What does it mean to be locally adapted and who cares anyway?

14 Pages·2008·0.1 MB·English

by  F. D. Provenza

What does it mean to be locally adapted and who cares anyway?1,2
F. D. Provenza3
Department of Wildland Resources, Utah State University, Logan 84322-5230
ABSTRACT: Theavailabilityoffossilfuelswilllikely landscapes we inhabit. In the process of relearning
declinedramaticallyduringthefirsthalfofthetwenty- theseskills,plantswill becomemoreimportantasnu-
first century, and the massive deficits probably will trition centers and pharmacies, their vast arrays of
notbealleviatedbyalternativesourcesofenergy.This primary (nutrients) and secondary (pharmaceuticals)
seemingcatastrophewillcreateopportunitiesforcom- compounds useful in nutrition and health. There also
munitiestobenefitfromfoodsproducedlocallyinways willbeaneed,asintimespastbeforeourheavyreliance
that nurture relationships among soil, water, plants, onfossilfuels,toproducelivestockineasy-caresystems
herbivores, and people to sustain their collective well that match seasonally-available forages with produc-
being. Agriculture will be much more at the heart of tionneedsandthatmatchanimalsanatomically,physi-
communities than it is currently, but by necessity, it ologically, and behaviorally to local landscapes. This
will no longer be so dependent on fossil fuels to power will mean reducing inputs of fossil fuels to increase
machineryortoproducefertilizers,herbicides,andin- profitability by1) matchinganimal needs toforage re-
secticides to grow and protect plants in monocultures, sources;2)selectingforanimalsthatareadaptedana-
antibiotics, and anthelmintics to maintain the health tomically,physiologically,andbehaviorallytolocalen-
ofherbivores,ornutritionalsupplementsandpharma- vironments;3)cullinganimalsunabletoreproducewith
ceuticals to sustain humans. Rather, from soils and minimal help from humans; and 4) creating grazing
plants to herbivores and people, we will have to learn systems that enhance the well-being of soils, plants,
once again what it means to be locally adapted to the herbivores, and people.
Key words: adaptation, change, forage, fossil fuel, learning, livestock
©2008 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2008. 86(E. Suppl.):E271–E284
doi:10.2527/jas.2007-0468
INTRODUCTION withallofthealternativesourcesofenergy,especially
given concerns about human influences on climate
Sustainability is first and foremost about ongoing change. This seeming catastrophe will create opportu-
adaptationineverchangingenvironments.Whatmight nitiesaslifechangesfromurbantorural,andthecom-
thatmeaninthetwenty-firstcentury?Inabooktitled munities that emerge come to rely on foods produced
The Long Emergency, James Kunstler (2005) argues locally,duetoourinabilitytotransportgoodsoverthe
thattheavailabilityoffossilfuelswilldeclineconsider- vast distances that we currently do nationally and in-
ably in the first half of the twenty-first century and ternationally.
that the massive deficits will not be alleviated, even Agriculture will become much more at the heart of
thesecommunitiesthanitispresently,butitslifeblood
will not be fossil fuels to power machinery or produce
fertilizers,herbicides,andinsecticidestogrowandpro-
1ThisworkwassupportedbygrantsfromtheUtahAgricultural tectplantsinmonocultures,antibiotics,andanthelmin-
ExperimentStationandtheInitiativefortheFutureofAgriculture ticstomaintainthehealthofherbivores,ornutritional
andFoodSystems(awardNo.2001-52103-11215)oftheUSDACoop-
supplements and pharmaceuticals to sustain the well-
erativeStateResearch,Education,andExtensionService.Thispaper
beingofhumans.Rather,fromsoilsandplantstoherbi-
is published with the approval of the director, Utah Agricultural
Experiment Station, and Utah State University, as journal paper vores and people, we will learn once again what it
number1928. means to be locally adapted. In this century, we will
2PresentedattheSheepsymposiumattheannualmeetingofthe of necessity nurture relationships among soil, water,
American Society of Animal Science, San Antonio, TX, July 8 to plants,herbivores,andpeopleinwaysthatsustainthe
12,2007.
production, health, and well-being of ecosystems and
3Correspondingauthor:[email protected]
thatmakefarmingprofitableandenjoyable.Plantswill
ReceivedJuly26,2007.
AcceptedSeptember30,2007. beusedmoreasnutritioncentersandpharmacies,their
E271
E272 Provenza
vastarraysofprimary(nutrients)andsecondary(phar- agriculture, people like Kit Pharo (http://www.Pharo-
maceuticals)compoundsusefulinnutritionandhealth. Cattle.com) are developing management philosophies
Nature provides the creatures of this earth with a full and practices that harmonize with natural processes.
rangeofbenefits,includingthenutritionandhealthof Theygrazeanimalsinwaysthatmimicnaturalgrazing
plants,herbivores,orpeople,withoutmanyofthecosts systems to sustain soils and plants. They retain only
wesustainnowadaysduetoourheavyrelianceonfossil- animalsthatcansurviveonwhatnatureprovides,with-
fuel-intensive fertilizers, herbicides, insecticides, and outanyadditionalforageinputs,byselectingforlocally
antibiotics. adapted cattle and by culling any animal unable to
Animals will be locally adapted to the landscapes reproduceeveryyearwithouthelpfromhumans.That
where they will live from conception to consumption. approachmakessenseecologicallyandeconomically.It
If we continue to use ruminants as a source of food, alsomakessensefromabehavioralstandpoint:behav-
therewillbeincreaseddemandforlivestockproduction
ior links ecology and economy by creating a match be-
frompasturesandrangelandsbecauseitrequiresonly
tween what animals need and what is on hand.
one-thirdtoone-halfthefossilfueltoproduceapound
Althoughunderstandinganimaladaptationstoland-
of beef from range as compared with beef produced in
scapeshasalwaysbeenanimportantaspectofthenu-
feedlots. We will again be required to produce rumi-
tritional ecology of ruminants (Demment and Van
nants on forages, as nature has done for millennia.
Soest,1985;Hofmann,1988),untilrecently,landman-
Therewillbeaneed,asintimespastbeforeourheavy
agers havenot attempted toput these ideasinto prac-
relianceonfossilfuels,toproducelivestockinsystems
tice. Instead, many people involved in academia, agri-
that match seasonally available forages with produc-
business, and livestock production have emphasized
tionneeds,andthatmatchanimalsanatomically,phys-
productionattheexpenseofprofit,withoutlinkingani-
iologically,andbehaviorallytolandscapes.Totakead-
malsecologicallytothelandscapestheyinhabit.Thus,
vantage of these benefits, we must learn to make the
animals have been selected with nutritional demands
most efficient use of what nature provides when she
that exceeded the capacity of the forage resource to
provides it.
meet their needs. This problem has been exacerbated
SELECTING FOR LOCALLY by performance testing bullsand rams in confinement
ADAPTED CREATURES on concentrate rations, which likely has selected for
animalsthatperform wellinfeedlots,but arenotwell
How might severe reductions in oil and natural gas
adaptedtofinishingonpasturesandrangelands.Such
affect trade and shipping? With regard to commerce,
ecological mismatches decrease animal performance,
Kunstler(2005)arguesthat“Thesalientfactaboutlife
harmtheproductivityof plants,diminishtheviability
inthedecadesaheadisthatitwillbecomeincreasingly
of soils, and ultimately increase costs and diminish
and intensely local and smaller in scale”. With regard
profitability.
to transportation, he contends “The twenty-first cen-
Norhaveweappreciatedthatongoingadaptationby
tury will be much more about staying put than about
wildanddomesticherbivoresmustinvolveacontinuous
going other places”. In this scenario, livestock will of
dialogue among genes and behavior in ever-changing
necessity be produced from birth to death on pastures
socialandbiophysicalenvironments.Soils,plants,ani-
and rangelands and then sold locally.
mals, and the continents they inhabit change con-
Fossilfuelshaveenabledpeopleandmanyofthewild
stantly. Even within the short span of 20,000 yr since
and domesticated species of plants and animals that
thelastglaciations,changesinclimatehavedrastically
interact with us to exceed the carrying capacities of
alteredphysicalenvironmentsandthespeciesofplants
landscapes. In the process, people and the agriculture
andanimalsthatinhabitthoseenvirons(Pielou,1991).
upon which we all rely have become dependent upon
fossil fuels to power farm equipment (oil), synthesize Nonetheless, we have attempted, with massive inputs
nitrogen fertilizer (natural gas), and transport goods of fossil fuels, to eradicate “invasive” species of plants
(oil) (Pollan, 2006). Low oil prices made it feasible to andanimals.Whatwouldwehavedonewhenthespe-
use high-input harvested forages and feed grains. At cies we now consider native were “invading” after the
some point in the not-too-distant future, rising prices lastglaciations?Likewise,wehaveattempted,atgreat
for oil and natural gas and demands for ethanol will cost economically and ecologically, to change land-
increasegrainpricestothepointwhereitwillnolonger scapes to suit domestic animals, rather than consider-
be feasible to finish animals on grain in feedlots. Al- ing how animals must continually adapt to the ever-
thoughtheyweremeanttodotheopposite,fossil-fuel- changingavailabilityoffoodsandhabitats.Withcattle
intensivepracticeshaveincreasedcostsandadversely and sheep in particular, we have attempted in vain
affected the environment during the latter half of the with massive mechanical and chemical inputs to con-
twentieth century. vertlandscapesdominatedbyshrubstograsstofitour
perceptionoflivestockasgrazers,ratherthanselecting
Cutting Costs by Mimicking Natural Processes
among and within breeds of livestock for individuals
Many grassroots efforts in agriculture now empha- that can use the plants that exist on landscapes. Al-
size cutting costs to maximize profits. To survive in though we often consider cattle to be grass eaters and
Localadaptation E273
sheep to be forb eaters, they can thrive under a wide whereas in 1985 they were selected for production on
range of conditions, including shrub-dominated areas everincreasinginputs.Georgeremarksthat,“Ourewes
inthearidsouthwestUnitedStates,providedtheyhave were strong and as well muscled as deer, and yours
beenselectedanatomically,physiologically,andbehav- wouldn’t last a day where ours went”.
iorally to survive on their own in the landscapes they George emphasizes the value of local knowledge,
inhabit (Provenza and Balph, 1990). which once lost, is hard to regain. In the latter part of
Wemusttakeadvantageofthetremendousvariation the twentieth century, people enamored with stories
within breeds to select for individuals able to perform aboutthe“oldsheepcycle”hopedtorecreateit.Butas
efficiently on poor quality forages high in secondary George points out, “They were crazy. Once the knowl-
compoundscommoninaridenvironments,asthepoten- edge is gone, you can’t get it back just like that. They
tialcertainlyexiststodoso(ProvenzaandBalph,1990; didn’tevenhaveadogthatknewanything.Whenthey
Provenzaetal.,1992,2003).Inaridareas,thatmeans went through here, you knew they were looking for
selecting for animals of smaller frame size that better trouble. And they found it”. The lack of adaptation by
matchtheseasonalavailabilityanddiversityofforage all involved, from dogs and sheep to people, ensured
supplies,andselectingforanimalsthatareabletocon- theywereunableeventomovethesheepfromthebot-
sumethediversearray ofsecondarycompoundsfound tomoftheSanLuisValleyintothesurroundingmoun-
invariousspeciesofplantsnow“invading”landscapes. tains, let alone recreate the old cycle. Everybody in-
Smaller frame sizes reduce the amount of food that volvedlackedtheanatomical,physiological,andbehav-
must be consumed, which enables animals to better ioralknowledgetoaccomplishthetask.Inmakingsuch
mix various plant species, thereby allowing them to majorchangesinmanagement,aminimumof3yrtypi-
copewiththechemicalandphysicaldefensesabundant callyarerequiredassoils,plants,herbivores,andpeo-
in plants that inhabit arid environments (Coley et al., ple adapt to the new regimens (Provenza, 2003a). Ray
1985). Historically, livestock production systems have Bannister, for instance, needed3 yr to retrain a cattle
selected for animals of uniformly larger frame sizes herd to “mix the best with the rest” rather than “eat
andbodycompositions,aswellasformeatflavormade thebestandleavetherest”onrangesineasternMon-
homogeneousbyfinishinganimalsonhigh-graindiets. tana, and Bob Budd took 3 yr to retrain cattle to use
With the decline in fossil fuels, that will change as uplands as opposed to riparian areas on Red Canyon
animals are produced and consumed locally, and as Ranch near Lander, WY (Provenza, 2003a).
consumers acquire preferences for the flavors of ani-
mals produced from plants grown on local soils. Variation Among Individuals Enables Adaptation
Matchinganimalneedstoseasonallyavailableforage
supplies also means mothers will have offspring when Weemphasizemeansandpopulationsinscienceand
foragequalityishighestinlatespringorearlysummer, management, but variation is the basis for selection
rather than when plants are mature and dormant in in natural and agricultural systems. People calculate
the middle of winter. Wild ruminants have adapted average values for representativepopulations, but na-
these reproductive behaviors to ensure that they have turegeneratesonlyindividualsandvariation.Withre-
ample nutrients during late gestation and early lacta- gard to animals, we value the tremendous diversity of
tion, times when their needs are greatest. They must speciesacrosslandscapes,butwehavenotfullyrealized
rely only on what nature provides each year because the significance of the variation among individuals
living on fossil fuels is not an option. In the case of withinaspeciesforhowwecanbecomelocallyadapted
cattle (and sheep), the advantages of having offspring to the environs we inhabit.
in synchrony with nature occur because 1) feed and With regard to easy-care-lambing systems, for in-
labor costs are reduced by 70%; 2) most (90%) calves stance, variation in behaviors among individual ewes
areborninthefirst30dofthecalvingseason,without provides the basis for transitioning from intensive-
feedinganyhay;and3)moretotalpoundsofcalvesare lambingsystemsinjugstoeasy-caresystemsonrange-
weaned that are worth more per pound (Kit Pharo; lands.Thequestionsare:whichewesshouldaproducer
http://www.PharoCattle.com). selectforaneasy-caresystemandcantheybeidentified
In the book The Last Ranch, Sam Bingham (1996) a priori? Based on scientific and experiential knowl-
discusses elements of change and adaptation with a edge,itisprobablyimpossibletoidentifyapriorieach
livestock producer named George Whitten. George re- ewethatpossessesthecombinationofphysiologicaland
counts the “old sheep cycle” practiced in the San Luis behavioral traits that will work best in an easy-care
Valley of Colorado in the early part of the twentieth system. We do, however, know the traits we desire: a
century. He points out that in 1935 they selected for ewe that 1) can lamb successfully without help from
ewes that produced a 75-pound lamb and they culled humans; 2) bonds tightly to her lambs and protects
ewes with twins. In 1985, his sons were selecting for them from predators, and 3) knows the best foods and
ewesthatproduced90-poundlambs,witha150%lamb habitats in which to raise her lamb. How do people
crop. In 1935 the ewes were selected to produce on likeKitPharo(http://www.PharoCattle.com)andJanet
minimal forage inputs and a nomadic way of life, McNally (http://www.tamaracksheep.com) select ani-
E274 Provenza
mals that can make a living without inputs from hu- considermaternaleffectsascomplicatingfactorsines-
mans? Livestock producers who have changed from timating heritabilities (Wade, 1998), again dates back
calvingandlambinginwintertospringandwhorequire toDarwin(1859)whoemphasizedthat“seedlingsfrom
their animals to survive and reproduce on landscapes thesamefruit,andtheyoungofthesamelitter,some-
with little or no human intervention do what natural timesdifferconsiderablyfromeachother,thoughboth
selection does: they put them to the test; those that the young and the parents...have been exposed to ex-
reproduce remain in the herd and those that do not actlythesameconditionsoflife;thisshowshowunim-
are culled. Thus, producers enable natural selection portantthedirecteffectsoftheconditionsoflifearein
without heavy reliance on labor or fossil fuels. comparison with the laws of reproduction, and of
Initialconditionsarevitalwhenitcomestoacquiring growth, and of inheritance” (p. 10). Nowadays, news
newbehaviors.Younganimalsbegintoexperienceand reportsthatregularlyannouncethediscoveryofanew
learnaboutsocialandbiophysicalenvironmentsbefore geneforeverythingreinforcethisone-dimensionalview
birth, and experiences in utero and early in life mark- that genes function in isolation of social and biophysi-
edly influence food and habitat selection (Provenza, cal environments.
2003a). As environmental conditions change, adults Althoughgenescertainlyinfluencetheexpressionof
alsomustlearnnewbehaviors,andamanagercanplay behaviors,itisjustastruethatbehaviorsinfluencethe
a key role in developing a rearing environment that expressionofgenes.Inthatsense,geneslearnfromthe
encouragesmotherstoraiseandeducatetheiroffspring environment (Lipton, 2005). There would be no need
withminimal interventionfrom humans.It isimpera- forgenestobeexpressedifbiophysicalandsocialland-
tivethatmanagersthinkcarefullyaboutmatchingthe scapeswerestatic,buttheever-changingnatureofna-
timing and location of calving or lambing with appro- ture requires that genes converse with the environ-
priate foods and habitats such that mothers relearn ment,andmuchofthisessentialdiscussionoccursdur-
and offspring learn appropriate mothering, foraging, ing development in utero and early in life.
and habitat selection behaviors. An important form of this discourse, termed pre-
For cows or ewes and their owners who have been dictiveadaptiveresponses,referstoresponsesthatare
trainedtocalveorlambundermoreintensivemanage- 1) induced by the environment early in life; 2) cause
mentsystems,thismaybeadifficulttransition.Consid- permanent changes neurologically, morphologically,
ering the power of experience to shape behavior, andphysiologically, and3) confersurvival advantages
changes in management will be most difficult for ma- whentheenvironmentofrearingmatchestheenviron-
ture adults; young replacements, reared in the new ment where a young animal then lives (Gluckman et
system,adaptreadilybecausetheyonlyknowthenew al.,2005).Predictiveadaptiveresponsesdonotneedto
system.Mostproducersindicatemajorchangesinman- conferanimmediatesurvivaladvantagetothefetusor
agement require 3 yr to complete (Provenza, 2003a). veryyounganimal;rather,theyactviadevelopmental
The first year is the most difficult because none of the plasticity early in life to modify the phenotype so it
adults (livestock or people) have any experience with matchestheenvironmentofrearing,whichisexpected
the new system. The second year is better because all tobeinhabitedlaterinlife.Thiswillbesoifthebehav-
those involved have a year of experience with the new ior of mother is appropriate for the postweaning envi-
system and the animals that were unable to adjust to ronment and if that environment does not change too
thenewsystemhavebeenculled.Bythethirdyear,all drastically during the life of the offspring. In this pro-
of the adults have 2 yr of experience with the new cess, the mother is a transgenerational link that pro-
systemandthereplacementfemalesbornintothenew vides stability to social systems by familiarizing off-
system are becoming adult members of the herd or spring in utero and early in life with the locally avail-
flock. able foods and habitats she uses. Offspring become
creative forces as they explore the potential value of
Home on the Range: Learning to Adapt foods and environments not used by mother. In the
from Mother process, they create a balance between constancy
(mother) and creative exploration (offspring) that en-
Since the dawn of the age of genetics, we have been ablesongoingadaptationasenvironmentschangefrom
taughtthatgenesaredestiny(Lipton,2005).EvenDar- generation to generation.
winconceded,neartheendofhislife,thattheenviron- Tothedegreethatpredictiveadaptiveresponsesbe-
ment was not considered suitably in evolution. In a come fixed, there is some degree of risk of a mismatch
letter to Moritz Wagner, Darwin (1888) wrote “In my betweenwhathasbeenexpressedandwhatisactually
opinion,thegreatesterrorwhichIhavecommittedhas needed to survive in an environment. Provided that
beennotallowingsufficientweighttothedirectaction environments do not change too quickly or radically
of the environment”. Still today, modern texts fail to relative to the life span of the individual, risk is low
addresstheall-encompassinginfluenceofmaternalef- and gene expression helps ensure a match between a
fectsonawideassortmentoftraits(Wade,1998).This generation of organisms and the environment where
bias, reinforced by quantitative genetic methods that theyarebornandreared.However,ifthefetuspredicts
Localadaptation E275
itsfuturereproductiveenvironmentincorrectly,dueto (MirzaandProvenza,1990,1992;Thorhallsdottiretal.,
failure of appropriate transduction of the state of the 1990;Howeryetal.,1998).Younganimalslearnquickly
environmentfrommothertofetusorbecausetheenvi- toeatfoodstheirmothereats,andtheyrememberthose
ronmentchanges radicallyfromthatpredicted, thefe- foodsforlife.Lambsfednutritiousfoods,suchaswheat,
tus will have increased risk of poor performance and alongsidetheirmothersforaslittleas1h/dfor5d,eat
disease (Gluckman et al., 2005). This is often the case morewheatthanlambsexposedtowheatwithouttheir
as domestic and wild animals moved from familiar to mothers present (Green et al., 1984). Even 3 yr later,
unfamiliar environments suffer more than locally with no additional exposure to wheat, intake of wheat
adaptedanimalsfrommalnutrition,ingestionofpoison- isnearly10timeshigheriflambsareexposedtowheat
ous plants, and predation (Provenza and Balph, 1990; withtheirmothersthanifinexperiencedlambsareex-
Provenza et al., 1992; Davis and Stamps, 2004). This posed alone or not exposed at all (Green et al., 1984).
disparityalsooccurscommonlywhendomesticanimals Livestock also eat more of poor-quality foods and
aremovedfromrangelandstofeedlotswherethefoods plants high in secondary compounds when they learn
andsocialandphysicalenvironmentsalldifferradically to eat them early in life with their mothers. Goats
fromwhattheyhavelearned.Thesemismatchesdonot reared from 1 to 4 mo of age with their mothers on
occur when animals are conceived, born, reared, and blackbrush-dominated land ate over 2.5 times more
die in familiar social and biophysical haunts. blackbrush than did goats naive to blackbrush (Distel
Given our predisposition to consider behaviors as and Provenza, 1991), a poorly nutritious food high in
fixed genetically, we have neither been aware of nor condensed tannins (Clausen et al., 1990). Experienced
haveweappreciatedthesignificanceofpredictiveadap- goatsalsoconsumed30%moreblackbrushthaninexpe-
tiveresponsesinhumans(Gluckmanetal.,2005)orin rienced goats when allowed to choose between black-
herbivores (Provenza, 1995b; Provenza et al., 2003). brush and alfalfa pellets (Distel and Provenza, 1991).
Nonetheless,experiencesinuteroandearlyinlifehave Likewise,foodintakeandanimalperformancediffered
life-longinfluencesondiet,obesity,health,anddisease markedly during a 3-yr study when cows 5 yr of age
inhumans.Likewise,experienceswithdietsandhabi- werefedstrawasamajorpartoftheirdietfromDecem-
tats that vary in quality have life-long influences on ber to May (Wiedmeier et al., 2002). One-half of the
performance and health of herbivores. By interacting cows ate straw with their mothers for only 2 mo as
withthegenomeduringgrowthanddevelopment,social calves, whereas the other half had never seen straw.
and biophysical environments influence gene expres- Throughoutthe3-yrstudy,experiencedcowsatemore
sionandbehavioralresponses(Lewontin,2000;McCor- straw, lost less weight, maintained better body condi-
mick et al., 2000; Dufty et al., 2002; LeDoux, 2002; tion, produced more milk, and bred back sooner than
Moore, 2002). cows not exposed to straw (Wiedmeier et al., 2002).
Experienceearlyinlifecausesneurological,morpho- Remarkably, with few exceptions (foraging skills: Or-
logical,andphysiologicalchangesthatinfluenceforag- tega-ReyesandProvenza,1993a;foodintake:Greenet
ing behavior (Provenza and Balph, 1990; Provenza, al., 1984; Wiedmeier et al., 1995, 2002), these studies
1995b;SchlichtingandPigliucci,1998;Provenzaetal., areconservativeestimatesofthedegreetowhichexpe-
1998). In the process, young herbivores learn motor rienceearlyinlifeaffectsperformanceofadultsasexpo-
skillsneededtoharvestforages(Floresetal.,1989a,b; sure and testing occurred when animals were young
Ortega-Reyes and Provenza, 1993a,b), they acquire and still learning.
preferences for foods (sheep: Nolte et al., 1992b,c; Herbivoreslearntooptimizeintakeoffoodsinaman-
Squibbetal.,1990;goats:BiquandandBiquand-Guyot, nerconsistentwiththeirpreviousexperienceswiththe
1992),andtheirbodiesadapttousingparticularfoods mixoffoodsoffered(Provenzaetal.,2003).Whenthey
(Distel and Provenza, 1991; Ortega Reyes et al., 1992; eat only a small subset of the more palatable foods
Distel et al., 1994, 1996). Thus, although the body in- that provide adequate nutrition, animals are unlikely
fluences the structure of experience, experience is at tolearn aboutthepossiblebenefits ofmixingdifferent
thesametimeinfluencingthestructureandfunctionof foods, especially those high in secondary compounds.
thebody.Thesedevelopmentalprocesses,whichenable Over time, such selective foraging on pastures and
animalstoadapttolocaldietsandhabitats,implythat rangelandswillchangethemixofplantsavailable,fur-
what constitutes a “high quality diet or habitat” will ther reducing opportunities to learn. However, herbi-
differforindividualsrearedindifferentenvironments. vores encouraged to eat all plants are more likely to
Learning from mother begins early in life as flavors learn to eat mixtures of foods that mitigate toxicity,
offoodsthemothereatsaretransferredtoheroffspring assuming appropriate choices are available. For in-
in utero and in her milk. In livestock, the flavor of stance,experienceandtheavailabilityofnutritiousal-
plants, such as onions and garlic, is transferred this ternativesbothinfluencedfoodchoicewhentheprefer-
way,increasingthelikelihoodthatyounganimalswill ences of lambs with 3 mo of experience eating plants
eatonionandgarlicwhentheybegintoforage(Nolteet containing tannin, terpenes, and oxalates were com-
al.,1992a,b,c).Asoffspringbegintoforage,theyfurther pared with lambs naive to the foods containing these
learnwhattoeatandwheretogobyfollowingmother secondarycompounds(Villalbaetal.,2004).Duringthe
E276 Provenza
studies,alllambswereoffered5foods,2ofthemfamil- families; asa result of selectionamong families, much
iar to all of the lambs (ground alfalfa and a 50:50 mix moregeneticvariancecanbemaintainedatequilibrium
ofgroundalfalfa:groundbarley)and3ofthemfamiliar with mutation than for ordinary genes. The increased
only to experienced lambs (a ground ration containing heterozygosity, in turn, permits random genetic drift
tannins,terpenes,oroxalates).Halfofthelambswere to quickly differentiate local populations and creates
offered the familiar foods ad libitum, whereas half of opportunities for local adaptation via individual selec-
thelambswereofferedonly200gofeachfamiliarfood tion. Accelerated local divergence of isolated popula-
daily.Throughoutthestudy,naivelambsatemuchless tions due to maternal effects can quickly contribute to
of the foods with secondary compounds if they had ad locallyadaptedindividuals,socialgroups,andcultures,
libitum (66 g/d) compared with restricted (549 g/d) ac- whichcaneventuallycontributetospeciation.Thus,the
cess to the nutritious alternatives. Experienced lambs environmentinteractingwithgenescreatesorganisms,
also ate less of the foods with secondary compounds if andthedevelopmentofeachindividualisanemergent
they had ad libitum (809 g/d) as opposed to restricted propertyinfluencedbytheinterplaybetweenitsgenes
(1,497g/d)accesstothenutritiousalternatives.Inboth and social and the biophysical environments where a
cases, however, lambs with experience ate markedly creature is reared. Unfortunately, as Lewontin (2000)
morethannaivelambsofthefoodscontainingthesec- emphasizes,“Moderndevelopmental biologyisframed
ondarycompounds,whetheraccesstothealfalfa-barley entirely in terms of genes and cell organelles, while
alternativeswasadlibitum(809vs.66g/d)orrestricted environmentplaysonlytheroleofabackgroundfactor.
(1,497vs.549g/d).Inacompanionstudy,whenaccess The genes in the fertilized egg are said to determine
tofamiliarfoodswasrestrictedto10,30,50,or70%ofad the finalstate of the organism,while the environment
libitum, animals ate more of the foods with secondary in which development takes place is simply a set of
compoundsandtheygainedmoreweightalongacontin- enabling conditions that allow the genes to express
uum (10% = 30% > 50% = 70%), which illustrates that themselves, just as an exposed film will produce the
animalsmustbeencouragedtolearntoeatunfamiliar image that is imminent in it when it is placed in a
foods that contain secondary compounds (Shaw et al., chemicaldeveloperattheappropriatetemperature”.If
2006). Critically, grazing management can influence wegiveonlylipservicetotherichnessofhowenviron-
what animals learn; continuous grazing at low stock ments affect local adaptation, we don’t even consider
densities encourages selective foraging, whereas man- the role of chance, yet history, necessity, and chance
agement-intensive and short-duration grazing at high arefundamentally interconnectedin developmentand
stockdensitiesencouragesanimalstolearntomixtheir behavior. Lewontin (2000) provides examples of how
diets (Provenza, 2003a,b). chance influences development in plants and animals,
and he makes the point as well with regard to neural
Young sheep and cattle also learn habitat selection
networks:“Aleadingcurrenttheoryofthedevelopment
behaviors from their mothers, as illustrated by cross-
of thebrain, the selectivetheory, is thatneurons form
fostering studies with sheep (Key and MacIver, 1980)
randomconnectionsbyrandomgrowthduringdevelop-
and cattle (Howery et al., 1998). Indeed, natal experi-
ment.Thoseconnectionsthatarereinforcedfromexter-
ences affect habitat preferences in animal taxa from
nal inputs during neural development are stabilized,
insects and fishes to birds and mammals (Davis and
whilethe othersdecay anddisappear. Butthe connec-
Stamps, 2004). In polygynous mammals, dispersal is
tionsmustberandomlyformedbeforetheycanbestabi-
male-based and social groups often are composed of
lized by experience. Such a process of neural develop-
closely related philopatric females (Greenwood, 1980;
mentcouldgiverisetodifferencesincognitivefunction
Dobson, 1982). Retention of daughters within the ma-
that were biological and anatomically innate, yet nei-
ternal home range and male-based dispersal form the
ther genetic nor environmental”. Given the role of
basis of sociality in many mammalian species (Armi-
chance in development, individuals and the develop-
tage, 1981). Social organization leads to culture, the
ment social networks of which they are a part become
knowledgeandhabitsacquiredbyancestorsandpassed
self-organizing systems withemergent properties that
from one generation to the next about how to survive
cannotbepredictedapriori(Provenzaetal.,1998;Ta-
inanenvironment(DeWaal,2001).Aculturedevelops
leb, 2001; Laughlin, 2005).
whenlearnedpracticescontributetothegroup’ssuccess
in solving problems. Cultures evolve as individuals in
groupsdiscovernewwaysofbehaving,aswithfinding NURTURING LOCALLY ADAPTED SOILS,
newfoodsorhabitatsandbetterwaystousefoodsand PLANTS, HERBIVORES, AND PEOPLE
habitats (Skinner, 1981).
Insummary,experiencesearlyinlife,andinparticu- The health of landscapes depends on interrelation-
lar maternally mediated effects on food and habitat ships among soils, plants, herbivores, and people.
selection, are widespread, and their evolutionary dy- Nearly 50 yr ago, in a book titled Soils, Grass and
namicsareunusualrelativetostandardgenetictheory Cancer,AndreVoisin(1959) highlightedtheseconnec-
(Wade, 1998). Specifically, the evolution of maternal tions and warned that people, in our attempts to pro-
effectsinvolves2levelsofselection,withinandamong duce food for a burgeoning world population, have for-
Localadaptation E277
gottenthatourbodiescomefromthesoil.ToVoisin,it plantscanbetoxictolifeinsoils,herbivores,andpeople,
seemedthattheriseoftheartificialfertilizerindustry especially when plants grow in monocultures. Con-
hadcausedpeopletobecomeso reliantonitsproducts versely, moderate levels of secondary compounds are
that we have forgotten our intimate relationship with likelytopromotehealthinsoils,plants,herbivores,and
the soil as nature made it, and that our adulterations humans (Provenza et al., 2007).
of the soil from which we arise may be sealing our All plants contain secondarycompounds that, at too
destinyasaspeciesonearth.Thoughthisquandaryis high concentrations, limit how much of any particular
littlemorethanacenturyold,itsprogressionhasbeen food an herbivore can consume. Herbivores regulate
geometricintheincreaseofdiseasesinplants,animals, intakeofplantswithsecondarycompoundsinorderto
and humans due to overuse of artificial fertilizers ap- ingestadequatelevelsofnutrientsandavoidtoxicosis.
pliedtoplantsgrowninmonoculture.Conversely,soils Eatingavarietyoffoodsisthebestwaytoaccomplish
developed naturally and rich in organic matter and thisobjectivebecausedifferentkindsofsecondarycom-
nutrientsprovide thebasis forhealth inplants, herbi- pounds are processed at different rates and through
vores, and people. differentmetabolicpathways,therebyprovidingmulti-
Managing for healthy relationships among soils, ple avenues for detoxification (Freeland and Janzen,
plants, herbivores, and people can provide invaluable 1974; Provenza, 1996). Conversely, monocultures of
servicestosocietyintheformsofcleanair,water,and plantshighinsecondarycompounds,producedthrough
healthful food, while at the same time reducing costs inappropriate grazing practices or genetically engi-
and increasing profits, especially as the availability of neeredintopastureandcropplants,cancreatevicious
fossil fuels declines and their price increases. With cycles that escalate to the detriment of soils, plants,
growingconcernsabouttheroleoffossilfuelsinclimate herbivores, and people (Provenza et al., 2007).
change,andincreasingincentivesintheformofcarbon As Friend Sykes (1951) wrote over 50 yr ago, “The
credits for sequestering CO , nurturing diverse mix- firstthingthatNaturedoeswhenshehasbeentreated
2
turesofplantwithabundantbiomassbelowandabove with a poison is to battle against it and try to breed a
ground will be a way to increase income (Lal, 2007). resistantstrainoftheformoflifethatisbeingattacked.
Theseincentives,whichwillencouragepeopletoman- If the chemist persists in his poisonous methods, he
age ecosystems, rather than mine particular facets of often has to invent more and stronger poisons to deal
with the resistance that Nature sets up against him.
systemsforshort-termgain,canbuffersystemsagainst
In this way a vicious cycle is created. For as a result
droughts and floods, diminish ecological and economic
of the conflict, pests of a hardier nature and poisons
risks by increasing choices for herbivores and people,
stillmorepowerfulareevolved;andwhoistosaythat,
and enhance sustainability by making best use of the
in this protracted struggle, man himself may not ulti-
sunlight, water, and nutrients that nature provides.
matelybeinvolvedandoverwhelmed”Diversemixtures
of plant species provide a way out of this vicious cycle
Soil Health and Plant Allocation to Growth byproviding avarietyoffoods, withadiverse arrayof
or Defense secondary compounds, to individually and collectively
meet the needs of herbivores (Freeland and Janzen,
How plants allocate resources depends on the avail- 1974).
ability of water, nutrients, and sunlight. Plants can
allocatecarbonfromphotosynthesisandnutrientsand The Value of Plant Diversity
water from soils to growth or to defense in the form of
secondarycompounds(HermsandMattson,1992).The Natural landscapes are diverse mixes of plants that
degree to which they allocate to one or another over occurinpatchesreflectinghistoryofuseinconcertwith
evolutionaryandecologicaltime-spansdependsonthe particular soil, precipitation, and temperature condi-
availability of water, nutrients, and sunlight (Bryant tions. For plants, diversity is the rule for species, phe-
et al.,1983; Coleyet al.,1985). Soilsrich in microand nologies,growthforms,andbiochemistries.Regarding
macro-organismsthatpromotehighratesofdecomposi- thelatter,plantsarenutritioncentersandpharmacies
tionandnutrientcyclingprovideorganicmattercapa- with vast arrays of primary (nutrients) and secondary
ble of holding vast amounts of water and nutrients (pharmaceuticals) compounds useful in animal nutri-
(Allen,2007;Pierretetal.,2007;Smuckeretal.,2007), tion and health (Craig, 1999; Engel 2002; Crozier et
whichstimulatesplantstogrowratherthandefend.On al.,2006).Regrettably,wehaveneitherunderstoodnor
the other hand, deficits of water and nutrients retard valueddiversityinagriculture,asevidentinourpersis-
growthandleadtoaccumulationsofexcessivelevelsin tent attempts to simplify ecological systems to max-
plants of secondary compounds (Bryant et al., 1983, imize yields of crops and pastures. Though often suc-
1991). Too high levels of secondary compounds reduce cessfulintheshortterm,“simplifying”ecosystemstypi-
foodintakebyherbivores(Provenza,1995a,b;Provenza cally leads to ruinous long-term impacts, as shown in
etal.,2003),andhindernutrientcyclingbysoilorgan- marine, forest, and rangeland systems (Gunderson et
isms (Bryant et al., 1991). Indeed, extreme levels in al. 1995).By maximizing the outputof one component
E278 Provenza
of a system, we inevitably hasten the demise of the the nutritional and pharmaceutical values of nature’s
system.Alternatively,studiesofnaturalsystemshigh- pharmacy, the secondary compounds. All plants pro-
light the benefits of biodiversity for reducing interan- duce secondary compounds, even the plants we grow
nual variability in production and minimizing risk of in our gardens, but until recently, people thought sec-
large-scale catastrophic events, such as wildfire and ondarycompoundswerewasteproductsofplantmetab-
outbreaks of diseases and pests (Gunderson et al., olism.Overtheyears,researcherscametounderstand
1995).Thestructuralandfunctionaldiversityinherent therolesofnutrientssuchasnitrogen,phosphorus,and
in naturalsystems increasesproductivity ofplant and potassiuminplantnutrition,buttheyhadnoideawhy
animal species and enhances system stability.
these other compounds occurred in plants. We have
Although humans have dealt with nature’s cornuco-
learnedmuchinthepast30yrabouttherolesofsecond-
pia in many ways, regardless of where they lived our
arycompounds inthehealthof plants,includingfunc-
ancestorstargetedafewspecies,thosethatwereabun-
tionsasdiverseasattractingpollinatorsanddispersing
dant, palatable, and easily cultivated and harvested,
seeds, helping plants recover from injury, protecting
for sampling and eventual use (Etkin, 1994). Of the
plantsfromultravioletradiation,anddefendingplants
roughly200,000speciesofwildplantsonearth,onlya
againstdiseases,pathogens,andherbivores(Rosenthal
fewthousandareeatenbyhumans;justafewhundred
and Janzen, 1979, Rosenthal and Berenbaum, 1992).
of these have been domesticated; and only a dozen ac-
At the same time we were learning of the value of
countforover80%ofthecurrentannualproductionof
secondary compounds, we were reducing their concen-
allcrops(Diamond,1999).Byfocusingonafewspecies,
trations through selection to maximize yields of crops
people transformed the diverse world of plants into a
and pastures that were inevitably more susceptible to
manageabledomainthatgenerallymetneedsfornutri-
environmental hardships. In their stead, we resorted
ents,mainlyenergy,andlimitedoveringestionoftoxins
to fossil fuel-based fertilizers, herbicides, and insecti-
(Johns, 1994). In so doing, however, we narrowed the
genetic basis of crop production to a few plants, rela- cidestogrowandprotectplantsinmonocultures,anti-
tivelyproductiveinthebroadestrangeofenvironments, bioticsandanthelminticstomaintainthehealthofher-
rather than broadening the range of plants valuable bivores,andnutritionalsupplementsandpharmaceuti-
in local environments. We have also discovered only a calstosustainthewellbeingofhumans.Suchsystems
fraction of the plant mixtures useful in nutrition and corrupt the health of soils, plants, herbivores, and hu-
health (Etkin, 1994), and we have simplified agricul- mansandgraduallydegradetheeconomicandenviron-
turalsystemsinwaysthatarehavingalarmingconse- mental health of landscapes. Ironically, we are now
quences on the health of people and landscapes (Pol- attempting to genetically engineer specific compounds
lan, 2006). with similar beneficial functions back into plants. In-
Eating a diverse array of foods is fundamental for stead,weshouldbeaskinghowandwhynaturegrows
nutrition and health. Given appropriate mixtures of plants in diverse mixtures with remarkable arrays of
plants, cattle, sheep, and goats eat more and perform secondarycompounds,andreconstructingpasturesand
betterwhentheyareofferedplantsthatcontainsecond-
grazing lands with assorted species that together en-
ary compounds (Provenza et al., 2007). Variety is so
hance soil fertility, provide benefits of secondary com-
important that bodies have built-in mechanisms that
pounds,andvaryintimeofproduction,depthsofroot-
ensureanimalssatiateonfoodseateninameal,which
ing, and contrasting uses of water and nutrients
guaranteesthatanimalseatavarietyoffoodsandfor-
(Provenza et al., 2007).
age in different locations (Provenza, 1996; Bailey and
Simplifyingagriculturetofacilitatelivestockproduc-
Provenza, 2007). Variety enables animals to reap the
tion,coupledwithaviewofplantsecondarycompounds
benefits of ingesting various primary and secondary
as toxins, has resulted in selecting for a biochemical
compoundsandalsoenablesindividuality.Bodieshave
balance in forages favoring primary compounds and
thenutritionalwisdomnecessarytomeetneedsforen-
nearly eliminating secondary compounds. To increase
ergy,protein,andvariousminerals(ProvenzaandVil-
intakeofsingle-plantdiets,onemustreducesecondary
lalba, 2006). Offering animals choices in confinement,
on pastures, and rangelands allows each individual to compoundsbecausetheylimithowmuchofanyparticu-
meet its needs for nutrients and to regulate its intake lar food humans and livestock can consume. The out-
of secondary compounds by mixing foods in ways that comeisenergy-andprotein-densemonocultureslowin
workforthatindividual(Provenza,2003a;Provenzaet the secondary compounds. The alternative, which we
al.,2003).Thus,varietynotonlyenablesindividuality, havenotpursued,isofferinganimalsavarietyoffoods
italsogreatlyincreasesthelikelihoodofprovidingcells that differ in primary and secondary metabolites,
with the vast arrays of primary and secondary com- therebyenablingthemandustoobtainamuchgreater
pounds essential for their nutrition and health. array of nutrition and health benefits from nature’s
bounty.
The Roles of Secondary Compounds in Nutrition
Forpeopleandherbivores,thebiochemicalcomposi-
and Health
tion of the meals we eat has become more uniform as
Weknowmuchabouttherolesofprimarycompounds the variety of foods in our diets has declined, and we
in nutrition, but we are just beginning to appreciate no longer experience the benefits of eating an array of
Localadaptation E279
plant-derived primary and secondary metabolites rumen (Waghorn, 1990). By making the protein un-
(Craig,1999;Engel,2002).That,inconcertwitheating available for digestion and absorption until it reaches
themeatofanimalsfromfeedlots,meansourintakeof themoreacidicabomasum,tanninsalsoenhancenutri-
a various beneficial compounds is far lower than if we tion by providing high-quality protein to the small in-
atewildplantsandherbivoresrearedonbiochemically testines(Barryetal.,2001).Thishigh-quality-protein-
diverse forages (Dhiman et al., 2005; Pollan, 2006). In bypass effect enhances immune responses and in-
concertwithlackofexercise,thismayexplainthecur- creases resistance to gastrointestinal nematodes (Nie-
rent obesity crisis in many countries, which may get zenetal.,2002;Minetal.,2004).Theresultingincrease
much worse unless we change our behavior. Indeed, inessentialandbranched-chain aminoacidsimproves
fast-food generations may be the first to have shorter reproductionefficiencyinsheep(Minetal.,2001).Tan-
lives than their parents and grandparents due to obe- nins in the diet are a natural way to reduce methane
sity-related diseases. Certainly, many foods preferred emission in ruminants (Woodward et al., 2004), which
by our ancestors areconsidered unpalatable by people is an important issue regarding ongoing efforts to di-
today due to their lack of experience with secondary minish the influence of livestock on global warming.
compounds. With ready access to processed foods high Finally,tanninseateninmodestamountsbyherbivores
insugar,carbohydrates,fat,andsalt,youngpeopleno can improve the color and quality of meat for human
longer acquire preferences for unpalatable foods be- consumption (Priolo et al., 2005). More generally, di-
cause they lack the traditional cultural foundations to verseassortmentsofSCinthedietsofherbivoresinflu-
guide their selection of foods high in secondary com- encetheflavor,color,andqualityofmeatandmilkfor
pounds(Johns,1994).Ontheotherhand,hunter-gath- human consumption, often in ways that are positive
ererswhohavemaintainedtheirtraditionaldietshave (Vasta et al., 2007).
farlesscancer,heartdisease,diabetes,andosteoporosis
than people who consume fast foods, and it is not be- Grazing to Enhance Soil and Plant Diversity
causehunter-gatherersdiebeforetheseillscandevelop and Quality
(Logan and Dixon, 1994). The Masai of Africa, for in-
stance,suffermuchlessheartdiseaseandcancer,even Understanding the options herbivores have when
with diets very high in meat and milk, evidently be- theyconsumefoodsthatvaryinprimaryandsecondary
causetheycombineanimalproductsincludingupto28 compoundsmayhelpcreatenewgrazingstrategiesthat
antioxidant herbs added to each meat-based soup and includesequentialforagingpatternstooptimizeintake
12 added to milk (Johns, 1994; Engel, 2002). and more evenly use all plant species. Shepherds in
Issues of diet mixing and secondary compounds are France stimulate animal appetites and more fully use
just as relevant for the nutrition and health of herbi- therangeofplantsavailablebyherdingsheepandgoats
vores. They are what they eat, as we are what they ingrazingcircuits(Hubert,1993;Meuretetal.,1994).
eat.CindyEngel’s(2002)booktitledWildHealth,How The circuit includes a moderation phase, which pro-
AnimalsKeepThemselvesWellandWhatWeCanLearn vides animals access to plants that are abundant but
from Them is a fascinating discussion of the roles of not highly preferred to calm a hungry flock; the next
secondary compounds in the health and well-being of phase is a main course for the bulk of the meal with
animals. With nutrients and secondary compounds plants of moderate abundance and preference; then
alike,everythingdependsonthedose.Anycompound, comes a booster phase of highly preferred plants for
including water, is toxic in too high doses; the right addeddiversity;andfinallyadessertphaseofpalatable
dosedifferentiatesatoxinfromaremedy,andbecause plantsthatcomplementpreviouslyeatenforages.Daily
every individual is different, it is critical to provide grazingcircuitsstimulateandsatisfyananimal’sappe-
animals with the opportunity to regulate their intake titefordifferentnutrients,theyenableanimalstomax-
ofprimaryandsecondarycompoundsbyofferingthem imizeintakeofnutrientsandregulateintakeofsecond-
avarietyofplants.Althoughwestillhavemuchtolearn ary compounds, and they ensure all plant species are
about plant mixtures and interactions among primary utilized,whichpreventsdirectionalshiftsinvegetation
and secondary compounds, it is becoming increasingly awayfrom diversespecies tomonocultures ofless pre-
clear that offering animals a variety of foods that not ferred plant species.
only meet their needs for nutrients, but that also pro- Diversity in the chemical composition of plants on
vide a variety of secondary compounds, can enhance landscapesprovidesthecontextforherbivorestolearn
nutrition and health. abouttheconsequencesofeatingdifferentfoodsinsuc-
Ascaseinpoint,tanninsareincreasinglyrecognized cession. The time when herbivores eat different foods
as compounds important in health and nutrition, inasequencemayinfluencehowmuchofdifferentfoods
though historically they were thought by agricultural- they can consume as food intake and preference are
istsand ecologistsalike toadversely affectherbivores. influenced by rates of absorption of secondary com-
Eating plants high in tannins is a way for herbivores pounds and their interactions in the gastrointestinal
toreduceinternalparasites(MinandHart,2003),and tract.Forinstance,terpenesaresmall,fat-solublemole-
tannins alleviate bloat by binding to proteins in the culesthatareabsorbedquicklythroughtherumenepi-
E280 Provenza
thelium such that they can quickly decrease food in- caninfluencetheamountofforageherbivoresingestin
take,whereastanninsarehigh-molecular-weightcom- management-intensive grazing systems or in herding
poundsthatremaininthegutwheretheycaninteract systems where animals are moved from one pasture
withotherchemicals.Thus,amealoftanninsfollowed to another.
byamealofterpenesmayleadtohigherlevelsofintake AswiththeFrenchherdingcircuits,intheaforemen-
than the reverse if tannins reduce absorption of ter- tioned studies, we found that ingestion of foods with
penes.Sheepeatmorefoodwithterpenesandtannins secondary compounds was greatest when highly pre-
whentheyeatamealwithfoodsinthesequencetannin- ferredfoodswerefedlast(Moteetal.,2007).Moreover,
containing food → terpene-containing foods → alfalfa/ the ensuing food intakes and preferences for different
barley than when fed alfalfa/barley → tannin-con- foods that develop from learning different foraging se-
taining food → terpene-containing food (Mote et al., quences suggest that synergistic sequences increase
2007).Withtheformersequence,tanninsevidentlyare preference for foods with secondary compounds,
free to bind to terpenes, whereas with the latter se- whereas those that are not synergistic do not (Baraza
quenceproteinsinthealfalfa/barleybindtothetannins et al., 2005; Villalba et al., 2006; Mote et al., 2007). If
andpreventtheminteractingwithterpenes(Jonesand researchcanelucidatehowsequencesofingestingfoods
Mangan,1977;BenSalemetal.,2005).Likewise,sheep thatdifferinprimaryandsecondarycompoundsaffect
do not benefit when fed the sequence of terpene-con-
food intake and preference, ecosystem managers will
tainingfood→tannin-containingfood→alfalfa/barley,
have a valuable tool to influence the health of land-
evidently because terpenes are absorbed so quickly
scapes.
through the gastrointestinal tract walls that they are
Most importantly, people can use grazing circuits to
not available to interact with tannins (Dziba et al.,
generatesoilsrichinorganicmatterandnutrientsand
2006).
diverse in plants. Large herds of animals grazing at
Complementaritiesamongsecondarycompoundsare
high stock densities for short periods of time add to
animportantbutlittleunderstoodareaofplant-herbi-
soils organic matter and nutrients from feces, urine,
voreinteractions(FreelandandJanzen,1974;Provenza
andthetramplingofplants(McNaughton,1984;Bryant
et al., 2003). Even less is known about how the se-
et al., 1991; Savory and Butterfield, 1999; Augustine
quencesofeatingplantswithdifferentsecondarycom-
et al., 2003; Gerrish, 2004). Thus, herbivores can help
poundsaffectsforaging,thoughtheyappeartobecriti-
to build healthy soils and increase the palatability of
cal. As mentioned, sheep eat more food with terpenes
plants by providing conditions conducive for plants to
whentheyfirsteatfoodwithtannins(Moteetal.,2007).
growratherthandefendwithexcessivelevelsofchemi-
Cattlesteadilydecreasetimeeatinghigh-alkaloidendo-
caldefenses.Highstockdensitiesalsoencourageherbi-
pyhyte-infected tall fescue from 40 to 15% when they
voresto“mixthebestwiththerest”ratherthanto“eat
first graze fescue alone for 30 min followed by high-
thebestandleavetherest”,whichcanhelptomaintain
tannin birdsfoot trefoil alone for 60 min; amazingly,
plantdiversityandpreventdirectionalshiftsinvegeta-
when the sequence is reversed they forage actively on
tiontolandscapesdominatedbyoneoronlyafewspe-
bothtrefoilandfescuethroughoutthe90-minmeal(T.
cies of plants high in secondary compounds (Provenza
D. Lyman, F. D. Provenza, and J. J. Villalba, Dept.
et al., 2003; Provenza, 2003b).
Wildland Resources, Utah State University, unpub-
Ironically,herbivoresarelikelytobethebestjudges
lished data). These patterns of foraging are analogous
of the health of soils and plants and the quality of
with birdsfoot trefoil and high-alkaloid reed ca-
their meat for humans. Through a lifetime of learned
narygrass. Sheep similarly decrease intake of endo-
feedbackfromcellsandorgans,theirbodiescontinually
phyte-infectedtallfescueinameal,unlesstheyreceive
process and integrate the diverse array of biochemical
intraruminal infusions of tannins before the meal, in
interactionsandsignalsgeneratedbyhundredsofpri-
which case they eat fescue throughout the meal; con-
maryand secondarycompounds intheplants theyeat
versely, they eat trefoil readily unless they receive in-
that ultimately influence the palatability of any mix-
traruminal infusions of tannins before the meal in
which case they eat less trefoil (L. Lisonbee, J. J. Vil- tureoffoodsintheirdiets(Provenza,1995a).Onlybod-
lalba, and F. D. Provenza, Dept. Wildland Resources, ies can integrate such multifaceted and dynamic sig-
UtahStateUniversity,unpublisheddata).Whensheep nals.Chemicalanalysesarenotuptothetask,asWil-
eat foods high in tannins or saponins along with foods liam Albrecht (1958) wrote many years ago: “Though
high in alkaloids, the tannins and saponins bind with the cow cannot classify forage crops by variety name,
alkaloids, reducing their adverse effects on animal or by tonnage yield per acre, she is more expert than
healthandnutrition(Lymanetal.,2007).Collectively, any biochemist at assessing their nutritional value”.
these findings suggest that cattle and sheep regulate And what is ultimately being assessed by cells and
intake of plants as a function of interactions between organs are messages from soils expressed in the pri-
tannins,saponins,andalkaloidsandthatthesequence mary and secondary compounds in the plant mixtures
inwhichtheyeatforagesiscrucialforincreasingtheir selectedas dietsby herbivoresreared inlocal cultures
intake of plants that differ in secondary compounds. evolved in particular landscapes. That, in essence, is
Importantly,interactionsamongsecondarycompounds what it means to be locally adapted to ever-changing