As I announced this morning, there will be several guest posts here over the next several weeks. The first one, by Barn Owl of the lovely Guadalupe Storm-Petrel blog, is likely to appeal to a lot of my readers as it combines several of my own interests:
In this guest-post for A Blog Around the Clock, I'll combine three things that Coturnix especially likes: horses, circadian biology, and an Open Access research paper. For the equestrian, there are two main seasonal issues, controlled primarily by photoperiod, or day length, which must be considered, especially if one shows the horse or competes in various events and games. Perhaps the most obvious seasonal changes are in the horse's coat, with shedding cycles in the spring and in the fall. In the Northern Hemisphere, the fall shedding cycle is relatively inconsequential for equestrian activities (though it is important, as always, to groom your horse frequently to remove the shed hair), but the spring shedding cycle can be a nightmare, so to speak. The horse hair permeates your saddle blankets, your riding clothes, the interior of your car, and your respiratory tract. Birds gather around eagerly when you groom your horse, to fly away with tufts of hair for their nests. One of my friends used to mark "the lying down of the grey horse" each year, i.e. the spring day on which her big flea-bitten grey gelding rolled and rubbed off much of his shed winter coat, in the form of a large "hair angel".
Although humans have selected for horse coat colors and patterns that they find attractive and interesting, the horse's coat evolved to complement the thermoregulatory functions of the other skin components. The long outer, or "guard", hairs of a horse's coat are equipped with piloerector muscles, allowing a layer of insulating air to be trapped between the raised shafts. Our winters here in South Texas are relatively mild, so we rarely need to blanket our horses for more than a day or two at a time. A light blanket is sufficient, and is a good thing to take along to early-season polocrosse tournaments, when nighttime temperatures can dip below freezing, and the horses cannot move about sufficiently in their small temporary pens to warm themselves. Even in colder climates, horses are capable of staying warm during rough weather, as long as they have plenty of fodder, some shelter from wind, rain, and ice, and can move around to generate heat. In fact, a heavy winter coat can cause a performance or show horse to sweat excessively, and so some equestrians "body clip" their equine athletes, and blanket them when they are not exercising or performing.
Seasonal hair growth and pigmentation cycles have been studied extensively in sheep, goats, mink, arctic fox, and mice, and it is clear that they are responsive to photoperiod and melatonin levels. As Coturnix has described previously in his blog, melatonin is a multifunctional lipophilic molecule, primarily produced by the pineal gland in response to noradrenergic stimulation from sympathetic neurons. Numerous brain areas have high levels of melatonin receptors, but cells in other organs, including the skin, are also responsive to melatonin. The transcription levels of genes encoding melatonin receptors appear to be correlated with the hair cycle phases of telogen (resting) and anagen (growth). Hair follicle activity and hair shaft elongation are very responsive to melatonin, with both "overcoat" and "undercoat" fur affected; these effects of melatonin on hair growth have been demonstrated in sheep, goats, mink, ferrets, dogs, and red deer (Fischer et al., 2008). The autumn and spring molt, or shedding, phases in the horse are likely to reflect changing melatonin levels, and could perhaps be modified by dietary melatonin supplements, as has been achieved in cashmere goats and merino sheep. However, another important melatonin target organ is the hypothalamus, which in turn regulates secretion of hormones by the anterior pituitary.
Of course the involvement of the anterior pituitary indicates that a second major seasonal cycle for horses is reproduction. Melatonin inhibits production of gonadotropin-releasing hormone (GnRH), which causes secretion of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) by the anterior pituitary. During the breeding season, a mare will cycle from ovulation to ovulation approximately every 21 days, and the changing levels of FSH and LH will in turn alter levels of estrogen and progesterone. A fertile mare "in season" (in estrus) will show distinctive behavior that is recognizable to every other horse, and to every horse owner as well. She will raise her tail and hold it to one side, she will squat and urinate small amounts frequently, and she will lean or rub against other horses, fences, trailers, and humans. She will be friendly and flirtatious to geldings that she normally disdains, and needless to say, this can be a very frustrating time for the geldings. I had a Thoroughbred mare who once sneaked out of a gate that was open for a split second, to make a beeline for a Quarter Horse stallion on a farm half a mile away; I caught her prancing and "showing" and trying desperately to figure out how to get into his paddock. And I currently have a Thoroughbred gelding who loves flirtatious mares of any breed, and will crawl under electobraid, or swim across stock ponds, to pay a gentlemanly visit to the ladies.
In the winter, when day length is short, most mares will enter a non-cycling phase, with an inactive reproductive tract. Lower levels of GnRH mean less FSH to induce the maturation of oocyte-containing follicles, and insufficient LH to induce ovulation. There is a transitional phase between the non-cycling (anestrus) and cycling (estrus) phases, during which the ovarian follicles will mature, but not undergo ovulation, and it is this phase that some horse breeders will attempt to manipulate with prolonged light exposure. In the US, all Thoroughbred foals, regardless of which month they are born, will have their first birthday on their first January 1. On average, gestation in the horse is 340 days, so ideally, the mare should be bred in late winter or early spring, such that her foal is delivered in January, February, or early March of the following year. This is important in the racing industry, to produce a bigger colt at a given racing age, but of course there are other reasons to alter a mare's breeding cycle, particularly if she is a show or performance horse.
The desire to manipulate equine breeding and the timing of foal delivery has led to a substantial amount of physiological research on fluctuating hormone and melatonin levels, and on light cycle responses, in horse reproduction. For a nice comparison of circadian melatonin levels, temperature, locomotor activity, and blood chemistry in the Thoroughbred mare and the Comisana ewe, see a recent paper by Piccione and colleagues; in the horse, melatonin levels peak after midnight (middle of dark phase), whereas locomotor activity peaks in the middle of the light phase. Since the late 1940s, it has been recognized that the photoperiod is the major signal (zeitgeber) that controls the timing of estrus in mares. By the 1980s, it was generally accepted that the reproductive cycle for most long-lived mammals was optimally synchronized with seasonal changes, through an interaction of the environmental photoperiod and endogenous melatonin levels. However, subsequent measurements of fluctuations in melatonin levels, in horses and in other seasonal breeders, made it clear that the model of suppression of the reproductive cycle by increased melatonin levels was overly simplistic (though the simplistic model still persists on equine information websites).
In a 1995 paper, Guerin and colleagues reported plasma melatonin levels in mixed breed mares, under conditions of natural photoperiod, and though there was a clear circadian pattern to melatonin secretion, the peak values and duration of elevated levels of this molecule did not differ significantly between seasons. The observation that about 15-20% of mares continue to cycle throughout the nonbreeding period, i.e. fail to enter the anestrus phase during the shorter day-lengths of winter, led to the identification of other signals that influence the hypothalamus-pituitary control of the breeding cycle. Fitzgerald and McManus (2000) found that this continuous reproductive activity, throughout the winter months, is much more common in mature mares, than in young mares. Continuous treatment with melatonin, through an implant under the skin, did not suppress the estrus cycle in these mature mares. Instead, energy availability, as measured by weight, percent body fat, and circulating leptin levels, seems to alter the occurrence of anestrus in mares. Moreover, mature mares that failed to undergo anestrus had similar winter month levels of melatonin, as did mares that ceased reproductive activity in response to shorter day length.
Finally, a little discussion of an Open Access paper, on a chronobiology issue that is relevant to the performance of elite equine athletes in the Olympics, and at other international venues. Of course the horse and rider must both travel to the competition site, and both are potentially subject to the fatigue, malaise, loss of appetite, and impaired concentration, characteristic of jet lag. To determine how horses might be affected by jet lag, Murphy and colleagues (2007) housed six healthy mares (mixed light horse breed), entrained to a 12 hour light/12 hour dark natural photoperiod, in a light-proofed barn. The researchers then advanced the light/dark cycle by ending the dark period six hours early, and measured both body temperature and serum melatonin levels over the next 11 days. In contrast to the melatonin rhythm in humans and other animals, the equine melatonin phase advance occurred within the first day after the light/dark cycle shift. Re-entrainment of the body temperature rhythm occurred more slowly, and was not complete until 3 days after the shift. Nevertheless, by the criteria of both melatonin and body temperature rhythms, horses appear to adapt much more quickly to abrupt shifts in the light-dark cycle, than do most other animals. This same group of researchers has also examined regulation of clock genes in different tissues of the horse, a paper which might make an interesting subject for another post.
Bastian, T. (2005) The Foal is the Goal: Managing Your Mare and Handling a Stallion. Trafalgar Square Publishing: North Pomfret, VT
Fischer, T.W., Slominski, A., Tobin, D.J., and Paus, R. (2008) Melatonin and the hair follicle. J. Pineal Res. 44, 1-15.
Fitzgerald, B.P., and McManus, C.J. (2000) Photoperiodic versus metabolic signals as determinants of seasonal anestrus in the mare. Biol. Reprod. 63, 335-340.
Guerin, M.V., Deed, J.R., Kennaway, D.J., and Matthews, C.D. (1995) Plasma melatonin in the horse: Measurements in natural photoperiod and in acutely extended darkness throughout the year. J. Pineal Res. 19, 7-15.
Murphy, B.A., Elliott, J.A., Sessions, D.R., Vick, M.M., Kennedy, E.L., Fitzgerald, B.P. (2007). Rapid phase adjustment of melatonin and core body temperature rhythms following a 6-h advance of the light/dark cycle in the horse. Journal of Circadian Rhythms, 5(1), 5. DOI: 10.1186/1740-3391-5-5
PICCIONE, G., CAOLA, G., REFINETTI, R. (2005). Temporal relationships of 21 physiological variables in horse and sheep. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 142(4), 389-396. DOI: 10.1016/j.cbpa.2005.07.019