Chapter One
Keepers of Time
One mid-August morning in the high desert of Arizona, withthe promise of monsoon rains rumbling in distant clouds and the metallicbuzz of cicadas portending another hot summer day, I stepped outof my rock house on top of the mesa and immediately registered a sensationof fall. It took me quite by surprise, like a rustling in the bushes,and I looked around expecting to see what it was that struck me, as if"fall" were an object of some kind. There was nothing, of course; but thesensation was real and lingered like early morning frost in a deep shade.
It was a fleeting incident, one I might have shrugged off without furthercontemplation, except that something kept drawing me back to it,kept puzzling me as to why I should have experienced it at all. By thecalendar, autumn was undoubtedly progressing in the north, but why, Iwondered—without any conscious awareness and indeed after manyyears removed from my native forest environment—was my sense oftiming still so closely synchronized with events I could not see? Wasthere some biological value to humans in monitoring seasonal progression,a vestige of our mammalian heritage, a carryover from an ancientancestry in which an ability to anticipate change well in advance of itsarrival may have been of adaptive value, especially in the face of winter'suncertainty? And what could I have been responding to on that cleardesert morning? Were there cells in my brain coded to measure daylength and send out hormonal messages that say "pay attention, thingsare changing"? To such questions, Edward O. Wilson, the eminent naturalistand sociobiologist from Harvard, would likely have answered yes,suggesting that with only a few thousand years of separation we mightwell carry genes from ancestral hunter-gatherers whose fitness mighthave increased with the sensitivity of their own biological calendars.
If this were so, I wondered, could such a link to our distant past accountfor other emotions that seem deeply rooted within my core—aneed, for example, to be roaming the woods at this time of year; an urgeto pick up the gun and go in search of game, though I am not a hunter?Others have felt it too: "the time of the chase, the season of the buckand doe and of the ripening of all forest fruits; the time when all menare incipient hunters." Even Thoreau, one of the most sensitive observersof natural history, who hunted as a boy but had long since shunnedmeat and given up the gun even for his bird studies, admitted to suchfeelings:
I found myself ranging the woods, like a half-starved hound, with a strange abandonment, seeking some kind of venison which I might devour, and no morsel could have been too savage for me. The wildest scenes had become unaccountably familiar. I found in myself, and still find, an instinct toward a higher ... spiritual life, as do most men, and another toward a primitive rank and savage one, and I reverence them both. I love the wild not less than the good ... even in civilized communities, the embryo man passes through the hunter stage of development.
Perhaps these responses—the sense of timing, the urges within—simplyare conditioned by experience and long habit. Yet if such learnedbehavior were to be of any benefit to ourselves or our ancestors in preparingfor difficult times ahead, it is implicit that we have the ability toanticipate change, which requires measuring something and then comparingthis to yesterday's measurement, or last week's, or last month's,which also requires memory in one form or another.
That we might possess the ability to carry out these computationssubconsciously does not tax the imagination excessively, but the problemgets much more difficult when we consider an animal of temperateor northern latitudes, born in the spring, whose first winter's survivalnow requires numerous timely adaptations in physiology and behavior.Less than 6 months old, it must register impending change and makeprofound adjustments for a season it does not know. Plants, too, musthave a way of anticipating change, for in acclimating to winter conditions,timing is critical. Survival of freezing, for example, requires manyalterations at the cellular level that must be completed well in advanceof the immediate need.
Virtually every organism, then, native to temperate or higher latitudes—andthat lives for more than one growing season—must possessa physiological yardstick or calendar, a means of tracking time either directlythrough internal rhythms or indirectly by monitoring changes insome tangible quality of the environment. What might provide such aprecise clock or calendar? Understanding the possibilities first requiresunderstanding the nature of seasonal change.
* * *
Autumn, though more subtle in some areas than others, is universaloutside of the tropics. When a newcomer to an area such as the shortgrassprairie that generally lacks colorful deciduous trees remarks thathe or she misses the seasons, what the person usually means is that he orshe misses the turning leaves of aspens, maples, birches, or some otherconspicuous indicator of the season. But the changing of leaves does notbring on the season. The absence of deciduous trees in the shortgrassprairie does not mean that fall, any more than spring, fails to come tothe grasslands. It is the steady, progressive change in angle of incomingsunlight as the earth, tilted on its axis, voyages around the sun that determinesthe annual march of seasons; and it is only the intensity ofchange, increasing with distance from equatorial regions, and the vegetativeexpression of seasons that varies geographically.
The earth in its voyage around the sun traces an imaginary path thatdefines the plane of our orbit in space. The sun does not sit at the centerof the plane, however, for our orbit is elliptical, with the earth passingclosest to the sun in the latter part of December and reaching its mostdistant point in June. It is not, therefore, our elliptical orbit, our varyingdistance from the sun, that results in seasons of warmth or coolness, forif this were so our northern summers would occur from Decemberthrough February as in the southern hemisphere. Rather, it is the tilt ofthe earth's own axis from vertical (with respect to the plane of our orbitaround the sun) that results in large monthly variations of incomingsolar radiation at any given location outside the tropics. As we approachthe aphelion of our orbit on the summer solstice, the northern hemisphereis tilted prominently toward the sun, giving all the northern latitudeslonger, warmer days and keeping the region above the Arctic Circleentirely within the sunlit sector as the earth turns. Six months later,we (in the northern hemisphere) are closer to the sun but tilted awayfrom it. Between these two turning points in our annual journey are theseasons of spring and fall.
Transitions between summer and winter are seldom as smooth, however,as described by planetary physics. Of spring and fall Burroughs remarked,"the [season] comes like a tide running against a strong wind; itis ever beaten back, but ever gaining ground, with now and then a madpush upon the land." Indeed, many of us live in places where spring isoccasionally turned on its heels with a surprise May snowstorm, or thebite of autumn frost is temporarily soothed with a placid "Indian summer"of unseasonably warm weather (see p. 122). Though the annualcourse of incoming solar radiation is entirely predictable, it gives rise tomuch less dependable changes, on a daily or weekly basis, in the surfacetemperatures that drive our weather systems. This unpredictability oftemperature results from considerable variation over time and distancein the amount of radiant energy absorbed by the earth, as affected bycloudiness, the presence of snow and ice cover, and differences in vegetationor soil character. Thus, temperature alone is too uncertain toserve as the primary signal for the myriad changes that must take placein the fall. The environmental cues by which plants and animals coordinatetheir seasonal rhythms must be far more dependable.
Three direct aspects of incoming solar radiation, apart from its varyingeffect on surface temperatures, offer potentially useful measures inpredicting the seasons. Each of these is related to the ever-changingangle at which sunlight strikes the earth, as the earth's poles alternatelydip toward and then away from the sun. One obvious result of a lowerangle of incidence is an increase in shadow length. In order for changesin shadow length to be used effectively as a calendar, however, theywould have to be referenced to some fixed measure and standardized fortime of day—a practice that was used successfully by prehistoric culturesto anticipate important events, but that would require extraordinaryneural function on the part of animals to accomplish subconsciously.More useful, perhaps, is the change in light quality—thespectral character of light reaching us—that accompanies the seasonallychanging angle of incidence. Light passing through the atmosphereinteracts with various gasses and particulates, each of which tends to absorbor reflect differently, depending on the wavelength or energy of thelight. As the distance a beam of sunlight must travel through the earth'satmosphere increases, more attenuation occurs in the ultraviolet andinfrared portions of the spectrum, energy just beyond the two ends ofthe visible spectrum. While this is light the mammalian eye can't see,both ultraviolet and infrared wavelengths are, nonetheless, capable ofregulating the biological clocks in rodents (see later discussion). In addition,some attenuation occurs in the blue-green region of the spectrum,which corresponds to the wavelength of peak sensitivity in thebiological rhythms of many mammals. Insofar as light quality alsochanges on a daily basis, however, as between early morning, noon, andevening (hence the prevalence of reds, yellows, and oranges when thesun is near the horizon), some means of time correction would be requiredif this were to serve as an effective calendar.
The one seasonal trend in solar radiation that seems to affect humansmost in fall is the accelerated rate of decrease in total daylight hours ornight length. This is particularly dramatic at higher latitudes, of course,where the transition from long summer days ("days" that last for weeksabove the Arctic Circle) to equally long winter nights is especially rapid.Day length at 65° N latitude (Fairbanks, Alaska, for example) shortensby 31/2 hours between August 1 and September 1. But even at mid latitudesthe changing day length at this time of year is easily perceptible,and it is not difficult to imagine this as furnishing a useful calendar, providedsome mechanism exists by which an organism can keep track oftotal hours of sunlight or darkness. The problem seems simple enoughfor us, as we subconsciously register the slowly changing light conditionsof morning and evening relative to clock time and our daily habitsof working and eating, but we must keep in mind that for plants and animalsthe only clocks are internal, and environmental information ofthis nature must not only be quantified, but also translated into aphysiological response.
* * *
If light is to serve as a clock or calendar, something has to receive informationabout it and translate that information into action. The eye, ofcourse, gathers light, but there is compelling information that it is notthe only organ to do so. A congenitally blind person may still showchemical responses to light despite absence of any pupillary reflex, outerretinal functioning, or conscious awareness of a light stimulus. Retinallydegenerate mice show normal biological rhythms under simulated dayand night light regimes in spite of near total loss of visual perception.And in both birds and insects, the primary receptor of environmentalsignals regulating reproduction, migration, and fat deposition lies somewhereother than in the retina. Experimentally covering portions of abird's skull, but not its eyes, can make a vast difference in its developmentalresponse to simulated long or short days. The light receptor inbirds and insects, for nonvisual information, appears to lie in the brain,not the eyes.
While the exact location and nature of the extraretinal light sensor inbirds and insects remains elusive, in mammals the pineal appears to bethe "third eye." The pineal is a single, somewhat club-shaped organ usuallyfound in the midline of the brain at the point where the cerebralhemispheres and the cerebellum come together. It is a distinct organ,separate from the brain, and is highly vascularized—a condition linkedto its ultimate function.
The pineal exhibits several properties that suggest a central role as abiological calendar. For one, it is photoreceptive by itself, meaning thatit is capable of detecting and responding to light, both electrically andmetabolically, even when surgically isolated from the body. The pineal ofmany animals contains cells with a photosensitive pigment, probablyrhodopsin (the same pigment that receives light in the rod cells of theretina). But the pineal also functions in conjunction with neural signalsfrom the brain or nervous system, and is thus capable of integrating lightinformation from the retina as well. Most importantly, the pineal actslike an endocrine gland, a ductless gland that, in response to nerve signals,secretes chemical products into the blood—in this case melatonin,a hormone that regulates a number of developmental and reproductiveprocesses.
In essence, then, while the pineal shows independent light sensitivity,its function as a principal light-monitoring organ in mammals seemstied directly to both the retina and a biological clock that is located inthe hypothalamus of the brain. Light impulses from the retina are sentvia a special nerve tract directly to the hypothalamus, which coordinatesgeneral biological rhythms with day-night cycles. The light informationis then relayed by neural signals to the pineal, where it is translated intochemical information via the secretion of melatonin and sent to otherparts of the body.
It is the pineal's sensitivity to light information received from thebrain and its ability to translate this into chemical information (itsendocrine function) that places it in a central position with regard totime measurement. The pineal is essentially the endpoint of an opticsystem for processing day-length information, not unlike that of thevisual cortex in the brain for processing images. The usefulness of thepineal as a calendar, however, hinges on the importance of melatonin asa chemical messenger and its sensitivity to day-night duration. Melatoninis a key player in mediating a number of seasonal changes in animals,many of which are critical to its overwintering success. Introducedartificially into the blood of white-footed mice, melatonin can inducefall molt, even during long days. It can stimulate the accumulation ofbrown adipose tissue, increase the animals' basal metabolic rate, anddouble their number of spontaneous daily torpor bouts. Injected intoweasels and djungarian hampsters it can prevent molting from white tobrown during the lengthening days of spring. Melatonin is also a keyhormone in regulating reproductive development in animals. In everycase, whether an animal be diurnal or nocturnal in habit, melatonin issynthesized at night, and therefore its quantity in the bloodstream providesdirect information to other tissues regarding day length.
A single enzyme is responsible for the light sensitivity of melatoninproduction. NAT, as it is called (for N-acetyltransferase), one of 59 enzymespresent in the pineal, catalyzes the conversion of the chemical serotoninto an intermediate product, which is then acted upon by anotherlight-insensitive enzyme to complete the production ofmelatonin. NAT itself is so sensitive to light that its concentration inthe pineal can increase more than 20-fold during a 12-hour night.Longer dark periods result in extended periods of high NAT activity,and hence melatonin secretion, thereby converting light informationinto a biochemical message in the form of nocturnal melatonin peaks ofvariable length. Long-duration melatonin peaks signal short days.(Continuous darkness, however, does not continuously stimulate NATactivity and melatonin production. The biological clock functioning inthe hypothalamus restricts this activity to periods falling within the "expected"nighttime.) In essence, then, it is night length, rather than daylength, that is being measured. If animals are exposed experimentally toa strong light pulse in the middle of the night, NAT levels plummetrapidly, halving in 3 to 5 minutes, with a subsequent drop in melatoninproduction signaling the end of the dark period. The light pulse is readas a new dawn, and the animal responds physiologically as if the longdays of summer had returned.
* * *
If the sensitivity of the mammalian clockworks and calendar seems extraordinary,the timekeeping mechanism of plants is no less so. Lackinga central nervous system to process light impulses from optic sensors,and lacking the integrative function and information distribution capabilityof an endocrine gland, plants nonetheless anticipate the comingseason unfailingly, and do so by acting on the same light informationthat animals receive. That two such disparate organisms might evolvesimilar strategies should not be so surprising; the two kingdoms have,after all, responded to the same need, with day length generally the onlycompletely reliable environmental cue available to either. And when itcomes to monitoring light, few organisms are better suited to the challengethan green plants, for if photoreceptors depend universally onlight-sensitive pigments, then plants have no equal.
Photosynthetic plants have developed an impressive array of pigmentsdesigned to capture energy from almost the entire spectrum of visiblesunlight. Chlorophyll molecules are the most abundant pigment inleaves, but their light-gathering effectiveness is limited to a relatively narrowcolor band at the blue-green and red ends of the spectrum. Becauseenvironments may differ in the spectral quality of light available toplants (energy reaching the forest floor, for example, has had much ofthe blue-green and red light filtered out by chlorophyll in the leavesoverhead), additional pigments are often employed to capture light ofdifferent wavelengths and transfer its energy to the chlorophyll molecules,which are the only ones to participate directly in the chemical reactionsof photosynthesis. The accessory pigments are themselves brilliantlycolored—primarily shades of yellow and orange—but are notoften seen until fall because they are masked by the sheer abundance ofchlorophyll during the growing season.
With many different pigments present in the leaf, it would not be illogicalto assume that one or another was somehow involved in themeasurement of day length. Yet the identity of the clockwork pigmentescaped discovery for a long time. When finally the timekeeper was revealed,it turned out to be a very different pigment indeed—one thatseemed almost a contradiction in form and function to those previouslyknown. This pigment wasn't found where the others usually were, yet itwas almost everywhere in the plant. Its color wasn't far from that ofchlorophyll, yet its appearance depended entirely on how, or when, youlooked at it. New and fresh, it was bright blue, but the moment themolecule was illuminated by sunlight, it switched to an olive-greencolor. Exposed specifically to light at the far-red end of the spectrum,however, it reverted immediately back to blue. The pigment had nothingto do with energy capture for photosynthesis, yet by its absorptionof light it seemed to have a decided influence on the timing of such keyevents as the onset of flowering, senescence, and dormancy.
The pigment is called phytochrome, and among all those light-absorbing(and -reflecting) molecules that excite our senses in the fall,this one, the least noticeable, may in many ways be the most importantat this time of year. We now know it to serve as both a calendar and anon/off switch for a number of processes essential to the orderly cessationof growth and onset of winter acclimation in the plant. The exactmechanism by which phytochrome works remains a mystery, but thedetails of its timekeeping ability have largely been solved, and its splitpersonality seems to be the key.
Phytochrome exists in two distinct and reversible states, each sensitiveto light of slightly different color and each having greatly differenteffects on physiological processes in the plant. As noted already, whenphytochrome is synthesized from protein by the plant it is blue in colorand has an absorption peak (the color band to which a pigment is mostresponsive) centered in the orange-red region of the spectrum, specificallyat a wavelength of 660 nm. In this state, which we call phytochrome-red(or Pr) for its reaction color, the molecule is essentially biologically inert.In fact, when present in abundance it seems to actually block specific developmentalprocesses in the plant.
When phytochrome is excited by absorption of energy in the redband of sunlight, however, it changes state to a form in which it is biologicallyactive, behaving almost like a hormone to open a gate for anumber of developmental processes in the plant. In this state the pigmentis olive-green in color and no longer reactive to orange-red light.Instead, it absorbs much more efficiently in a region centered near thefar end of red, close to the limit of our color vision (we label this formPfr for far-red)—but when it does so, strangely, it reverts back to itsoriginal state. Phytochrome undergoes this same reversal in darkness,too—or decays altogether—and this, it turns out, may be its most usefulproperty as a timekeeper.
How, then, might phytochrome work as a calendar to regulate seasonalevents? Sunlight is constantly converting phytochrome from itsinitial inhibitory form to the active state. But the reverse is also true becausethe full spectrum of sunlight contains energy affecting both formsof phytochrome (the absorption ranges of Pr and Pfr overlap slightly).Here's an important twist, though: The efficiency with which Pr absorbsred light is greater than the absorption efficiency of Pfr for far-redlight, so sunlight acts more like a red source, with more of the Pr endingup as Pfr during the day than is true of the reverse. The result is establishmentof an equilibrium concentration of the two forms of phytochromein daylight, with the biologically active form dominant.
Length of day, by itself, doesn't change this balance, for sunlight willalways drive the opposing reactions at about the same rate; but lengthof night is another matter. With Pfr undergoing either complete destructionand loss during the night, or chemical reversion to its original,inhibitory form, the length of night will have much to do with howlong the active form of phytochrome, Pfr, or the blocking form, Pr, ispresent in the plant at any given season. And in much the same waythat exposure to light in the middle of the night will cause a rapidplummet in NAT and melatonin synthesis in mammals, so too willeven a 2- or 3-minute dark interruption signal a new dawn in plants.Thus, the parallels are nearly complete. Like the pineal in the animal,phytochrome is capable of responding to light information and communicatingthat information via chemical messengers, behaving muchlike a hormone to switch critical plant processes on or off. It is almostcertain that phytochrome does not act alone (calcium is now suspectedas an important accomplice), but it is the master. Concealed by the fallbrilliance of other pigments, the unseen phytochrome, to the plant atleast, may be the real glory of the season.
* * *
By mid-August the gradual increase in the length of night begins tomake a difference to plants and animals. There are few outward signsof fall yet, for the days are still warm enough to nurture the progeny ofsummer, but the solstice is already two months past and the shadows ofa year's new growth are testing their reach. In the Arctic, the caribou areentering their period of autumnal reproductive development even beforethe return of true night, with their biological calendar registeringthe progressively diminishing light intensity around midnight as shorteningdays. Some of the grasses are browning at their tips as theybegin to move reserves of energy and nutrients to the safety of below-groundtissues. Flowers are maturing into seed heads of a differentbeauty. The signs are subtle at first, but the internal timekeepers are atwork sending the first messages of impending cold. There is a quiet revolutionstarting behind the mask of August calm.
WHAT SAITH SEPTEMBER?
A Fair month, truly—golden fair, spiced with breath of the orchards,the vineyards' winy smell ...
All the earth lies dry and warm, and palpitant in sunshine. Thetouch of it is vital. Lie at length here in the pasture, prone on itsspringy turf, and let the strength of it, the sweetness, the balm ofhealing, lap your tired soul to the Elysium, sleep—such sleep ascomes never within four walls, or to the downiest couch ever fashionedby man's hand. Sleep, and dream not. This the hour of fruition,needs not to borrow charm of such insubstantial stuff. A fullworld and goodly lies all about. Upland orchards blush red andyellow; lowland, stubble, meadow, corn-field, chant in high, colorfulnotes a swelling prelude to Nature's harvest-home.
What scent comes out of the corn-land—rare, fine, subtile asbreath of elfin flowers? All the russet rustling stretch is steeped inits balm. You drink it in long gasps, and turn away, sighing—it isfull, so full, of spring, and dew, and dawn, and hope ...
A jocund time this should be. The earth, the fulness thereof, liessmiling peace to a perfect heaven. Yet somehow there creeps in anunder-note—a wailing minor of loss and waste. Faint, ah, so faint!you hear it in the singing waters, the full, rich, rustling leaves, thelow winds sighing out of the sky to lose them as wafts of balm.Through them September saith to this fair world, "Laugh, dance,lie in the sun; eat, drink, and be merry. To-morrow you must die."
Walk afield [then] every day ... Whether sun shines, or raindrips, or white frost bites and stings, you should find a liberal educationin the hectic beauty of death; not cruel death, but a tenderdoom, sweet with the glory of full harvest, and spanned with therainbow of spring resurection.
— MARTHA MCCULLOCH WILLIAMS, 1892
Continues...
Excerpted from Autumnby Peter J. Marchand Copyright © 2000 by Peter J. Marchand. Excerpted by permission.
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