alpha-2u globulin, MUP, or albumin effect of the bull reduces the postpartum interval of releases the androgen-dependent pheromone anovulation by causing cows to produce larger DFs into the environment after it has been excreted. that are capable of ovulating sooner than cows not This pheromone(s) is then sensed by the cow by exposed to bulls. It is possible that a component of binding to odorant-binding protein (OBP) in the biostimulatory mechanism for accelerating the the nasal mucosa. The pheromone–OBP com- resumption of ovulatory activity in postpartum, plex excites odorant receptor neurons in the anovular, suckled cows intimately involves activa- main olfactory epithelium or vomeronasal organ, tion of the HPO axis by producing larger DFs cap- which stimulates mitral tufted cells in either the able of producing LH receptors allowing them to main olfactory bulb or accessory olfactory bulb. secure LH dependence sooner and ovulate earlier Depending on which bulb is stimulated, the signal under appropriate endocrine signals. is transmitted through the vomeronasal or lateral olfactory tracts, which stimulate the medial or STREAMS 1: PADDLING TO THE BANK cortical amygdala, respectively. It is within these central nervous system structures that perception So where does this leave us? After 33 yr in this occurs by interacting with hypothalamic, hip- “stream,” I concluded that the response of anovu- pocampal, and cortical centers that interpret the lar, primiparous cows to the biostimulatory effect of strength, duration, etc., of the pheromonal signal. bulls may be depended on the intensity of exposure Perception of the pheromone stimulates HPO ac- (frequency of exposure, duration of exposure, and tivity by influencing HPA function. Cows per - quantity of stimuli) of pheromonal stimuli produced ceive pheromones when they are within less than by bulls. On the basis of the results and interpret- 6 to 8 m of bulls or excretory products of bulls. ation from the literature in other species, and the Perception of pheromones leads to stimulation of results of this stream of research, it is obvious that pheromonal sensory systems of cows above some the physiological mechanisms responsible for regu- yet unknown threshold. As time after calving in- lating this process are extraordinarily complex and creases, the threshold for perception and sensory very much dependent on conditions that influence the pathways decrease. Each stimulation period is fol- mode of transmission of pheromonal signals between lowed by a period of relaxation, and cows respond bulls and cows. In the following narrative, I will try to this stimulation sooner as the duration of daily to summarize my proposed model of this complex stimulation and relaxation cycles increase. The re- sult is an increase in the frequency of LH pulses FRLA RLA that is facilitated by activation of the HPA axis. This change in frequency of LH pulses stimulates growth and maturation of a DF, which leads to the preovulatory increase in secretion of estradiol 14 a from the DF and the preovulatory release of LH. a The LH surge causes ovulation of the DF and formation of a functional corpus luteum, i.e., re- -3 -2 -1 sumption of ovarian cycling activity. Wave Number before RLA Figure 8. Least squares means for the maximum dominant follicular (MDF) diameter in mm, three follicular waves before the resumption FEET ON DRY LAND: THE END OF THE of luteal activity (RLA) for cows exposed to bulls that RLA during JOURNEY the 45-d exposure period and those cows exposed to bulls that failed to RLA (FRLA) during the exposure period and were assigned the end of Thoughts on the Evolutionary Significance of the the exposure period as their RLA date. The vertical bars represent the Biostimulatory Effect of Bulls. Why did this arise pooled SEM. Means among time points lacking a common superscript are different (P < 0.05). evolutionarily? I believe that the biostimulatory Translate basic science to industry innovation Follicular diameter, mm Streams of a career in research 1625 Figure 9. Conceptual model of hypothetical physiological model by which bulls accelerate resumption of ovarian cycling activity in prim- iparous, postpartum, anovulatory, suckled cows. HPA, hypothalamic–pituitary–adrenal; HPO, hypothalamus–pituitary–ovarian; MOB, main ol- factory bulb; MOE, main olfactory epithelium; MT, mitral tufted; MUP major urinary protein; OBP, odorant-binding protein; ORN, odorant receptor neurons; VNO, vomeronasal organ. effect of bulls is a “failsafe system” for whenever milieu is insufficient to develop the system that re- major internal and environmental effects begin to sponds to the biostimulatory effect of bulls or gen- limit breeding activity in anestrous, postpartum etic controls are not switched on to allow for the cows. Cows and bulls synchronize the breeding sys- development of this system. On the other hand, if tem around a time of the year when survival of the internal and external conditions are optimized (i.e., cow and calf is optimum. Cows have a long period growth rate and the promise of continued nutri- of gestation. If postpartum anestrous is extended ents in the environment), then the internal milieu by major factor limitations, then they will fail to and (or) genetic controls switch on the pheromonal get bred in the breeding season and lose this year systems necessary for heifers to respond to bulls. to reproduce. Furthermore, if cows are bred late in Thus, heifers and cows can show such disparate the breeding season then cows will calve and raise a (variation) responses to the biostimulatory effect of calf under less than optimal environmental condi- bulls. Nevertheless, in my opinion, the biostimula- tions the next year. Cows gain the ability to respond tory effect of bulls ensures sustainable and efficient to the biostimulatory effect of bulls after the peak reproductive performance of anovulatory females in lactation and once calves begin to fend for them- under changing environment conditions, which of selves. If conditions are limiting, i.e., nutrition or course leads to optimum survival of the species. other stress, then these cows become more sensitive To end, I would like to say that this was a won- to biostimulatory effect of bulls earlier after calving. derful journey, this career of mine, that had at its I think that it is a “redundant system” to ensure that foundation love of family and science, and a dedi- as many females will be bred and calve in the next cation and commitment to always “endeavor to season as possible. So, what about heifers, why do persevere.” Remember this is a stream of research, they show this? But not all do. If major factors are as such, this never ends! limiting, then heifers do not respond to bull (i.e., Conflict of interest statement . None declared. decreased growth rate)—the internal hormonal Translate basic science to industry innovation 1626 Berardinelli restoration of reproductive activity in aging rats. Life Sci. LITERATURE CITED 74:3285–3290. doi:10.1016/j.lfs.2003.11.015. Baruah, K. K., and L. N. Kanchev. 1993. Hormonal response Peng, M. W. 2010. Research streams. http://www.utdallas. to olfactory stimulation with bull urine in postpartum edu/~mikepeng/documents/CV201101_ResearchStream. dairy cows. Proc. VII World Conf. Anim. Prod. 3:356–361. pdf. Accessed May 8, 2019. Berardinelli, J. G., R. L. Fogwell, and E. K. Inskeep. 1978. Rekwot, P. I., D. Ogwu, E. O. Oyedipe, and V. O. Sekoni. 2001. Effect of electrical stimulation or presence of a bull on The role of pheromones and biostimulation in animal re- puberty in beef heifers. Theriogenology 9:133–141. production. Anim. Reprod. Sci. 65:157–170. doi:10.1016/ doi:10.1016/0093-691X(78)90144-9. S0378-4320(00)00223-2. Berardinelli, J. G., and P . S. Joshi. 2005. Initiation of postpartum Roberson, M. S., R. P. Ansotegui, J. G. Berardinelli, R. W. luteal function in primiparous restricted-suckled beef cows Whitman, and M. J. McInerney. 1987. Influence of biostimu- exposed to a bull or excretory products of bulls or cows. lation by mature bulls on occurrence of puberty in beef heifers. J. Anim. Sci. 83:2495–2500. doi:10.2527/2005.83112495x. J. Anim. Sci. 64:1601–1605. doi:10.2527/jas1987.6461601x. Berardinelli, J. G., J. R. Olsen, J. R. C. Wilkinson, and S. A. Tauck, S. A. 2008. The biostimulatory effect of bulls on hypo- Tauck. 2010. Influence of daily bull urine exposure on thalamic-pituitary-adrenal and ovarian axes and on tem- resumption of luteal activity in postpartum, anovular, poral aspects of resumption of ovarian cycling activity suckled cows. Biol. Repro. 83(Suppl. 1):296. doi:10.1093/ in primiparous, postpartum, suckled, beef cows [PhD biolreprod/83.s1.296. dissertation]. Bozeman (MT): Montana State University. Berardinelli, J. G., and S. A. Tauck. 2007. Intensity of the https://scholarworks.montana.edu/xmlui/handle/1/2396. biostimulatory effect of bulls on resumption of ovulatory Tauck, S. A., J. G. Berardinelli, T. W. Geary, and N. J. Johnson. activity in primiparous, suckled, beef cows. Anim. Reprod. 2006. Resumption of postpartum luteal function of prim- Sci. 99:24–33. doi:10.1016/j.anireprosci.2006.03.019. iparous, suckled beef cows exposed continuously to bull Cambridge Academic Content Dictionary. 2019. Definition urine. J. Anim. Sci. 84:2708–2713. doi:10.2527/jas.2006-181. of “research.” Cambridge (UK): Cambridge University Tauck, S. A., J. R. Olsen, and J. G. Berardinelli. 2007. Adrenal Press. https://dictionary.cambridge.org/us/dictionary/eng- involvement in the biostimulatory effect of bulls. Reprod. lish/research. Accessed May 4, 2019. Biol. Endocrinol. 5:33. doi:10.1186/1477-7827-5-33. Chenoweth, P. J. 1983. Reproductive management procedures Tauck, S. A., J. R. Olsen, J. R. Wilkinson, and J. G. Berardinelli. in control of breeding. Anim. Prod. Aust. 15:28–35. 2010a. Duration of daily bull exposure on resumption of Custer, E. E., J. G. Berardinelli, R. E. Short, M. Wehrman, and ovulatory activity in postpartum, primiparous, suckled, R. Adair. 1990. Postpartum interval to estrus and patterns beef cows. Anim. Reprod. Sci. 118:13–18. doi:10.1016/j. of LH and progesterone in first-calf suckled beef cows ex- anireprosci.2009.06.010. posed to mature bulls. J. Anim. Sci. 68:1370–1377. doi:10. Tauck, S. A., J. R. Olsen, J. R. Wilkinson, R. J. Wedlake, K. 2527/1990.6851370x. C. Davis, and J. G. Berardinelli. 2010b. Characteristics of Fernandez, D., J. G. Berardinelli, R. E. Short, and R. Adair. temporal patterns of cortisol and luteinizing hormone in 1993. Temporal requirement for the presence of mature primiparous, postpartum, anovular, suckled, beef cows bulls to alter the postpartum period to resumption of exposed acutely to bulls. Reprod. Biol. Endocrinol. 8:89. ovarian cycling activity and reproductive performance in doi:10.1186/1477-7827-8-89. first-calf suckled beef cows. Theriogenology 39:411–419. Wilkinson, J. R. C. 2009. The biostimulatory effect of bulls on doi:10.1016/0093-691X(93)90384-H. postpartum follicular wave development in, postpartum, Fernandez, D. L., J. G. Berardinelli, R. E. Short, and R. Adair. anestrous, suckled beef cows [master’s thesis]. Bozeman 1996. Acute and chronic changes in luteinizing hormone (MT): Montana State University. https://scholarworks. secretion and postpartum interval to estrus in first-calf montana.edu/xmlui/handle/1/2543. Accessed June 6, 2019. suckled beef cows exposed continuously or intermittently Zalesky, D. D., M. L. Day, M. Garcia-Winder, K. Imakawa, to mature bulls. J. Anim. Sci. 74:1098–1103. doi:10.2527/ R. J. Kittok, M. J. D’Occhio, and J. E. Kinder. 1984. 1996.7451098x. Influence of exposure to bulls on resumption of estrous Mora, O. A., and J. E. Sánchez-Criado. 2004. Involvement cycles following parturition in beef cows. J. Anim. Sci. of the corticoadrenal hormones in the pheromonal 59:1135–1139. doi:10.2527/jas1984.5951135x Translate basic science to industry innovation http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Translational Animal Science Oxford University Press

Streams of a career in research: “It was a wonderful journey, this career of mine”

Berardinelli, James G
Translational Animal Science , Volume 3 (Supplement_1): 10 – Dec 16, 2019
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© The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science.
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10.1093/tas/txz105
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James G. Berardinelli Department of Animal and Range Sciences, Montana State University, Bozeman, MT 599717 © The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which per- mits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Transl. Anim. Sci. 2019.3:1617–1626 doi: 10.1093/tas/txz105 cows; 3) fertility of heifers and postpartum cows STREAMS OF A CAREER exposed to bulls during estrous synchronization The first question a reader might ask is, “what protocols that incorporate a controlled internal does he mean by streams of research?” Well, a drug-releasing device; and, 4) developing the use research stream may be defined as a series of re- of nuclear magnetic resonant spectroscopy of lated experiments or articles on one topic, each small molecular weight metabolites to identify progressing to dig deeper, especially to discover critical interactions of metabolites and metabolic new or unique information or to reach a new or hormones involved with reproductive endocrine more profound understanding: the best stream function, disease, and behavior of domestic and is programmatic and systematic, progressing wild ruminant species. There were many other from a hypothesis or conceptual mechanism, to “streamlets” in my career that were exceptionally fundamental, quantitative research. Ultimately, interesting and productive; however, I do not have this stream may lead to an application. A vi- the space to discuss these topics in this article. brant stream does not end [adapted from Peng The following narrative represents the chron- (2010) and the Cambridge Academic Content icles of “STREAM 1,” namely, the biostimula- Dictionary (2019)]. I hope this is made clear to the tory effect of bulls on postpartum, primiparous, reader by the end of this monograph. anovular, suckled beef cows. The long-term goal This journey is based on the premise/assump- of “Stream 1” was to determine the physiological tion that by understanding the variation in bio- mechanism(s) and pheromonal pathways by logical processes, we might be able to discover the which the biostimulatory effect of bulls acceler- underlying biological mechanisms that will allow ates the reproductive neuroendocrine–endocrine us to improve the efficiency and sustainability of cascade that culminates in resumption of ovula- the biological system that we are studying, espe- tory cycles in postpartum, anovulatory, suckled cially for economically important species. The cows. My hope was to develop technologies based major streams of research in my career included 1) upon the fundamental mechanism(s) involved physiological mechanism(s) whereby the biostim- with the biostimulatory effect of bulls that would ulatory effect of bulls accelerates resumption of increase reproductive efficiency of cow–calf op- cycling activity and improves fertility in heifers erations by providing management strategies that and in primiparous, postpartum, suckled beef were low cost, were time and labor saving, yielded cows; 2) factors that influence fertility at puberty consistent results and returns, and were easily ap- in heifers and ewe lambs, and at the resumption plicable, socially acceptable, and sustainable. of ovulatory cycles in postpartum, suckled beef STREAM 1: PUTTING IN (1974 TO 1979) Corresponding author: jgb@montana.edu Received June 6, 2019. As a young M.S. student in 1974, under Accepted July 25, 2019. the supervision of Dr. E. K. Inskeep, I got my 1617 1618 Berardinelli introduction to phenomenon of “biostimulation,” Technical Committee, W112, especially Drs. Ron although this word had yet to be coined in the Randall, Bob Short, Bob Staigmiller, Bob Bellows, literature. The term “biostimulation” originally Terry Nett, and Dennis Hallford. And, there are appeared in the literature in 1983 to refer to any many more collaborators on this committee that I stimulatory effect of a male on estrus and ovula- lack the space to mention but I would like to thank. tion in females through genital stimulation, prim- They were a tremendous resource and an invaluable ing pheromones, or other less defined external cues. network over the past 37 years. However, there are cases where females may have So, my “paddling” continued with one of the a biostimulatory effect on males or on other con- objectives of the W112 at the time, which was to specific females; thus, this term is not mutually ex- determine those factors that limit reproductive per- clusive for a given sex in mammals (Chenoweth, formance of beef heifers and postpartum, anestrous 1983). One could say that most of my career cen- cows. My first attempt at WVU to use mature bulls tered around this “biostimulatory effect” of males to accelerate the onset of puberty in heifers proved on anestrous or anovular females. disheartening; however, I reasoned that those By this time, it was known that the presence of negative results might have been caused by small an adult male reduced the age at puberty in female numbers of heifers and limited exposure periods. mice and gilts, and hastened the onset of the breeding Perhaps, heifers needed to be exposed to bulls for season in sheep and goats (for review, see Rekwot et longer than 30 d. Dr. Mark Roberson, then an MS al., 2001). So, we (actually, Dr. Inskeep) asked the student, and I tested this hypothesis by starting question, does the presence of a mature bull for 21 d bull exposure at 200 d of age on 100 prepubertal accelerate age at puberty in beef heifers? The answer heifers. Again, we found that bull exposure of beef to this question was NO, the presence of a bull, under heifers for 152 d did not accelerate age at puberty these conditions, did not influence age at puberty in (Roberson et al., 1987). We concluded that bull ex- beef heifers (Berardinelli et al., 1978). We then asked, posure of prepubertal beef heifers to long-term ex- if we “primed” heifers with progesterone (P4) and posure of bulls did not influence the occurrence of increased the exposure period to 30 d, would com- puberty under these conditions. Another “tip of the bining this treatment with the presence of bulls accel- canoe.” However, as we will see in the discussion of erate age at puberty in prepubertal heifers? Again, the postpartum, anovular cows, conditions matter! answer was NO; this combination did not appear to While I was working on the effect of bull on accelerate age at puberty in heifers (Berardinelli et al., heifers, I read an article from Nebraska indicating 1978). Thus, my first experience with biostimulation that resumption of estrous cycles was advanced by was certainly not positive. But I had learned much exposing mature, multiparous cows to bulls during about how to do science, gained vital experience in the early postpartum period (Zalesky et al., 1984). learning field and laboratory techniques, under - Ah, here is a case where a clear biostimulatory ef- standing the value of statistics, and learning how to fect occurs in cattle. As I dug into the literature, I write in a scientific manner during this 5-yr period at failed to find a single article regarding effects of bull West Virginia University (WVU). I was learning how exposure on primiparous suckled, anovular beef to paddle a canoe. cows, and Zalesky et al. (1984) made no mention of the physiological mechanisms by which bulls might influence postpartum reproductive function of STREAM 1: INTO THE MAIN CHANNEL suckled cows. Luckily, and thanks to Dr. Richard (1981 TO 2001) (Butch) Whitman, there was a management change I began my academic career by joining the fac- in 1985 involving first-calf cows in our herd. They ulty of Montana State University in the Department would now be housed and maintained on the farm of Animal and Range Sciences in 1981 as an as- in Bozeman. This was vitally important for it al- sistant professor. This required me to develop a lowed me direct and easy access to this type of cow, modern laboratory (for the time) from scratch and and with some effort, I could manipulate the facil- establish a research program in reproductive physi- ities to isolate groups of cows and bulls from one ology and endocrinology. These were no easy tasks another. In hindsight, it was like I could stop “pad- at the time. However, I had a very good mentor dling” and use a motor on this journey. and collaborator in Dr. Peter Burfening, whom I Our first experiment involved exposing first- thank for all his support and encouragement dur- calf, suckled cows to bulls continuously, starting 3 ing my career. As important as he was in shaping d after calving to determine whether this type of my career were the members of the Western Section exposure would alter postpartum interval to estrus, Translate basic science to industry innovation Streams of a career in research 1619 and patterns of luteinizing hormone (LH) con- 15-min intervals every third day for 18 d. Sampling centrations. More importantly, we thought to get from BEI cows began 2 h before introduction of a a glimpse of a mechanism by taking serial, 15-min bull every other day. We found that mean LH and blood samples for 6 h at weekly intervals starting LH pulse frequency increased within the 6-h sam- 10 d after initial exposure of cows to bulls for assay pling period in both NEBE and BEI cows to bulls of LH. Our hypothesis was that characteristics of compared to NE cows. Surprisingly, even though pulsatile patterns of LH would increase sooner in LH pulse frequency increased with intermittent cows exposed to bulls (BE) than in cows not ex- 2-h exposure every third day, these cows did not re- posed to bulls (NE). Results of two trials clearly spond to the biostimulatory effect, i.e., interval to demonstrated that the presence of bulls accelerated resumption of ovulatory activity did not occur any resumption of ovulatory cycles in primiparous, sooner than that in NE cows. suckled beef cows. However, characteristics of LH On the basis of these data and the hypoth- patterns in weekly sample did not indicate that the esis that increased LH secretion plays a significant presence of bulls altered temporal pattern of LH role in the resumption of ovarian cycling activity, (Custer et al., 1990). This result did not seem to one might conclude that bulls effect a reduction in fit the consensus hypothesis that in order to accel- postpartum interval to ovulation by increasing LH erate resumption of ovulatory cycles in anovular secretion acutely and chronically after exposure. females, any stimulus(i) should affect the hypothal- However, cows that were intermittently exposed amic–pituitary axis to increase GnRH and in turn to bulls did not exhibit estrus and ovulation any increase pulse frequency of LH, which stimulates sooner than cows isolated from bulls. One interpret- final stages of follicular development, estradiol in- ation of these results is that immediate exposure to crease, and ovulation. Perhaps the timing of sam- bulls induces a pheromonally activated trigger (sig- pling was insufficient to determine if the presence naling type) that induces a hypothalamic release of of bulls altered this axis and LH patterns. GnRH and subsequent acute release of LH, specif- At this point, we thought two important issues ically an increase in pulse frequency. However, this had to be addressed to gain some insight into this type of stimulation (conditions) does not result in physiological mechanism. The first was whether cows the induction of ovarian cycling activity. We pos- needed to be exposed continuously to bulls “soon” tulated that there must either be exteroceptive cues after calving to obtain a biostimulatory response, and other than pheromones or that there is some type the second was whether continuous, 24-h exposure, of “re-enforcement mechanism” associated directly was required to elicit a biostimulatory response. Dr. with the physical presence of the bull involved in Dave Fernandez was a graduate student of mine at the biostimulatory effect of bulls on postpartum the time that tackled these difficult issues. First, we cows (Fernandez et al., 1996). This was a dilemma exposed of primiparous, suckled beef cows to mature that needed attention in order to understand this bulls in the first 30 days after calving (BE/NE), ex- mechanism. posed them beginning 30 d after calving (NE/BE), or Before we tackled this dilemma and to gain a exposed them continuously starting 3 d after calving more profound understanding of the biostimu- (BE). We found that postpartum intervals to resump- latory effect of bulls it was vital to precisely nail tion of ovarian cyclic activity did not differ among down the temporal development of the response of BE, BE/NE, and NE/BE cows, but they were 15.4 d postpartum anovular cows to the biostimulatory ef- shorter than for NE cows (Fernandez et al., 1993). fect of bulls. The question to be answered was are We now knew that we could obtain a biostimulatory primiparous, anovular, suckled cows more sensitive effect of bulls by exposing cows continuously 30 d to the biostimulatory effect of bulls when exposure after calving that was the same as continuous ex- to bulls occurs at progressively longer intervals posure beginning 3 d after calving. after calving? To answer this question, we exposed We then exposed cows to a bull initially on day primiparous, anovular, suckled cows to bulls at 15, 30 after calving (NEBE), exposed cows to a bull for 35, or 55 d after calving. Evaluation of the cumu- 2 h every third day beginning on day 30 after calving lative 10-d distribution of percentages of cows that (intermittent exposure; BEI), or did not expose resumed ovulatory activity among cows exposed to cows to a bull (NE). More importantly, this design bulls beginning 15, 35, and 55 d after calving indi- gave us the opportunity to collect serial blood sam- cated that cows become responsive to the biostimu- ples from cows to evaluate temporal LH patterns latory effect of bulls about 35 to 40 d after calving acutely and chronically after exposing cows to bull. and sensitivity increases as time after calving in- Blood samples were obtained over a 6-h period at creases (Fig. 1; Berardinelli and Joshi, 2005). Translate basic science to industry innovation 1620 Berardinelli BE15 NE15 80 BE35 NE35 BE55 NE55 Insensitive period Sensitive period 0-10 11-20 21-30 31-40 41-50 51-60 Days after calving Interval (d) Figure 2. Relative hypothetical sensitivity of primiparous, anovu- Figure 1. Cumulative percentages of primiparous, suckled beef lar, suckled beef cows to the biostimulatory effect (BSE) of bulls after cows exposed to presence of a bull (BE) or not exposed to a bull (NE) calving (day 0). on either days 15, 35, or 55 after calving that resumed ovarian cycling activity. Interaction Χ = 18.6, df = 10; P < 0.05. This was an important finding that impacts the Please note that we think that insensitive to sen- effectiveness of the biostimulatory effect of bulls dur- sitive periods can slide left or right depending on ing early postpartum anestrus of cows. We would the influences of other major factors that affect the have recognized this earlier if I would have examined length of postpartum anestrus in suckled cows. the differential in intervals to resumption of ovula- Around 2000, it became apparent to my labora- tory activity between cows exposed to bulls starting 3 tory that a critical feature of the biostimulatory ef- d after calving compared to cows exposed on day 30 fect of bulls was missing, that was, what might it after calving (Fernandez et al., 1996). The differen- be and what is its source? We and most investiga- tial was much shorter for cows exposed beginning on tors at the time assumed or speculated that bulls day 30 after calving than for cows exposed 3 d after produce a primer pheromone that acts via an ol- calving! Nevertheless, the question then became what factory pathway to evoke this response (for review, is it about those first 35 d after calving that dampens see Rekwot et al., 2001). Thus, we investigated the or attenuates the biostimulatory effect of bulls? hypothesis that the biostimulatory effect of bulls is The answer to this question may be the fol- mediated by exteroceptive stimuli of bulls in a series lowing. This corresponds to the period during of three experiments. The first experiment tested which inhibitory influences on LH secretion, such the hypothesis that exposing postpartum, anovular as increased sensitivity to the negative feedback of suckled cows to excretory products of bull for 12 estradiol, the maternal cow–calf bond, and lacta- h daily would evoke the same biostimulatory re- tional stimuli are still very high. Possible explan- sponse as continuously exposing cows to the phys- ations for this observation are either there is no ical presence of bulls. Indeed, we found that interval pheromonal mechanism in cows during this period to resumption of ovulatory activity and the propor- to respond to bulls and they developed them espe- tions of cows that resumed ovulatory activity were cially for this time in their reproductive life cycle shorter and greater, respectively, for cows exposed (not likely), or the pheromonal mechanism is pres- to a bull continuously or cows exposed to the ex- ent but the negative effects that suppress LH release cretory products of bulls for 12 h daily compared have the same inhibitory effect on the pheromonal with those metrics of cows not exposed to a bull or system that mediates the biostimulatory effects of excretory products of bulls. More importantly, the bulls (highly likely). If the latter is the case, then the temporal responses for the proportions of cows cyc- apparent “insensitive period” is related to the inten- ling at 10-d intervals after exposure to a bull or the sity of stimulation. Increasing the “intensity” (dose excretory products of bulls were identical (Fig. 3; or duration of exposure) should induce a response Berardinelli and Joshi, 2005). to the biostimulatory effect of bulls. If the former These data clearly indicate that excretory prod- is true, then no level of intensity of bull biostimula- ucts (urine, feces, or mucus/saliva) of bulls hastened tion will evoke a response. Nevertheless, cows begin the resumption of ovulatory activity in postpartum, to become responsive to the biostimulatory effect anovular, suckled cows. Therefore, the biostim- of bulls about 35 to 40 d after calving, and it ap- ulatory mechanism appears to be mediated by a pears that sensitivity increases as time after calving pheromone(s) present in their excretory products increases (Berardinelli and Joshi, 2005). An illustra- and does not appear to be reenforced by the phys- tion of this conceptualization in presented in Fig. 2. ical presence of bulls. This was an extraordinary Translate basic science to industry innovation Cumulative % Relative sensitivity to BSE Streams of a career in research 1621 Figure 3. Cumulative percentages of first-calf restricted suckled Figure 4. Percentages of first-calf suckled cows exposed to ma- beef cows exposed continuously to presence of a bull (BE), exposed ture bull urine (BUE) or exposed to steer urine (SUE) that resumed to excretory products of bulls (EPB), not exposed to a bull (NE), or ovarian cycling activity by the beginning of the estrus synchronization exposed to excretory products of cows (EPC) that resumed ovarian protocol. Bars with common letters do not differ, P = 0.25, X = 1.3, cycling activity in 10-d intervals from day 0 to end of the experiment. df = 1. The blue-shaded area represents points that do not differ (P > 0.10) among BE, EPB, and EPC cows. activity (Berardinelli et al., 2010). We concluded discovery at the time. But, could we nail down a that continuous or 12-h exposure of postpartum, specific excretory product that would be a major anovular, suckled cows to bull urine does not carrier for such a pheromone? allow for a pheromonally induced activation of Perhaps we could as Baruah and Kanchev the hypothalamus–pituitary–ovarian (HPO) axis (1993) reported that bull urine sprayed into the to stimulate the cascade resulting in resumption of nasal passages of dairy cows 7 d after calving in- ovulatory activity. creased systemic LH and follicle stimulating hor- However, these results do not preclude the pos- mone concentrations within 70 min of exposure, sibility that bull urine contains a biostimulatory and we knew that other reproductively active pheromone(s), but may indicate that the “mode” pheromones in mammals are carried in urine. We (frequency, amplitude, duration) of pheromonal asked the question: does exposing cows to mature stimulation may be an important factor that deter- bull urine mimic the biostimulatory effect of bulls mines the biostimulatory effect of bulls on resump- to reduce the postpartum interval to ovulatory ac- tion of luteal activity in postpartum, suckled beef tivity in primiparous, anovular suckled cows? In an cows. Too much for too long each day may “desen- elegant experiment by Tauck et al. (2006), we tested sitize” or overly stress the HPO axis, whereas too the hypothesis that continuous exposure (24 h) of little or too short a duration of exposure may be cows to bull urine would accelerate resumption of insufficient to be recognized as stimuli to generate ovulatory activity. Urine from bulls and steers was a response by the HPO axis of primiparous, anovu- delivered continuously to cows by means of an in- lar, suckled cows. genious, controlled urine deliver device. We found That this might be the case can be inferred from that interval from urine exposure and proportions an experiment involving fenceline contact between of cows that resumed ovulatory activity did not bulls and cows. We found that exposing cows to differ between BUE- and SUE-exposed cows after direct fenceline contact (BEFL) with bulls penned 64 d of exposure (Fig. 4). This was a disconcerting within their pen accelerated resumption of ovula- result. However, we reasoned that perhaps 24-h ex- tory activity compared with cows not exposed to posure of cows to bull urine, under these conditions bulls (NE). However, the biostimulatory response (again, conditions) in some manner, actually “de- of cows exposed to fenceline contact was not as dra- sensitized,” downregulated, or otherwise stressed matic as that for cows exposed to the physical pres- the physiological system(s) that sense and perceive ence of bulls (Fig. 5; Berardinelli and Tauck, 2007). a urinary pheromone by cows. To test whether this Although these data indicate qualitatively that might be the case, we exposed primiparous suckled intensity of the biostimulatory effect of bulls is an cows to mature bull urine or saline by constant drip important factor to consider in this effect, they did for 12-h daily onto straw-bedding, and then placed not yield insight regarding the quantity and dur- cows into these areas for 12-h daily. Again, 12-h ation of exposure necessary to evoke a response. As exposure to straw-bedding containing bull urine I stated previously, these are critical variables that did not affect interval to resumption of ovulatory we had yet to measure. Nevertheless, we think that Translate basic science to industry innovation 1622 Berardinelli Figure 6. Linear regression of interval from the start of bull ex- posure (D 0) to resumption of ovulatory activity on hours of daily ex- Figure 5. Cumulative frequency distribution of the percentages of posure for primiparous, postpartum, anovular, suckled cows exposed primiparous, anovular cows exposed to close physical contact with ma- to bulls for 0, 6, or 12 h. Y-intercept (b0) = 42.2 d; slope (b1) = 1.01 d/h ture bulls (BE) or not exposed to bulls (NE) for 35 d and exposed to (P < 0.05); R = 0.18. fenceline contact with bulls (BEFL) or not exposed to bulls (NE) for 42 d. collectively, these data indicated that there is a min- Integrating the results of our “stream of re- imum and maximum intensity to the pheromonally search” to this point, we developed the concept that mediated effect of bulls, if the pheromone is carried cows respond to bull-pheromonal “stimulation and by urine. relaxation cycles” in a dose-dependent manner. This The next critical question that we asked was does type of cyclic presentation of stimuli may be a critical the response of cows to the biostimulatory effect of component of the pheromonal mechanisms by which bulls involve a duration of exposure component? the biostimulatory effect of bulls accelerates resump- Fernandez et al. (1996) reported that interval from tion of ovulatory activity. However, it appeared to calving to resumption of ovulatory activity was not us, that in some way, there was some type of reen- accelerated in cows exposed to bulls for 2 h every third forcement mechanism or agent related to dosage, in- day for 18 d beginning 33 d after calving. However, tensity, and duration of the mechanism involved a length of postpartum anestrus was reduced in cows pheromonally mediated biostimulatory effect of bull. exposed to the excretory products of bulls for 12 h This idea led us to the following question: what daily (Berardinelli and Joshi, 2005). With these re- physiological factor(s) might act as a “triggering” sults in mind, we tested the hypothesis that duration and (or) “re-enforcing” agent for the putative phero- of bull exposure and interval to resumption of ovula- monal mechanism to stimulate resumption of ovu- tory activity ovulatory in primiparous, anovular, suck- latory activity? In rodents, there appeared to be a led cows exposed to bulls for 0, 6, or 12 h daily would clear functional relationship between the hypothal- progressively accelerate resumption of ovulatory ac- amic–pituitary–adrenal (HPA) axis and induced tivity in anovular, suckled primiparous cows. Indeed, pheromonal activation or inhibition of female re- the results of this experiment showed that the number productive events (Mora and Sánchez-Criado, of hours of daily bull exposure required to accelerate 2004). Might there be the same relationship in the resumption of ovulatory in postpartum, anovular, bovine? To answer this question, we evaluated cor- suckled cows decreases in a linear manner (Tauck tisol concentrations in blood samples obtained at et al., 2010a; Fig. 6). Thus, the duration of bull-pher- 3-d intervals from cows exposed continuously to omone stimuli that cows perceive each day is related bull urine (BUE) and cows exposed to the physical to how soon after exposure primiparous, postpartum, presence of bulls (BE) starting 35 d after calving anestrous, suckled cows respond to this stimulus and (Tauck et al., 2007). Remember, interval to resump- undergo the physiological changes necessary to re- tion of ovulatory activity for BUE cows did not sume ovulatory activity. The dose-dependent manner differ from that in SUE cows, but BE cows resumed by which pheromones produced by bulls accelerated cycling much sooner that NE cows (Tauck et al., resumption of ovulatory activity in postpartum, ano- 2007). Surprisingly, systemic cortisol concentra- vular, suckled cows may explain disparate reports in tions in BE cows increased significantly within 9 d the literature concerning fenceline contact and inter- after exposure, and the difference in cortisol concen- mittent exposure of cows to bulls. trations was maintained throughout the exposure Translate basic science to industry innovation Streams of a career in research 1623 period compared to those of NE cows, and all BE characteristics of temporal patterns of both LH cows resumed cycling activity! In contrast to these and cortisol by increasing LH pulse frequency and results, cortisol concentrations in BUE cows clearly decreasing cortisol pulse frequency. Interestingly, follow the same temporal pattern as that of SUE in cows exposed to bulls, as amplitude and fre- cows over the exposure period, and BUE cows had quency of cortisol pulses decreased, amplitudes of the same interval to resumption of ovulatory ac- LH pulses increased, and frequency of LH pulses tivity as SUE cows. We suggested that these data tended to increase (Tauck et al., 2010b). Thus, the indicated a strong possibility that activation of the physiological mechanism of the biostimulatory ef- HPA axis might be intimately, but subtlety, involved fect of bulls may initially involve modification of with the pheromonally mediated biostimulatory ef- the HPA axis, and these changes may facilitate ac- fect of bull (Tauck et al., 2007). tivation of the HPO axis and resumption of ovula- To gain insight into this possibility, we evalu- tory cycles in postpartum, anovular, suckled cows ated characteristics of temporal patterns of cortisol (Tauck, 2008). Our interpretations of these results and LH in postpartum, anovular, suckled beef cows are graphically presented in Fig. 7. after acute exposure to bulls. Our hypothesis was Finally, in this stream, there is “the rest of the that acute exposure of cows to bulls for 5 h daily story.” For resumption of ovulatory activity to occur over a 9-d period would increase cortisol concen- in postpartum, anovular suckled cows, changes in trations, and in turn, increase mean and frequency LH pulse frequency related to ovarian follicular of LH concentrations like that which would trigger development, maturation of dominant follicles the neuroendocrine–endocrine ovulatory cascade. (DFs), and ovulation are required. Therefore, it was We reported that exposing postpartum, anovu- reasonable to postulate that as the physical pres- lar, suckled cows to bull in this manner altered ence of bulls to cows increases pulse frequency of Effect of Anestrous Factors Effect of Pheromones of Bulls (Cow-calf bond, lactation, nutrition, Frequency Duration Smoothness etc.) 7 7 5 5 4 4 1 1 060120 180240 300360 060120 180240 300360 Time, min Time, min Cortisol on LH secretion Cortisol on LH secretion LH pulse frequency 1.5 1.5 1 1 0.5 0.5 0 0 060120 180240 300360 060120 180240 300360 Time, min Time, min Figure 7. Graphic representation of the effect of factors that influence length of postpartum anestrus and the biostimulatory effect of bulls on the hypothalamic–pituitary–adrenal axis of postpartum, anovulatory, suckled beef cows. Translate basic science to industry innovation LH, ng/mL Cortisol, ng/mL LH, ng/mL Cortisol, ng/mL 1624 Berardinelli LH in postpartum cows, the biostimulatory effect mechanism with the following illustration (Fig. 9) and of bulls may influence follicular wave dynamics of interpretation. exposed cows. Indeed, in the studies by Wilkinson Bulls produce an androgen-dependent phero- (2009), it was reported that exposing cows to bulls mone that is carried from the blood to the urine altered follicular growth and developmental pat- by major urinary protein (MUP), α-2u globulin, terns by decreasing the number of follicular waves albumin, or a combination thereof. This phero- and increasing mean follicle diameter before re- mone is excreted in urine, feces, cutaneous se- sumption of ovulatory activity (Fig. 8). We inter- cretions, or a combination of these excretory preted these results to mean that the biostimulatory products. Alpha-2u globulin, MUP, or albumin effect of the bull reduces the postpartum interval of releases the androgen-dependent pheromone anovulation by causing cows to produce larger DFs into the environment after it has been excreted. that are capable of ovulating sooner than cows not This pheromone(s) is then sensed by the cow by exposed to bulls. It is possible that a component of binding to odorant-binding protein (OBP) in the biostimulatory mechanism for accelerating the the nasal mucosa. The pheromone–OBP com- resumption of ovulatory activity in postpartum, plex excites odorant receptor neurons in the anovular, suckled cows intimately involves activa- main olfactory epithelium or vomeronasal organ, tion of the HPO axis by producing larger DFs cap- which stimulates mitral tufted cells in either the able of producing LH receptors allowing them to main olfactory bulb or accessory olfactory bulb. secure LH dependence sooner and ovulate earlier Depending on which bulb is stimulated, the signal under appropriate endocrine signals. is transmitted through the vomeronasal or lateral olfactory tracts, which stimulate the medial or STREAMS 1: PADDLING TO THE BANK cortical amygdala, respectively. It is within these central nervous system structures that perception So where does this leave us? After 33 yr in this occurs by interacting with hypothalamic, hip- “stream,” I concluded that the response of anovu- pocampal, and cortical centers that interpret the lar, primiparous cows to the biostimulatory effect of strength, duration, etc., of the pheromonal signal. bulls may be depended on the intensity of exposure Perception of the pheromone stimulates HPO ac- (frequency of exposure, duration of exposure, and tivity by influencing HPA function. Cows per - quantity of stimuli) of pheromonal stimuli produced ceive pheromones when they are within less than by bulls. On the basis of the results and interpret- 6 to 8 m of bulls or excretory products of bulls. ation from the literature in other species, and the Perception of pheromones leads to stimulation of results of this stream of research, it is obvious that pheromonal sensory systems of cows above some the physiological mechanisms responsible for regu- yet unknown threshold. As time after calving in- lating this process are extraordinarily complex and creases, the threshold for perception and sensory very much dependent on conditions that influence the pathways decrease. Each stimulation period is fol- mode of transmission of pheromonal signals between lowed by a period of relaxation, and cows respond bulls and cows. In the following narrative, I will try to this stimulation sooner as the duration of daily to summarize my proposed model of this complex stimulation and relaxation cycles increase. The re- sult is an increase in the frequency of LH pulses FRLA RLA that is facilitated by activation of the HPA axis. This change in frequency of LH pulses stimulates growth and maturation of a DF, which leads to the preovulatory increase in secretion of estradiol 14 a from the DF and the preovulatory release of LH. a The LH surge causes ovulation of the DF and formation of a functional corpus luteum, i.e., re- -3 -2 -1 sumption of ovarian cycling activity. Wave Number before RLA Figure 8. Least squares means for the maximum dominant follicular (MDF) diameter in mm, three follicular waves before the resumption FEET ON DRY LAND: THE END OF THE of luteal activity (RLA) for cows exposed to bulls that RLA during JOURNEY the 45-d exposure period and those cows exposed to bulls that failed to RLA (FRLA) during the exposure period and were assigned the end of Thoughts on the Evolutionary Significance of the the exposure period as their RLA date. The vertical bars represent the Biostimulatory Effect of Bulls. Why did this arise pooled SEM. Means among time points lacking a common superscript are different (P < 0.05). evolutionarily? I believe that the biostimulatory Translate basic science to industry innovation Follicular diameter, mm Streams of a career in research 1625 Figure 9. Conceptual model of hypothetical physiological model by which bulls accelerate resumption of ovarian cycling activity in prim- iparous, postpartum, anovulatory, suckled cows. HPA, hypothalamic–pituitary–adrenal; HPO, hypothalamus–pituitary–ovarian; MOB, main ol- factory bulb; MOE, main olfactory epithelium; MT, mitral tufted; MUP major urinary protein; OBP, odorant-binding protein; ORN, odorant receptor neurons; VNO, vomeronasal organ. effect of bulls is a “failsafe system” for whenever milieu is insufficient to develop the system that re- major internal and environmental effects begin to sponds to the biostimulatory effect of bulls or gen- limit breeding activity in anestrous, postpartum etic controls are not switched on to allow for the cows. Cows and bulls synchronize the breeding sys- development of this system. On the other hand, if tem around a time of the year when survival of the internal and external conditions are optimized (i.e., cow and calf is optimum. Cows have a long period growth rate and the promise of continued nutri- of gestation. If postpartum anestrous is extended ents in the environment), then the internal milieu by major factor limitations, then they will fail to and (or) genetic controls switch on the pheromonal get bred in the breeding season and lose this year systems necessary for heifers to respond to bulls. to reproduce. Furthermore, if cows are bred late in Thus, heifers and cows can show such disparate the breeding season then cows will calve and raise a (variation) responses to the biostimulatory effect of calf under less than optimal environmental condi- bulls. Nevertheless, in my opinion, the biostimula- tions the next year. Cows gain the ability to respond tory effect of bulls ensures sustainable and efficient to the biostimulatory effect of bulls after the peak reproductive performance of anovulatory females in lactation and once calves begin to fend for them- under changing environment conditions, which of selves. If conditions are limiting, i.e., nutrition or course leads to optimum survival of the species. other stress, then these cows become more sensitive To end, I would like to say that this was a won- to biostimulatory effect of bulls earlier after calving. derful journey, this career of mine, that had at its I think that it is a “redundant system” to ensure that foundation love of family and science, and a dedi- as many females will be bred and calve in the next cation and commitment to always “endeavor to season as possible. So, what about heifers, why do persevere.” Remember this is a stream of research, they show this? But not all do. If major factors are as such, this never ends! limiting, then heifers do not respond to bull (i.e., Conflict of interest statement . None declared. decreased growth rate)—the internal hormonal Translate basic science to industry innovation 1626 Berardinelli restoration of reproductive activity in aging rats. Life Sci. LITERATURE CITED 74:3285–3290. doi:10.1016/j.lfs.2003.11.015. Baruah, K. K., and L. N. Kanchev. 1993. Hormonal response Peng, M. W. 2010. Research streams. http://www.utdallas. to olfactory stimulation with bull urine in postpartum edu/~mikepeng/documents/CV201101_ResearchStream. dairy cows. Proc. VII World Conf. Anim. Prod. 3:356–361. pdf. Accessed May 8, 2019. Berardinelli, J. G., R. L. Fogwell, and E. K. Inskeep. 1978. Rekwot, P. I., D. Ogwu, E. O. Oyedipe, and V. O. Sekoni. 2001. Effect of electrical stimulation or presence of a bull on The role of pheromones and biostimulation in animal re- puberty in beef heifers. Theriogenology 9:133–141. production. Anim. Reprod. 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Published: Dec 16, 2019

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