Steppe-Tundra Transition: A Herbivore-Driven Biome Shift at the End of the Pleistocene
Author(s): S. A. Zimov, V. I. Chuprynin, A. P. Oreshko, F. S. Chapin III, J. F. Reynolds, M. C.
Chapin
Source: The American Naturalist, Vol. 146, No. 5 (Nov., 1995), pp. 765-794
Published by: The University of Chicago Press for The American Society of Naturalists
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Vol. 146, No. 5
The AmericanNaturalist
November 1995
STEPPE-TUNDRA TRANSITION: A HERBIVORE-DRIVEN
AT THE END OF THE PLEISTOCENE
S. A. ZIMOV,1V. I. CHUPRYNIN,2 A. P. ORESHKO,2 F. S.
J. F. REYNOLDS,4 AND M. C. CHAPIN3
BIOME SHIFT
CHAPIN III,3*
'North-EastScientificStation,PacificInstituteforGeography,Far-East Branch, Russian Academy
of Sciences, Republic of Sakha, Yakutia, Cherskii,Russia; 2PacificInstituteof Geography,
Far-East Branch, Russian Academy of Sciences, 7 Radio Street,690041 Vladivostok,Russia;
3Departmeiitof IntegrativeBiology, Universityof California,Berkeley,California94720-3140;
4Departmentof Botany, Duke University,Durham, NorthCarolina 27708-0340
December 18, 1993; Revised March 15, 1995; Accepted March 22, 1995
Sulbmnitted
Abstract.-A simulationmodel, recentexperiments,and the literatureprovide consistentevidence thatmegafaunaextinctionscaused by human huntingcould have played as great a role
as climate in shiftingfroma vegetationmosaic with abundant grass-dominatedsteppe to a
mosaic dominatedby moss tundrain Beringiaat the end of the Pleistocene. General circulation
of Beringiawas colder thanat the presentwith
models suggestthatthe Pleistoceneenvironment
broadly similarwind patternsand precipitationbut wvetter
soils. These and otherobservations
suggestthatthe steppelikevegetationand dry soils of Beringiain the late Pleistocene were not
a directconsequence of an arid macroclimate.Tramplingand grazingby mammaliangrazers in
tundracause a shiftin dominancefrommosses to grasses. Grasses reduce soil moisturemore
effectivelythanmosses throughhighrates of evapotranspiration.Results of a simulationmodel
based on plant competitionfor water and lightand plant sensitivityto grazers and nutrient
supply predictthateitherof two vegetationtypes,grass-dominatedsteppe or moss-dominated
tundra,could exist in Beringiaunderbothcurrentand Pleistocene climates.The model suggests
thatmoss-dominatedtundrais favoredwhengrazingis reduced below levels thatare in equilibriumwithclimateand vegetation.Togetherthese resultsindicatethatmammaliangrazers have
a sufficiently
thattheirextinctioncould have contriblargeeffecton vegetationand soil moistLure
uted substantiallyto the shiftfrompredominanceof steppeto tundraat thePleistocene-Holocene
boundary. Our hypothesissuggests a mechanism by which the steppe ecosystem could be
restoredto portionsof its formerrange. We also suggestthatmammalianimpactson vegetation
are sufficiently
large thatfuturevegetationcannot be predictedfromclimate scenarios without
consideringthe role of mammals.
The structure
of naturalvegetationcorrelatescloselywithcurrentclimate,
allowingvegetationto be classifiedaccordingto bioclimaticzones (Holdridge
1947).Similarly,
thedistribution
ofindividual
speciesor floristic
groupsis often
correlated
withspecificclimaticparameters
(Young1971;Whittaker
1975).These
havebeenusedtoexplainthecurrent
vegetation-climate
relationships
distribution
of species(Whittaker
1975)and majorbiomes(Woodward1987;Prenticeet al.
have been used to deduce
1992).The presentvegetation-climate
relationships
of pastvegetation
past climatebased on paleoecologicalindicators
(Davis 1981;
* To whom correspondenceshould be addressed; E-mail: fschapin(w'garnet.berkeley.edu.
Am. Nat. 1995. Vol. 146, pp. 765-794.
All rightsreserved.
t 1995 by The Universityof Chicago. 0003-0147/95/4605-0006$02.00.
766
THE AMERICAN NATURALIST
Grichuket al. 1984; COHMAP 1988) and to predictfuturevegetationdistribution
based on general circulationmodel (GCM) projectionsof futureclimate (Pastor
is
and Post 1988). The implicitassumptionbehindthese climatic,reconstructions
the distributionof vegetation.Howthatclimate is the major factordetermining
ever, animals also stronglyinfluencethe species composition,structure,and processes of ecosystems (O'Neill 1976) such as steppe (Vysotskii 1901; Pachosskii
1917; Prozorovskii1940 [as cited in Kucheruk 1985]; Walter 1979), savanna (McNaughton 1979; Owen-Smith1987, 1988), and boreal forest(Pastor et al. 1988,
1993; Bryantet al. 1991). Consequently,changes in animal abundance can radically alterthe structureand species compositionof vegetation,forexample, convertinggrassland to shrublandor forest(Owen-Smith 1987; Schlesinger et al.
1990). Moreover, factorsextraneous to climate (e.g., human huntingpressure)
can stronglyinfluenceanimaldensitiesand, therefore,the animalimpacton vegeof ecosystems (Pastor and
tation.Predictingthe futurestructureand distribution
Post 1988) may, therefore,requireconsiderationof trophicinteractionsas well
as directeffectsof climateon vegetation.
One of the most dramaticvegetationchanges of the last 20,000 yr was the
conversionof a vegetationmosaic dominatedby a semiarid,grass steppe witha
well-developedgrazingmegafaunato a mosaic dominatedby wet moss tundra
(includingforesttundrawith scatteredtrees) withouta large grazingfauna. In
thisarticle,we referto thisunproductivetundraand foresttundraas tundra.This
change occurredat theend of thePleistocene 10,000-12,000yrbeforethe present
at the end of the Pleistocene
(B.P.). In addition,boreal forestexpanded northward
steppe,presumablyin responseto climatic
intoareas thathad been predominantly
warming.In the remainderof this article,we emphasize those areas of Beringia
continentalshelf) presently
(easternRussia, westernAlaska, and the intervening
occupied by tundra,even thoughthese patternsalso extended south and west
into areas presentlyoccupied by forest.
The vegetationchanges at the end of the Pleistocene have generallybeen ascribed to climaticchange (see, e.g., Hopkins et al. 1982; Grichuk 1984). More
hypothesis
recently,Owen-Smith(1987, 1988) proposed the keystone-herbivore
to explain the widespread vegetationchange that occurred globally at the end
of the Pleistocene. This hypothesis,based primarilyon temperateand tropical
evidence, suggeststhatlargegrazingmammalsare "keystone" species thatmaintain an open vegetationthat undergoes succession to woodland or shrubland
hywhen grazers are removed. In this article,we apply the keystone-herbivore
pothesis to vegetationof the Far Northof Russia and westernAlaska. Based on
evidence fromthe literature,recentexperiments,and a simulationmodel thatwe
developed, we suggest that the Pleistocene grazing megafaunaplayed a major
role in maintaining
steppeconditionsduringthePleistoceneand thatits disappearance, whichcoincided withincreasedhumanhunting,contributedstronglyto the
transitionfromsteppe to tundraat the end of the Pleistocene.
HYPOTHESES
FOR THE STEPPE-TUNDRA
TRANSITION
The Pleistocene overkillhypothesissuggests that increased human hunting
pressurecaused or contributedto megafaunalextinctionat the end of the Pleisto-
HERBIVORE-DRIVEN BIOME SHIFT
767
cene (Hopkins 1967; Jelinek1967; Martinand Klein 1984). Early humans may
have coexisted with steppe megafaunain the mid-Pleistocene,using sharpened
bones and antlers as their huntingweapons. However, 10,000-15,000 yr B.P.
Beringia became occupied by an anatomicallymodernpeople who huntedwith
stone microblades(stone chips) insertedinto wooden or bone shafts(West 1981;
Guthrie1990) and who fed extensivelyon the steppe megafauna(Haynes 1982).
In muchof Beringia,the spread of thismodernmicrobladehuntingtechnologyis
correlatedin timewiththeextinctionofthe steppemegafaunaand withvegetation
change fromsteppe to tundra.WrangelIsland to the northof Siberia was isolated
fromhumanhunting(Lister 1993). Here, mammothssurviveduntil32700yrB.P.,
thatis, well intothe Holocene (Vartanyanet al. 1993),a timethatcoincided with
human arrival on Wrangel Island (Lister 1993). This suggests that survival of
Pleistocene grazingmammalsinto the Holocene was possible in the absence of
humanhunting.
The climatichypothesisformegafaunalextinctionassumes thatan arid, continentalclimateprevailedin Beringiaduringthe Pleistocene, causing low summer
precipitationand drysoils (Velichko 1973; Yurtsev 1974; Giterman1976; Hopkins
et al. 1982; Grichuk1984; Sher 1988; Vereshchagin1988). Well-drainedsoils and
warm summerspromoteda productivesteppe vegetationthatsupportedpopulations of large grazers (mammoths,bison, and horses) (Hopkins et al. 1982;
Guthrie1990). Dry soils facilitatedanimal movement.Accordingto the climatic
hypothesis,the climatebecame wetterduringthe Holocene: rainfallincreased, a
moss-lichencover developed, the amount and productivityof the herbaceous
vegetationdecreased, and snow depth increased. Togetherthese factorscaused
the extinctionof the steppe megafauna(Tomirdiaro1978; Yurtsev 1982; Shilo et
al. 1983; Guthrie1990).
The major evidence forthe climatichypothesiscomes fromPleistocene pollen
and macrofossilsof grasses,Artemnisia,
and othersteppe taxa thattoday are most
abundantin the arid regionsof centralAsia (Yurtsev 1974, 1982; Grichuket al.
1984; reviewed in Guthrie1990). Today, steppelikevegetationoccurs in the tundra zone primarilyas isolated islands on arid, south-facingbluffs(Yurtsev 1982;
Murrayet al. 1983; Edwards and Armbruster1989; Walker et al. 1991), which
leads to the assumptionthatthe warm, dry microclimatethatcharacterizesthis
habitattoday may also have characterizedthe Pleistocene macroclimate.Megafaunafossilsare commonin depositswithsteppe vegetationbut generallyabsent
fromHolocene deposits (Guthrieand Matthews1971; Guthrie1982, 1984b, 1990),
although the precise timingand rate of these changes is debated (Mead and
Meltzer 1984). Thus, there is a general correlationamong the presence of dry
soils, steppe vegetation,and megafauna.
There are several sources of uncertaintyin reconstructingthe Pleistocene
steppe landscape (Colinvaux 1964; Ritchie and Cwynar 1982; Anderson 1985;
Barnoskyet al. 1987; Edwards and Armbruster1989; Guthrie1990). First,many
of the taxa thatdifferentiate
fromtundra(sedge)
steppe (grasses and Artemnisia)
pollen assemblages cannot be identifiedto species and today contain taxa that
can be found on both wet and dry soils. Second, it is difficultto reconstruct
landscape-level vegetationpatternsfrompollen cores taken largelyfromlakes
(Schweger 1982; Barnoskyet al. 1987; Edwards and Armbruster1989). Finally,
THE AMERICAN NATURALIST
768
controversy
over polleninfluxratesraisesquestionsas to whetherthe steppe
vegetationwas unproductive
(Ritchieand Cwynar1982; Colinvauxand West
1984)or highlyproductive
(Guthrie1990).Based on thebulkoftheevidence,it
of Beringiawas productive
seemslikelythatthePleistocenesteppevegetation
mosaicwas probably
and occurredon drysoils (Guthrie1990).This vegetation
butsteppegrasslandwas probably
variablegeographically
and topographically,
a widespreadcommunity
type(Barnoskyet al. 1987;Edwardsand Armbruster
1989).
drawsheavilyon boththeoverkilland the
The keystone-herbivore
hypothesis
betweenaniclimatichypotheses
andlinksthembyassumingstronginteractions
thekeymalgrazingand ecosystemprocesses.As withtheclimatichypothesis,
assumesthata productive
steppevegetation
was necstone-herbivore
hypothesis
It extendsthePleistoceneoverkillhypothesis
essaryto supportmegaherbivores.
was essentialto themaintenance
by suggesting
thatgrazingby megaherbivores
whichproduceddrysoils through
of a productive
high
grass-steppe
vegetation,
Thisis illustrated
as a conceptualmodel(fig.1) that
ratesofevapotranspiration.
shows stronginteractions
amongclimate,animalgrazing,and ecosystemproof themegafauna
could cause a transition
from
cesses in whichtheextinction
ofmoss-dominated
tundra(i.e., tipthe
predominance
ofsteppeto predominance
data and paleoindicators
of
balancein favorof tundra).Because thevegetation
withboththe climaticand the keystone-herbivore
soil moistureare consistent
we cannotuse vegetation-based
climatereconstructions
to differentihypotheses,
we
address
two
Was thecliate betweenthesehypotheses.
questions:
Instead,
maticchangeat theend of thePleistocenesufficient
to cause a transition
from
Arethereplausiblemechanisms
bywhichtheloss ofmegafauna
steppetotundra?
couldcause a shiftfromsteppeto tundra?
EVIDENCE
AGAINST AN EXCLUSIVELY
CLIMATIC
EXPLANATION
FOR STEPPE
Changes in Aridityof Climate
inreconstructing
thecauses ofpaststeppevegetation
and
The majordifficulty
itschangeto tundrais thepaucityofdirectevidenceforthenatureofthePleistocene climatein Beringia.Here we presentindirectevidencefroma varietyof
thattheBeringian
sourcessuggesting
climatewas cold butnotnecessarilymore
thePleistocenethantoday.Largeice sheetsoccupiedCanada,Greenaridduring
land, and northern
Europeduringthe Pleistocene20,000yrB.P., but northern
shelfseparating
thesetwo areas
Russia,Alaska,and the Beringiancontinental
wereunglaciated,
glaciers(Hopkins1967;Nekraexceptforlocalizedmountain
sov et al. 1973;CLIMAP 1981;Serebryanny
1984).Oxygen-isotopic
composition
in thenorthPacific
of fossilforaminifera
indicatethatsea-surface
temperatures
southofBeringiawere2?-8?Ccolderduring
thePleistocenethanat present(CLIMAP 1981;Rind1987).Togetherthesedataindicatea colderclimatein Beringia
thanexiststoday.Consequently,
sea ice extended100 latitudefarther
souththan
at present(CLIMAP 1981;Kutzbachand Guetter1986).
The geographical
patternof the Pleistoceneclimate20,000yrB.P. has been
U)
--<p)
0
0~~~~~~~~~~~C
2C)
3
m-C
CO)~~~~~~~~~~~~~~~~~~C
-o~~~~~~u
L
Cd
Cd,
00~~~~~~~~~~~~~c
-00
~~~l
-C
4_
)
C)
0
C,,t
00~~~~~~~~~~~~~~~~~~~~~~~~~~~
Li
)
770
THE AMERICANNATURALIST
data on thePleistocenedistribution
of
simulatedusingGCMs thatincorporate
and albedo (Kutzbach
land,ocean, glaciers,sea ice, sea-surface
temperatures,
and Wright1985;Manabeand Broccoli1985;Kutzbachand Guetter1986;Rind
1987).These paleoclimatic
reconstructions
usingthreedifferent
GCMs suggest
thatthePleistoceneclimateof Beringiawas 2?-5?Ccolderin summerand 10?thegrowing
and much
20?Ccolderinwinterthanat present,
seasonwas shorter,
ice sheets
aroundthelargecontinental
ofthejet streamwas deflected
southward
in easternNorthAmericaand westernEurasia(Kutzbachand Wright1985;ManabeandBroccoli1985;KutzbachandGuetter1986;Rind1987).However,these
windpatand surfaceandjet-stream
GCM simulations
suggestthatprecipitation
ternsin Beringiawerebroadlysimilarto presentpatterns,
althoughin thepast
inclimatewithin
variation
(as today)therewas probablysubstantial
geographical
windsdirectly
west
Beringia.For example,theremayhavebeenmoresoutherly
or
of theLaurentideice sheet(Kutzbachand Wright1985)but morenortherly
and
windselsewherein Beringia.Because of similarprecipitation
continental
coldersummers
betweenthePleistoceneand presentclimate,thesemodelsprein Beringia(Rind1987)or geographically
variablesoil
dicthighersoil moisture
moisture(drysoils immediately
east of the Europeanice sheetand similaror
highersoil moisture
elsewherein Beringia)(Manabeand Broccoli1985).These
withassumptions
GCM simulations
conflict
thata warm,arid summermacroof
climatethroughout
forthewidespreaddistribution
Beringiawas responsible
and drysoils(Grichuk1984;Velichko1984;Guthrie1990).
steppevegetation
Asia and Alaska were moreextensivein the
Mountainglaciersof northeast
earlierglacialatePleistocenethanat present(although
less extensivethanduring
tions)(Pewe et al. 1965;Hamilton1982;Hopkins1982;Serebryanny
1984).Mass
balanceof mountain
glaciersis governedprimarily
by snowinputsand summer
Giventhatsea-surface
andairtemperatures
werelowerduringthePleismelting.
tocenethanat presentand thatsea ice extendedfarther
south,the extensive
mountain
thePleistoceneweremorelikelydue to cold
glaciersofBeringiaduring
summersthanto wetterwinters(Lebedeva and Khodakhov1984; Rind 1987;
Zimovand Chuprynin
1991),whichsuggeststhatthePleistocenedid nothave a
warmsummer
climate.
andlow climaticpotential
forevapotranspiration,
Despitecold summers
Pleistocenesoilsweredrierthanat present.ExtensivePleistocenedunesofsandand
siltthroughout
Beringia(Hopkins1982;Tomirdiaro
1982)suggesteitherthatthe
climateofthePleistocenewas too coldto supportproductive
vegetation
(Ritchie
andCwynar1982;ColinvauxandWest1984)or thatthesoilswereextremely
dry
dunes
(Hopkins1982;Tomirdiaro
1982;reviewedinGuthrie1990).Alternatively,
shorttimeperiodsand maynotreflect
mayhavebeenproducedduringrelatively
theaveragePleistoceneclimate.Carbonateand saltaccretionin thesedeposits
also indicatehighactualevapotranspiration
ratesfromthesesoils (Tomirdiaro
1982;Walkerand Everett1991).The vegetation
data also suggestdriersoilsbut
are not conclusiveevidenceof a drymacroclimate.
Many of the Pleistocene
grassesweremesophyllous
(Yurtsev1981,1982),and somesteppespecies(e.g.,
of disturbance
and drysoils ratherthanof
Artemisiaarctica)maybe indicators
drymacroclimate
(Webber1978).
The radiativeindexof aridity(Ia, theratioof netenergyinputto energyre-
771
HERBIVORE-DRIVEN BIOME SHIFT
TABLE I
AVERAGE
RADIATION,
PRECIPITATION
AND
INDEX
(NOVEMBER-MARCH,
OF ARIDITY
(SEE
APRIL-OCTOBER,
TEXT)
IN
i6
AND
WEATHER
TOTAL),
STATIONS
NET
TOTAL
OF NORTHEAST
SOLAR
ASIA
PRECIPITATION
(mm)
LATITUDE,
LOCATION
LONGITUDE
Kotelnyi
Priobr-ocheniya
WrangelIsland
Chetyrekhstolbovoi
Mostakh Island
Ayan
Olenek
Verkhoyansk
Cape Schmidt
Srednekolymsk
Uelen
Srednekan
Markova
Oimiakon
Yakutsk
Aldan
NOTE.-Data
75?N,140?E
74?N,110?E
72?N,180?E
71?N,160?E
71?N,129?E
70?N,168TE
68?N,112?E
68?N,133?E
68?N,180?E
67?N,153?E
67?N,173?W
64?N,153?E
64?N,171?E
63?N,142?E
62?N,129?E
580N,126TE
Nov.-
March
40
28
65
46
55
52
47
27
81
57
125
149
107
32
36
89
April-
NET
RADIATION
Oct.
Total
(kcal cm2-
101
144
117
101
177
137
219
120
173
131
261
268
230
143
166
457
141
172
182
147
232
189
266
147
254
188
386
417
337
175
202
546
11.1
15.8
23.8
20.5
14.7
24.7
21.3
23.8
26.3
26.3
19.1
23.4
27.1
31.0
29.3
26.4
yr' l)
INDEX
OF
ARIDITY
1.5
1.7
2.4
2.6
1.2
2.5
1.5
3.0
1.9
2.6
.9
1.0
1.3
3.3
2.7
.9
are averages for the entire record (up to 1980) of each station (n > 20 yr) from regional
volumes of the ClimaticAtlas ofthe/Soviet Union (Zimov and Chuprynir.1991).
providesan objectiveindexof aridity
quiredto evaporateannualprecipitation)
(Budyko1984):
1
PET/PPT,
and PPT = precipitation
(see app.
wherePET = potentialevapotranspiration,
A fordefinitions
and units).A valueofthreeindicatesthereis enoughradiation
ValuesofIa in northeast
inputto evaporatethreetimestheannualprecipitation.
dominated
Asia (an area currently
by wettundra)rangefromaboutone to three
stations(table 1), values thatare similarto areas in
among16 meteorological
centralAsia thatsupportsteppe(1a = 1-2) or semidesert
(la = 2-3) vegetation
(Budyko1984).
acrossBeringia(Manabeand Broccoli1985;KutzVariationsin macroclimate
withslope,aspect,and
bach and Guetter1986;Rind 1987)and in microclimate
elevation (Barnosky et al. 1987; Edwards and Armbruster1989) were probably
greaterthanthemagnitudeof changein these parametersbetweenthe Pleistocene
and today (Manabe and Broccoli 1985; Kutzbach and Guetter1986; Rind 1987).
Thus, we mightexpect a greaterabundance of steppe in the presentvegetation
mosaic, if macroclimatewere the only factorresponsibleforthe vegetationshift
across the entirearea of Beringia.
Effectsof Aridityon Vegetation
A major dilemmaforthe climatichypothesisis to explain how the late Pleistocene vegetationcould have been sufficiently
productiveto supportthe large size
THE AMERICANNATURALIST
772
andrapidgrowth
ratesofthePleistocene
megafauna
(Guthrie1984a,1990;OwenSmith1987).Becauseitis unlikely
thatthecoldertemperatures
ofthePleistocene
wouldhavepromoted
ithas beensuggested
productivity,
thatdrysummers
preventedwaterlogging
ofsoilsandcontributed
to a highproductivity
ofthePleistocene steppe(Hopkinset al. 1982;Guthrie1990).However,the distribution
of
current
tundraecosystemsindicatesa negativecorrelation
betweenaridityand
productivity
(Yurtsev1982).As discussedbelow,itis morelikelythatthespecies
composition
of steppewas morenutritious
to megafaunal
grazersthanis thatof
tundra.
Direct ClimaticEffectson Fauna
The climatichypothesis
suggeststhatclimaticchangeat theendofthePleistocenecouldhavecontributed
directly
tomegafauna
extinction
increasesin
through
snowdepth(reducing
access to winter
summer
food)and soilmoisture
(reducing
mobility)
(Guthrie1990).However,today'ssnowcoveris <30 cm in thecentral
plainsofYakutiaand in thebasinsoftheYana and Indigirka
Riversin northern
Yakutia(Gavrilova1973).At 61 of 83 Yakutianmeteorological
stations,winter
precipitation
is <50 mm(also see table 1) (Zimovand Chuprynin
1991).Areas
thatsupportnaturalor introduced
bisonpopulations,such as the GreatSlave
Lake of Canada or the Delta Junction
area of Alaska, currently
have greater
snow depththannorthern
Yakutia.Yakutianhorses,a hardynorthern
breed,
obtainsufficient
foodto sustainthemselves
frombeneatha 50duringthewinter
to60-cmsnowpack(Tikhonov1987).Moreover,thesehorsesgrazeinwetriparian
meadowsin summer
inpreference
withdriersoils(S. A. Zimov,
to communities
personalobservation),
whichsuggests
thatsummer
soilmoisture
does notgreatly
restrict
habitatuse.
In summary,
thePleistoceneclimatewas probablycolderthanat present,but
If theclimatehad beenmorearidin thepast,it
are uncertain.
changesin aridity
wouldprobably
havereducedrather
thanincreasedtheproductivity
ofthevegetation.Thus, thereis not strongevidencethata changein macroclimate
alone
caused a changein relativeabundancefromproductive
grasslandsteppeto less
productive
tundra.
POTENTIAL
MECHANISMS
FOR THE STEPPE-TUNDRA
TRANSITION
We suggestthatthe keystone-herbivore
hypothesis(Owen-Smith
1987)is a
usefulalternative
to theclimatichypothesis
becauseit providesa mechanism
to
anddrysoilsofthePleistocenesteppewithout
explainhighproductivity
assuming
a morefavorableclimateforplantgrowth.
The climatichypothesis
assumesthat
an aridPleistoceneclimateproduceddrysoils thatwere necessaryforsteppe
vegetation
and,therefore,
steppemegafauna
(fig.1) (Guthrie1990).The keystoneherbivore
hypothesis
arguesthatthepresenceofanimal-induced
steppevegetationcouldhaveproduceddrier,morefertile
soilsthanoccurin tundra.
VegetationEffectson Soil Moisture
influences
soil moisturebecause mostwaterevaporating
Vegetationstrongly
fromvegetatedsurfacesderivesfromtranspiration
(Jarvisand McNaughton
HERBIVORE-DRIVEN
BIOMESHIFT
773
1986).Transpiration
ratecorrelates
withphotosynthesis
at theleaflevelbecause
stomatalconductanceis adjustedto matchthebiochemical
potentialforphotosynthesis
(Farquharand Sharkey1982;Fieldet al. 1992)and at thecanopylevel
becausebothprocessescorrelate
withleaf-areadevelopment
(Collatzet al. 1991;
Field et al. 1992).Consequently,
transpiration
is proportional
to photosynthetic
carbongain(Chapin1993)andnetproductivity
(about400-500g water/g
production)(Larcher1980;Field et al. 1992).If primary
productivity
duringthe late
Pleistocenegrass-dominated
steppewas higherthanthatofthemoss-dominated
tundraof theHolocene,thePleistocenesoils couldhave been drierbecause of
thegreaterevapotranspiration
ratherthanbecauseofdrierclimate(fig.1).
Highplantproductivity
reducessoilmoisture.
Whenagricultural
landsremain
fallowin aridclimates,soil moisture
increases.Removalofforesttreesreduces
regionalevapotranspiration
and increasesrunoff
(Bormannand Likens 1979).
Computer
simulations
linkedtoGCM modelspredictthata conversion
oftropical
foresttograssland
wouldreduceevapotranspiration,
thereby
soilmoisincreasing
ture(Shuklaet al. 1990).Additionof nutrients
to tussock-tundra
vegetation
in
Alaskaincreasedproductivity
andreducedsoilmoisture
(Chapinet al. 1995).The
presenceof largegrazersincreasedthe productivity
of steppevegetationand
reducedsoil moisture
(Kucheruk1985).
To determine
whether
differences
amongtundravegetation
typescouldcause
largeeffects
on evapotranspiration
andsoilmoisture,
we measuredevapotranspirationfromdifferent
speciesand associatedsoils in weighing
lysimeters
at the
NortheastScientific
Stationin theKolymalowlandsduringa 6-wkexperiment.
Whensoils weremaintained
at fieldcapacity,vascularplantscharacteristic
of
steppe(i.e., grasses,sedges,and Artemesia)transpired
morewater(174 ? 18
mm)thannonvascularplantscharacteristic
of tundra(69 ? 13 mm)(table2).
Whenplantsreceivedonlynaturalrainfall,
mossesevaporatedless water(42 ?
3 mm)thanbareground(55 mm)because mosseslack a rootsystemand have
limitedaccess to soil water.By contrast,steppespeciesevapotranspired
99 ?
12mmofwater(all theavailablewaterinthesoilprofile)
wilted.
andsubsequently
Theseexperiments
demonstrate
thatsteppevegetation
morewaterand
transpires
producesdriersoilsthanmoss-dominated
tundravegetation.
VegetationEffectson Soil Fertility
To explaindifferences
in productivity
inbetweensteppeand tundra,without
vokinga changein climate,we mustunderstand
theroleof mossesand grasses
in plant-soil
feedbacks.Mosses reduceratesofdecomposition
minand nitrogen
eralization
(CoulsonandButterfield
andDamman1991;Van Cleve
1978;Johnson
et al. 1991)becauseoftheirlow nitrogen
and highconcentrations
concentration
ofrecalcitrant
lignin-like
conductance
polymers
(Chapinet al. 1986),lowthermal
thatreducessoil temperature,
and low ratesof evapotranspiration,
whichpromotethedevelopment
ofwaterlogged
soils.Theresulting
lownutrient
availability
limitstheproductivity
ofvascularplants(Chapinand Shaver1985).By contrast,
mossgrowth
is limited
morestrongly
bywaterthanbynutrients
(SkreandOechel
1979, 1981),so the moist,nutrient-deficient
soil environment
promotesmoss
growth.Eventually,
as themossesgrow,thawdepthdecreasesto thepointthat
774
THE AMERICAN NATURALIST
TABLE 2
RATESOF EVAPOTRANSPIRATION
FROMPLANTSPLUSASSOCIATED
SOILSPLACEDIN 2i-cm-DEEPWEIGHING
LYSIMETERS
IN THEKOLYMALOWLANDS
DURINGI989
MAXIMUM
EVAPOTRANSPIRATION
RATE
(mm d-')
SURFACE TYPE
Free water
Soil:
Steppe loam
Sand
Tundra plants:
Lichen (Cladonia)
Moss
Steppe species:
Agropyron
Eriophorumsw1
Equiisetiuml
A)rtemesia
Probabilityof differencebetween
nonvascularand meadow/steppe
species*
Field
Capacity
Natural
Precipitation
6.7
.
6.4
3.6
.
AVERAGE
RATEOF
EVAPOTRANSPIRATION
(mm d-1)
Field
Capacity
Natural
Precipitation
3.5
...
1.3
...
3.3
1.5
1.0
...
3.3
6.1
1.5
1.0
1.6
2.8
.9
1.0
16.2
9.6
8.8
14.7
4.3
5.6
3.1
3.6
6.7
5.3
4.0
6.1
2.5
3.0
1.6
2.3
.03
.
.01
.03
.02
NOTE.-Each lysimetercontainedbare soil, open water, or complete plant cover. Samples were
collected froman area of loess soil typicalof the region.Water was added to bringeach soil to field
capacity. Lysimeterswere weighed twice daily, and water was added weekly to maintainconstant
weight.Measurementswere made withlysimetersmaintainedeitherat fieldcapacity (n = 2) or with
natural precipitation(n = 1). We presentboth the maximumobserved rate and the average rate
duringJuly1989. Average environmentalconditionsduringthe experimentwere as follows: air temperature(25?C), wind speed (4 m s-'), relativehumidity(45%), daily directirradiance(21 h d-'), and
precipitation(7.4 mm wk- ').
* Probabilityvalue fromt-test,treatingeach species as a separate sample.
onlythemosslayeritselfthaws(Kriuchkov1973;Chernov1978;Van Cleve et
al. 1983),andgrasses,whichrequireaccess to thawedmineralsoil,are excluded
fromthesecommunities.
Because of thesefeedbacks(fig.1), moss ecosystems
developreadilyin theFar North.For example,in northwestern
Siberia,60%70% of the forestedarea disappearedduringhistoricaltimebecause of moss
andassociatedwaterlogging
development
ofsoils(Kriuchkov1973),andAlaskan
forestssucceedto moss-dominated
muskegsand spruceforestsin theabsenceof
fire(Van Cleveetal. 1991).Moss-dominated
ecosystems
areavoidedbymammalianherbivores
(Wolff1980)becausethelow tissue-nutrient
and highsecondarymetabolite
concentrations
inthevegetation
cause low digestibility
andlow palatabilityto animals(Bryantand Kuropat1980;Pastoret al. 1988).
In morefertile
grass-dominated
meadows,an alternative
set offeedbackspromotesproductivity
and grazing(fig.1) (Chapin1991).Growthof grassesin the
currenttundraenvironment
is stimulatedby nutrient
inputsfromfertilizers
(McKendricket al. 1978;Shaverand Chapin1986),animalcarcasses,and feces
(Batzliet al. 1980;McKendricket al. 1980)or intensive
disturbance
by humans
(Chapinand Shaver 1981;Zimov 1990)or animals(Batzli and Sobaski 1980).
HERBIVORE-DRIVEN
BIOMESHIFT
775
Mowingstimulatesthe abovegroundproductionof steppegrasslandsfivefold
(Kucheruk1985)and of sedgetundrathreefold
(Peshkovaand Andreiashchkina
1983),whichindicatesthatgrazingstimulates
aboveground
productivity
in these
ecosystems.Thisgrass-dominated
vegetation
has highertissue-nutrient
concentrationsthanmosses or dwarfshrubs,is moredigestible,and attractsgrazers
(Whiteand Trudell1980). Both the highlitterqualityand the rapidturnover
of nutrients
and nutrient
by grazersstimulatedecomposition,
mineralization,
turnover
(Batzliet al. 1980;Chapin1991)and reducesoil moisture(Chapinand
Shaver 1985).The dense vascularlitterfall
shades out or physicallysmothers
mosses, whichleads to a declinein theirabundance(Chapinet al. 1995). In
high-fertility
sitesmanygrassesare coveredwithsnowwhilegreenand, therethe winter(Tishkov1985),
fore,maintaintheirhighforagequalitythroughout
whichleads to intenseoverwinter
microtine
grazing(Batzliet al. 1980;Chapin
and Shaver 1981).These feedbacks,whichmaintaingrasslands,are also well
intemperate
andtropicalclimates(McNaughton
documented
1979;Huntly1991),
but theyoccur onlyin isolatedlocationsof intensivelemminggrazingin the
Far North,because thereare no largegrazingmammalsthatfeed mainlyon
grasses.
Possible Triggersfor VegetationChange
tundraand grass-dominated
Giventhatbothmoss-dominated
steppeecosyssoil moisture
and nutrient
temscan createtheirownself-sustaining
regimes(fig.
a changein therelativeabundanceof steppeand
1), whatcould have triggered
Fourfactorswerepotentially
imtundraat thePleistocene-Holocene
boundary?
thecessationof loess deposition,increasesin atmoportant:climaticwarming,
sphericCO,, and theloss oflargemammalian
grazers.
and groweffectively
Arcticgrassesand mossesbothphotosynthesize
at low
temperature
(Oecheland Sveinbjornsson
1978;Tieszen 1978)and exhibitbroad
thatwarming
latitudinal
distributions,
so it seemsunlikely
woulddirectlycause
a shiftfromgrassto mossdominanceat theend ofthePleistocene.
Pleistoceneloess depositionin theBeringianlowlandsceased
The substantial
at thebeginning
oftheHolocene(Tomirdiaro
1982).Whentheaveragedeposition
rateis greater
than1 mmyr-1,grasseshavea competitive
advantageas colonizers
sourceforgrasses
(ZimovandChuprynin
1991).Sediments
providea richmineral
andeliminate
shrubs(Walkerand
slowlygrowing
mosses,lichens,andevergreen
Everett1987,1991;Zimovand Chuprynin
1991).
In thelow-CO2Pleistoceneclimate(Webband Bartlein1992),stomatesmust
have remainedopenlongerand transpired
morewaterto absorba givenamount
of CO2 comparedto theHolocene(Larcher1980;Fieldet al. 1992).Thus,even
musthave
assumingno changein climate,a low-CO2Pleistoceneenvironment
anda morexerophytic
forwater,lowersoilmoisture,
causedgreater
competition
thanin current
tundra.Most of thischangein atmospheric
vegetation
CO2 occurredbefore12,000-15,000
yrB.P. (Webband Bartlein1992)and thuspreceded
thetransition
fromsteppeto tundra.
Theloss oflargemammalian
grazersatthePleistocene-Holocene
boundary
(see
to thetransition
fromsteppeto tundra.Ungrazed,
above)couldhavecontributed
776
THE AMERICANNATURALIST
unfertilized
meadowsare unstablein the absence of herbivoresor continued
disturbance
(Chernov1978).Whendry,uneatenlitteraccumulates,
nutrients
are
turnoverdeclines
sequesteredin undecomposedorganicmatter,and nutrient
(Batzli 1977).Drygrasslitteris highly
reflective,
reducingradiationgain,and is
an effective
heatinputto soilduringtheshortsummer
heatinsulator,
minimizing
thedepthofsoilthaw,and promotseason,coolingtheunderlying
soil,reducing
ingthegrowth
ofmossesand evergreen
shrubs(Batzli1977).Conversely,
herbivorescan cause a conversion
fromtundrato grass-dominated
meadow.Despite
itseffectiveness
in excludingothervegetation,
mosscoveris fragilewhentrampledor grubbedbyanimals(Chernov1980).AreasofRussiantundracoveredby
whichbothdestroy
deep snow,such as ravines,supportlemming
populations,
themossesand fertilize
thesoil. Duringpopulation
outbreaks,
lemmings
expand
intoareas betweenravinesand eliminatemossesby grubbing
(Chernov1978),
to themaintenance
ofmeadows,whichare 8- to 10-fold
whichcontributes
more
thanmossassociations(Chernovet al. 1983).The highproductivity
productive
of meadowsis associatedwithan 8-10-foldincreasein biomassof soil invertebratesand withrapidnutrient
cycling(Chernov1978;Chernovet al. 1983).Simibetweenice-wedgepolygons
larly,in Alaskanlowlandpolygonal
tundra,troughs
and morerapidnutrient
have deepersnow,largerlemming
populations,
cycling
reindeer
thanadjacentmicrohabitats
(Batzlietal. 1980).Similarly,
grazingcauses
and reducedcover of mosses and shrubs(Thing
the expansionof graminoids
and nutrient
1984).Snowgeesealso stimulate
productivity
cyclingin coastalsalt
marshesofnorthern
Canada and Alaska(Cargilland Jefferies
1984).On a larger
scale, wherefireor humandisturbance
destroysthemossturf,meadowvegetationdevelopsand becomesa focusforactivityof mammalian
herbivores
(Fox
1978;Wolff1980;Bryantand Chapin1986).
In the followingsection,we presentresultsof a simulationmodel to test
theimpactofmammalian
is sufficiently
whether
grazerson vegetation
strongthat
fromsteppeto tundra
theloss ofthegrazingmegafauna
couldcause a transition
in Beringia(fig.1). The modelwas originally
developed(Zimovand Chuprynin
ofvegetation
based on patterns
ofannual
1991)to predicttheglobaldistribution
radiationinputand precipitation,
competition
amongfunctional
groupsofplants
and water),and grazingby large
determined
resources(radiation
forclimatically
betweengrazing
mammals.In thisarticle,we applythemodelto theinteraction
and climatein Beringia.
A MODEL SIMULATION
OF MEGAFAUNAL
IMPACTS IN THE FAR NORTH
Overviewof Model
The model has threefunctional
groups:"trees" (woody plants,including
shrubs),"grasses" (herbaceousvascularplants),and "mosses" (nonvascular
maximum
plants,including
lichens).Each functional
grouphas a characteristic
whensuppliesof light,water,or nutrients
are
growthratethatis diminished
a group'sresource"demand,"
Thisgrowthrate,whichdetermines
suboptimal.
thataredetermined
is further
modified
coefficients
bycompetition
bythepriority
HERBIVORE-DRIVEN
BIOMESHIFT
777
of access of each groupto a limiting
resource(i.e., radiationor water).For
example,mossescompetewithtreesandgrassforwaterbutnotforlight(because
oftheirshorter
stature);treesandgrasscompetewithone anotherforlightinthe
Far Northwheretrees(i.e., shrubs)are short,but elsewheretreesare better
forlightthanare grassesand mosses.Comparablerulesofcompeticompetitors
tionforwaterare governedby rootingdepth.The modelis outlinedbriefly
in
appendixB and describedin detailelsewhere(Zimovand Chuprynin
1991).
Nutrient
supply,whichis linkedless directly
to climate,is assumedto affect
competition
through
differential
effectson growth(i.e., responseof grasses>
trees> mosses) (Chapinand Shaver1989)ratherthanbeingthe resourcefor
whichplantscompete.Nutrient
supplycan be variedin the modelto simulate
theincreasedsoilfertility
associatedwithPleistoceneloess deposition.
Mammalian
grazersaffectvegetation
through
consumption
and destruction
of
biomass.We assumethatgrazershave no long-term
detrimental
effecton grass
biomassina steady-state
ecosystem
controlled
byclimateandpredators
because
predators
prevent
overgrazing
on thelongtimescales(centuries)
simulated
bythe
in tundracompensateseffectively
model,and grasslandproduction
forgrazing
through
a varietyofecosystem
feedbacks(Peshkovaand Andreiashchkina
1983;
ofthemodelwerequalitaCargillandJefferies
1984;Kucheruk1985).Predictions
whenthisassumption
was relaxedtoallowgrassresponsetograzing
tivelysimilar
to rangefrommoderately
detrimental
to moderately
stimulatory
(app. B)-that
is, therangeofgrazingresponseobservedin naturalecosystems.
Climaticdata(radiation
wereestimated
foreach terresinputandprecipitation)
trial50 gridpointof longitudeand latitude(Budyko1984).The model,which
includesgrazingas a naturalprocess,was solvedfortheequilibrium
biomass(B)
ofeach functional
group(dBldt= 0) at each 5?gridpoint,assumingeach offour
valuesofnutrient
to estimatepatterns
offunctional-group
availability,
composition.At the two intermediate
soil fertility
of
levels,the simulateddistribution
functional
bothwithinBegroupscloselymatchedobservedvegetation
patterns
modelvalidation.
Fromthesedatawe deterringiaandglobally(fig.2), providing
thatcouldbe occupied
minedthecombinations
of Beringian
climaticconditions
and fertile
soils.
by each functional
groupon infertile
withan annualtimestepto simulate
The modelwas thenrunto equilibrium
inproductivity
andinfertile
soilsunder
ofeachfunctional
patterns
grouponfertile
a representative
PleistoceneBeringian
scenarioofcool climate,loess deposition,
ofpossiblechanges
and presenceoflargegrazers.We thenranfoursimulations
that
fromPleistoceneto Holoceneconditions
(table3): thecomplexofconditions
elimination
ofgrazers,
changedat theendofthePleistocene(climaticwarming,
climaticwarming;
elimination
ofloess depoandelimination
ofloess deposition);
in themodel.
oflargegrazers.We didnotincludeCO2 effects
sition;elimination
ofsoilfertility
was runundertwoconditions
Each ofthesesimulations
(to reprein nutrient
and geologicvariation
senttopographic
supply)and twoinitialdensitiesof colonizingspecies(i.e., mossesand trees)untilbiomasscame to equilibriumwiththe new conditions.A 10-foldvariationin initialcolonizerdensity
alteredtherateofvegetation
changebutnottheequilibrium
speciescomposition,
colonizerdensity
so we presentresultsfromonlythehigher
(table3). The climatic
J~~~~
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HERBIVORE-DRIVEN
BIOME SHIFT
779
TABLE 3
FROMPLEISTOCENE
CHANGES
IN MODELPARAMETERS
TO SIMULATE
POSSIBLECHANGES
TO HOLOCENECONDITIONS
Model Assumptions
Pleistocene conditions
Holocene conditions:
Eliminationof large grazers
Eliminationof loess deposition
Climaticwarming
Climaticwarming,eliminationof
grazers,and eliminationof
loess deposition
Potential
Evapotranspiration
(mm yr-')
HerbivoreImpact
on Moss Biomass
Soil Fertility
350
.5
1.3,1.6
350
350
400
.2
.5
.5
1.3,1.6
1.0,1.3
1.3,1.6
400
.2
1.0,1.3
NOTE.-Initial Pleistocene vegetationhad a greaterbiomass of grasses (Bg = 0.25) than of trees
and mosses (Bt = B,il = 0.1). Identical equilibriumvegetationcomposition occurred with a low
densityof initialcolonizers (Bt = Bi,l = 0.01). Parametersare definedin appendix A.
warming
scenariowe presentis therangefromPleistoceneto presentinincoming
netradiation(potential
evapotranspiration
[PET] increasedfrom300 to 500 mm
sceoftheseresults,we rerantheclimatewarming
yr-1) To testthegenerality
netradiationcurrently
reported
nariowithPET = 600 mmyr-1(themaximum
differed
inBeringia)andfoundthatthisextreme
climaticwarming
only
anywhere
fromthe"realistic"scenario.We do notpresentdatafromthismaximal
slightly
climatic warming.
Model Restults
Whenthemodelwas runforall terrestrial
itgavea realistic
climates,
geographithat
cal distribution
of each functional
group(fig.2), whichgave us confidence
themodelreasonably
controls
overvegetation
districapturesthegeneralclimatic
biomassofmabution,assuminga naturalgrazingregime.Whentheequilibrium
jor functional
groupswas calculatedin BeringiaunderPleistoceneconditions,
undertheentirerangeofclimaticconditions,
mosseswere
grasseswereabundant
to thewarmest,wettestcliabundantin dryclimates,and treeswererestricted
is consistent
withthePleistoofsoilfertility
mates,regardless
(fig.3). Thispattern
of thesegrasslandsby climate,
cene pollenrecordand withthe maintenance
grazers,or loess deposition.Whengrazerswereremovedin themodel,mosses
and trees
expandeddramatically,
grassesdeclined(especiallyat low fertility),
increasedslightly.
a changeintheclimatefromPleistoceneto HoloBy contrast,
cene conditionsresultedin a largeincreasein treesundermoistconditions,a
changein themoisture
dependenceof mosses,and modestchangesin grasses.
reducedgrassgrowthand
The loss ofloess depositionunderinfertile
conditions
enhancedtreegrowthbuthad no majoreffecton mosses. Underfertileconditions,the loss of loess depositionhad no majoreffecton speciescomposition.
The changefromPleistoceneto presentconditions
in all threeparameters
(graza
and
and
caused
of
mosses
ers,climate, loess)
completereplacement grassesby
and coexistenceof all threetypesat highersoil fertility,
treesat low fertility
A 11 09MOSS
Oj7Oj50.3 0;1
40
E
0.6
GRASS
0.4
0.2
0
TREES
22101940
RPLEISTOCENE
a 380
360
340
320
300
400
CHANGE
IN
GRAZING
380
zfw340
300
400
1
LOSS
OF
LOESS
z
360
340
0
320
LU
300
500
CHANGE
IN
480
0
A.
~~~~~~~~~~~~~~CLIMAT
440
420
400
500
CHANGE
a
480
-CLIMATE,
460
440
~~~~~IN
LOESS,
AND
GRAZING
~400
400
2.7
Drier
2.1
1.5 0.9 3.3
2.7
2.1
1.5 0.9 3.3
INDEXOF ARIDITY
2.1
2.7
-
b
1.5 0.9
Wetter
groupsunderthe rangeof
FIG. 3.-Predictedequilibrium
biomassof majorfunctional
and indexofaridityin Beringiaand
evapotranspiration
of potential
Pleistoceneconditions
loss of
underfourpossiblescenariosof changefromPleistoceneto Holoceneconditions:
andcombined
ofloessdeposition,
climatic
changeinall condiwarming,
grazers,elimination
loss of loess deposition,
and loss of largemammalian
tionsincluding
climaticwarming,
scenariosbeganwithPleistoceneconditions(>99%o
grazers.Each of thesebiome-change
ofcolonizers(Bi = B, = 0.01),moderatedensityof
grass)and was testedat low densities
colonizers (Bm = B, = 0.1), and low fertility
(s = initialfertility= 1.0; A) and highfertility
= 1.3; B). Equilibrium
of initialcolonizer
biomasswas independent
(s = initialfertility
andexplanation
oftermsand table3 for
density.See appendicesA and B forthedefinition
values.
parameter
;
B
E
GRASS
MOSS
1I
0i9
0i
7 0j503
0.6
0.4
380
0.2
TREES
1
ino
r
0
aPLEISTOCENE
360
340
320
300
400
CHANGE
IN
380
z
GRAZiNG
340
OF
co380
0
-320
4300
1L-
400
X
~~~~~~~~~~~~~~~~~~~~~OLOSS
LOESS
E360
0.
4320
LU
3no
|
.
_|5CIMT
_CHANGE
500
4
~~~~~~~~~~~~~~~~~~~~
CLIMATE
zP480
uI
0
0.
460
440
420
400.
500
CHANGE
IN
CULMATE,
LOESS,
AND
GRAZING
480
460
~~~~~~~~~~~*
440
32420
0
40
3 .3 Li
Drier
L IS1.
0.9 3.3
Li7
1
1.5 0.9 3.3
INDEXOF ARIDITY
781
Li
27
-
1L i 15
0.9e
Wetter
782
THE AMERICANNATURALIST
in northern
Beringia.These results
patternssimilarto thoseobservedpresently
especiallygrazersandclimate,couldcause
suggestthatchangeinseveralfactors,
a biomeshiftfromdominanceby grassesto dominanceby mossesand shrubs
as a singlefactor
andthatneither
climatechangenorloss ofgrazerswas sufficient
Holocenevegetation.
changefromPleistocene-to
in causingobservedvegetation
to vegetation
In summary,
themodelsuggeststhatmanyfactorscontributed
butthatclimatewarming
was parboundary
changeat thePleistocene-Holocene
ticularly
important
to theinvasionof woodyplantsand thattheloss of grazers
hadthegreatest
effect
on thebalancebetweenmossesandgrasses.Theseresults
whereclimatepermits
withpaleorecords
a switchtoforest
areconsistent
showing
formtoreachlargesize. However,itsuggests
thatloss ofgrazers
a woodygrowth
in areaspresently
occuwas criticalto theswitchfromgrassto mossdominance
ourcontention
thatextinction
ofthe
supports
piedbytundra.Thus,themodeling
in areaspresently
occupiedby tundra
Pleistocenemegafauna
by humanhunting
mosaicfrompredominance
ofgrasscouldhave causeda shiftin thevegetation
of moss-dominated
tundra,even in the abdominatedsteppeto predominance
sence of a largeclimaticchange.The modelalso suggeststhatotherfactors,
tothischangeandenhanced
particularly
changesinclimateandloess,contributed
growth
ofwoodyplants.
RECONSTRUCTION
OF THE MAMMOTH-STEPPE
ECOSYSTEM
A large-scale
reintroduction
ofmammalian
grazersto tundrawouldbe thebest
model.Muskoxenhavebeen successvalidation
ofoursimulation
experimental
Siberiaand northern
Alaska (Klein 1988),and
intonorthern
fullyreintroduced
of centralAlaska (Guthrie1990).
bisonhave been broughtintothe mountains
demonstrate
thatlargemammalian
grazerscan withstand
These reintroductions
whenhuand successfully
current
climaticconditions
exploittundravegetation,
manhunting
Beringia
is controlled.
Moreover,mammoths
persistedin northern
et al. 1993).
until3,700yrB.P., whenprotected
fromhumanhunting
(Vartanyan
is globallyimportant
beofgrassland-grazing
ecosystems
The reestablishment
cause grasslandshave been morestrongly
change
impactedby anthropogenic
the worldthanany otherecosystemtype,bothby conversionto
throughout
ofnativefauna.The RussianFar Northis perhaps
andbyoverhunting
agriculture
of grassland-grazing
the onlylargearea wherethe reconstruction
ecosystems
1989;Zimov 1990).Here, fragments
mightbe attempted
(Zimovand Chuprinin
ofthesteppevegetation
occuron dry,south-facing
slopes(Yurtsev1982;Murray
et al. 1983),and meadowsof sedgesand grassesoccur alongriversand thermokarst
depressions
(alases).ThesespeciesprovidethegeneticbasisofBeringian
ifcompetition
andmight
from
expandintootherenvironments,
steppevegetation
by mammalian
grazers.
mossesand othertypicaltundraspecieswerecontrolled
we initiated
an experiment
to generatea populationof
To testthishypothesis,
wildYakutianhorsesin thelowlandtundraof Kolyma,100kminlandfromthe
foalsweretransplanted
500kmfromthesouth.
ArcticOcean. In 1988,25 yearling
and
are
without
food
acclimatized
supplemental
reproducing
Theysuccessfully
herd
The
the
was
or water(Zimovand Chuprynin
assistance
given
1991).
only
HERBIVORE-DRIVEN BIOME SHIFT
783
protection
frompoachers.In areas in whichtheactivity
of thisherdis concentrated,grassesincreasedin abundance,whilemosses declined(S. A. Zimov,
F. S. ChapinIII, andJ. F. Reynolds,personalobservation),
consistent
withour
hypothesis
thatgrazingmammals
can generategrass-dominated
vegetation.
Caribou and reindeer,whichwere also important
componentsof the Pleistocene
megafauna,
are stillimportant
herbivores
in thenorthbuteat shrubsand lichens
morethangrasses.The maintenance
of an effective
grazingregimecould be
improvedby addingothergrazerstypicalofthePleistocenesteppe(e.g., bison,
muskoxen). Predators,
suchas thetiger,werealso essentialcomponents
ofthe
Pleistoceneecosystem
(Vereshchagin
1988).TheAmurtigeroccursintheRussian
Far East and formerly
extendedintocold regionsof centralYakutia.This tiger
is presently
an endangered
speciesbecauseofa lackofsuitableprey.Largecats
have beenimportant
components
ofall grazingecosystems.If introduced
to the
north,the tigercould servethe dual purposeof providing
a viablehabitatfor
tigersand controlling
grazerdensityin Beringia.
has important
Steppereconstruction
implications
forcurrentecologicaland
social problems.Northern
mossand forestcommunities
are sensitiveto human
disturbance
Siberiais currently
a regionofwide(Kriuchkov1973),andnorthern
spreadhumandisturbance
(Zimov1990).Because grassesand othersteppespeto disturbances
suchas humanactivity
cies areless sensitive
(ChapinandShaver
tundraareas to steppe
1981),it maybe easierto convertsomehighlydisturbed
thanto restoretheoriginaltundra.If steppereconstruction
weresuccessful,the
grazingmammalscouldprovidea sustainablefoodsourcefornorthern
peoples
and a modelforreconstruction
ofgrazingecosystemsthroughout
theworld.
CONCLUSION
We willneverknowtherelativeimportance
ofthemultiple
causesofthetransitionfromsteppeto tundraat theendofthePleistocene.The keystone-herbivore
forthehigh
discussedhere,however,providesa plausibleexplanation
hypothesis
of foragespeciesthatmusthave been necessaryto supportmegaproductivity
faunain a Pleistoceneclimatethatwas colderthanat present.Ouranalysisindicates thatnorthern
grazershave sufficiently
largeimpactson vegetationand
to predict
ecosystemprocessesthattheirrolemustbe consideredin anyeffort
ofpastor future
thepatternandproductivity
vegetation.
are mammalian
Underwhatcircumstances
herbivoreslikelyto cause large
biomeshifts?In forestedregions,mammalspreferentially
browseearlysuccessional species,whichspeeds successionand increasesthe abundanceof latesuccessionalforestsin the landscape(deToitet al. 1991;Pastoret al. 1993).
at ecotonesbetweenbiomes,whereclimateis suitable
However,it is primarily
formore thanone ecosystemtype,thatmammalswill have theirgreatestimpact.
Here overgrazingcan shiftthe balance between tundraand steppe (this article)
or betweengrassland,shrubland,and desert(Schlesingeret al. 1990),whichcould
on thebasis ofvegetation
cause changesthatcouldnotbe predicted
responseto
climate.
THE AMERICAN NATURALIST
784
ACKNOWLEDGMENTS
S. Bret-Harte,J. Bryant,M. Edwards, D. Goldberg,
We thankS. Armbruster,
D. Guthrie,M. Guthrie,S. Hobbie, J. Pastor, M. Power, and H. Reynolds for
criticallyreviewingthe manuscript.The collaborative research was funded by
the Russian Fund of FundamentalResearch and the U.S. Departmentof Energy.
APPENDIX A
TABLE Al
DEFINITION
Symbol
OF SYMBOLS AND UNITS USED IN THE MODEL
Description
Value(s) Used
in Simulations
AET
a
ao
Climaticmaximumpotentialevaporationrate (mm yr-1)
Growthrate (yr-I)
Maximumgrowthrate underoptimalresources (yr-I)
Computed
Computed
ao = 8, ao = .4,
a'
B
b
c
Resource-determined
growthrate (yr-V)
Plant biomass (kg m--)
Scalar governingnutrientsupplyto plants
Rate of biomass loss to grazingand tramplingby herbivores
d
Natural mortalityrate (yr-')
Computed
Computed
Computed (0-1)
cv = 0, c,, = 1,
c, = .1 c,,
d,,,+ ,,, .25,
dg + rg
1.5,
(yr-')
.2
a=
=
=
e
F
GPP
g
Ia
Kii
L
in
n
Fractionof AET due to transpiration
(0-1)
Rate of resource consumptionby the plant community(mm
yr-1)
Gross primaryproductivity
(kg m- yr-')
Subscriptindicatingvalues forgrasses
Index of aridity(PET/PPT)
Competitioncoefficientdescribingeffectof species i on species j (0-1)
Latent heat of evaporation(kcal m-3)
Subscriptindicatingvalues formosses
Coefficientgoverningplant nutrientrequirement(dimensionless)
PET
PET*
PPT
Potentialevapotranspiration
(mm yr-V)
Maximumpotentialevapotranspiration
(mm yr-V)
Precipitation(mm yr-1)
R
Radiation input(kcal cm-2 yr-')
r
Respirationrate (yr-V)
Coefficientgoverningeffectof soil fertility
on nutrientsupply
(dimensionless)
Transpirationrate (mm yr-')
Subscriptindicatingvalues fortrees
Maximumpotentialgross productivitycorrespondingto complete consumptionof the limitingresource
Rate of supplyof limitingresource (mm yr-')
Coefficientgoverningclimaticinfluenceon nutrientsupply
Constantrelatingproductivity
to transpiration
(mm m2kg-')
s
T
t
ii
V
w
51
d, + tt = .06
.8
Computed
Computed
Computed
Computed
.59
ng = 1, n,, = .01,
nt = .33
Computed
850
Varies, typical
values = 140-600
Varies, typical
values = 175-250
See d
.7-1.6
Computed
Computed
Computed
Computed
250
HERBIVORE-DRIVEN
BIOME SHIFT
785
APPENDIX B
BRIEF DESCRIPTION OF THE MODEL
The model addresses vegetationchangeover longtimescales(decades to centuries)and,
therefore,excludes seasonal and demographicprocesses. In this version, we also ignore
abiotic disturbanceand insectherbivory.The model is runwithan annual timestep under
constantconditionsto determinesteady-statevalues of biomass (dB/dt = 0). Whereas the
originalmodel was programmedin FORTRAN (Zimov and Chuprynin1991), to examine
model structureand confirmits behavior,we reprogrammed
the model in Stella (Stella II
User's Guide 1990) and C++ based on the descriptiongivenbelow and elsewhere (Zimov
and Chuprynin1991) and obtained similarresults. All symbols and units are definedin
appendix A.
UNIFORM VEGETATION MODEL
First, we describe the general structureof the model in termsof a homogeneousplant
community.Change in biomass is given by
dB
dt= (a - r - d - c) B,
(B 1)
whereB is the communitybiomass per unitarea, a is the growthrate, r,is the respiration
rate, d is the mortalityrate, and c is the rate of biomass loss to grazingand tramplingby
herbivores.The value of a is a functionof ar, a resource-determined
growthrate, and the
balance between the supply of the limitingresource (V) and rate of consumption(F) by
the community,thatis,
(V(F)
a = ar. (V
F)
(B2)
In this versionof the model, we considertwo climate-relatedresources to be potentially
limiting-waterand nutrients.
Inflluenceof WaterAvailability
The relationshipof wateravailabilityto communityproductivity
is incorporatedintothe
model via its effectson V and F using two general relationships.First, across various
ecosystems,gross primaryproductivity(GPP) is approximatelyproportionalto transpiration(T) (Rosenzweig 1968; Leith 1975). Thus, the rateof consumptionof water(F), which
is equal to T, is given by
F=
f GPP = f a B,
(B3)
where fl is a proportionality
constant(250 mmm2kg-') (Leith 1975). The second generalizationis thatthe supplyofwaterfortranspiration
(V) tendsto be limitedacross ecosystem
types eitherby precipitation(PPT) in arid and semiaridclimates or by the evaporative
climate (i.e., potentialevapotranspiration,PET) in subhumidand humid climates. We
use Budyko's (1984) simple approach to quantifythe trade-offbetween PPT and PET in
controllingactual evapotranspiration(AET) and ultimatelyV (AET minus evaporation).
This approach is based on thefactthatover a sufficient
periodoftime(e.g., week, month),
PET is highlycorrelatedwith solar radiation(R) across many communities(Campbell
1977; Jensenet al. 1990), such thata reasonable approximationis
PET=
R
L
(B4)
whereL is the latentheat of vaporization.The crossoverpointon the climaticcontinuum
between PPT and PET controlof AET is then determinedby the ratio of PET to PPT,
which Budyko (1984) refersto as the index of aridity(Ia):
THE AMERICAN NATURALIST
786
I - PET
a
PPT
_
-
RIL
PPT
(5
(B5)
The climate-controlled
AET forthe communityis thus determinedas
forIa < I
>
1PPT forIa_
PET
AETr
(B6)
The value of AET, whetherfromPET or PPT, however,representsthe supplyof water
and evaporation.Therefore,we definee as the fractionof AET due
forboth transpiration
to transpiration,so that
(B7)
V= e AET.
Althoughe depends primarilyon plant cover, the type of community,and, to a lesser
extent,the degree of stomatalcontrolof waterloss (Jarvisand McNaughton 1986; Jensen
et al. 1990),we use a constantvalue of 0.8 forthe simulationspresentedhere.
Influenceof Nutrients
Nitrogenand othernutrientsgenerallyaffectmechanismsby whichlong-termwaterand
radiationbalances governproductivity(Gutierrezand Whitford1987; Chapin et al. 1988;
Vitousek and Howarth 1991). Hence, climaticeffectsof nutrientsupply on productivity
are included via theireffectson the growthrate, a, which fromequations (B2)-(B3) can
be writtenas
ar.
ar
V
(B8a)
aB+V
where
ar =ao? b,
b
=
(B8b)
1- exp
(B8c)
and
=
'PET-P-PT
[2 . .PET* - PET]
0.43 [PET*]2
e
I/la)
(B8d)
In this equation, a? is the maximumgrowthrate given optimalresources, b is a scalar
parameterthat varies with
(0-1) governingnutrientsupply to plants, s is a soil fertility
soil type (sandy soils < loams) and increases under conditions of loess deposition, w
describes the climatic influenceon nutrientsupply, n is a parameterthat determinesa
plant's demandfornutrients(0, low requirement,to 1, highrequirement),and PET* is set
to 850 (evaporation equivalent of solar radiationobserved at a net radiationof 30 kcal
cm-2 yr-ithe net radiationgivingmaximumproduction;neitherlightnor waterlimited)
(table 1). Also, w is an empiricalfunctionthat assumes nutrientsupply is maximal at
intermediatevalues of PET and Ia' with nutrientsupply being reduced at low and high
PET due to temperatureeffects,at highIa due to drought,and at low Ia due to leaching
losses. Detailed justificationforequation (B8d) is given elsewhere(Zimov and Chuprynin
1991).
MODEL FOR COMPETING FUNCTIONAL GROUPS
CompetitiveInteractions
We now divide vegetationinto threefunctionalgroups: grasses (herbaceous vascular
plants), mosses (includinglichens), and trees (includingshrubs), indicatedby subscripts
g, m, and t, respectively.These functionalgroups compete for the general resource V.
HERBIVORE-DRIVEN
BIOME SHIFT
787
The rate of resourceconsumptionby each functionalgroupis determinedby its consumption rate (Fj, wherej = g, m, t) and thatof its k competitors.Thus, followingequations
(B2)-(B3),
V- F, - Fkj
aj=
a7
,
(B39)
g, m, t and i # j). For example,
whereFj = Q aj Bj, and Fkj = Kji Qf ai Bi (i
the value of V - Fkj, in the case withj = g, is the resource supplyavailable to grasses,
and Kii is the competitioncoefficientdescribingthe effectof mosses and trees (i = in, t)
on resource captureby grasses (0 < Kii ' 1). If canopy or roots of any group i are in the
same layer as, or higherthan,those of groupj, it is a competitor(Kii > 0), while, if they
are lower, thenKii = 0, and thisfunctionalgroupis not a competitor.If, on the average,
the canopy is lower but its volume overlaps withthatof the higherfunctionalgroup,then
group i is a partialcompetitor.We specifyKii values as functionsof canopy/rootposition
and the radiativeindex of aridity(Ia ).
Functional-GroupParameters
All modelparameterswere estimatedfrommeasurements,experiments,or theliterature,
except fornutrientsupply(s) (eq. [B8c]), a scaling parameterthatwas adjusted untilthe
model gave a reasonable balance of moss and grass. This was determinedby runningthe
model at all 5? terrestrialgridpointsfor each of fourvalues of s (0.7-1.6). A value of s
= 1.3 gave an excellentmatchoftheglobal distribution
offunctionalgroupswithobserved
vegetation(fig.2), and a value of s = 1.0 slightlyunderestimatedthe abundance of grass
(Zimov and Chuprynin1991). We use these values of s to representhigh-and low-fertility
soils in simulationsforBeringia.No othertuningof the model was necessary. Parameters
a?, r, d, and e differamong these three functionalgroups, but we assume that these
parametersare not alteredby climatewithina group(i.e., forany climatewe use the same
parametervalues fora given group). Since we considergeneralfunctionalgroups rather
thanparticularspecies, we assume thatforeach climatethereare species of moss, grass,
and treesforwhichthisclimateis close to optimal.If the actual values ofthese parameters
vary withclimaticzone, this variationis probablysimilarformosses, grasses, and trees
and, therefore,would not alterour predictionsforthe outcome of competition.For example, we assume thatgrowthrate (a) for northernmosses, grasses, and trees is the same
as in the south. In the north,however, the total resource supply (V) is less, so that
production(GPP) is less than in the south. We assume that ao = 0.4, ao = 8.0, ao =
0.2-that is, thatthe maximumrelativegrowthrate (RGR) of grasses is greaterthan that
of mosses, which is greaterthan thatof trees (Grimeand Hunt 1975; Furness and Grime
1982). The loss of biomass of mosses, grasses, and trees throughdeath and respirationis
dM,+ r,,,= 0.25, dg + rg = 1.5, and d, + rt = 0.06 yr-1,respectively;thatis, growth-form
differencesin senescence and respirationparallel those in relative growthrate (Langer
1966; Chapin 1980). We assume that,in the absence of competitors,grasses, trees, and
mosses may grow in any climateif the nutrientsupplyis adequate. We tested the model
withtwo initialdensitiesof colonizingspecies (B,, = Bt = 0.01, 0.1) relativeto the density
of grass (Bg = 0.25).
The competitioncoefficientswere estimatedas follows. Under arid conditionsin Beringia,mosses (includinglichens) have ready access to limitedprecipitationand tolerate
dry conditionsmore effectivelythan do grasses and trees. Mosses, therefore,displace
and K,1,
grasses and trees in extremelydryclimates:As Ia goes fromzero to infinity,
K,mg
go fromzero to one. This patternis particularlyevidentin northernregions(Alexandrova
1980; Wielgolaski et al. 1981). However, grasses and trees are superior competitorsto
mosses forlight,because mosses are beneaththe vascular plantcanopy. Therefore,as Ia
and K,r go fromone to zero. In order to make this a
goes fromzero to infinity,
Kg,m,
smoothfunctionof Ia (vs. an abruptthreshold)thatcan be readilyincorporatedinto the
analyticalsolutionof the model, we used the empiricalfunction,p = (1 - exp[ - 1.23
betweenzero and one. At highIa (arid climates)
Ia])2, whichproduces a smoothtransition
THE AMERICAN NATURALIST
788
p = 1, and at low Ia (wet climates)p = 0. The justificationforthisfunctionis discussed
= Kt
elsewhere (Zimov and Chuprynin1991). Therefore,Kg,n= Kt,n= 1 - p and K,11g
= p.
In tundra,where PET < 300 mm, competitionbetween trees and grasses is always
reciprocal (Ktg = Kgt = 1) because trees (actually shrubs) and grasses are similarin
height.In the boreal-tundratransition(300 < PET < 400), the relationshipbetween trees
and grasses depends on both moistureand energy.In warm, wet climates trees always
compete withgrasses, whereas grasses are generallynot competitorswithtrees, because
lightis the limitingfactorin wet climates(i.e., Ktg = 1, Kgt = 0). As radiationdeclines
(PET goes from400 to 300 mm) or as the climate becomes drier(Ia goes fromzero to
one), grasses have a progressivelygreatereffecton trees (includingshrubs).Taking these
conditionsinto account,
Kgt
'pt+K*
where
K*
=
ifp+K*-1
ifp+K*<l,
I1,
ifPET - 300
(400-PET)/100,
if300 < PET < 400
40,
(BiG)
ifPET?-400.
nutrientsinfluencetheoutcome
Althoughgroupsdo notexplicitlycompetefornutrients,
nutrientrequirement(n), a factorthat
of competitionbecause each species has a different
influencesits maximumgrowthrate (a0) (Ingestad and Agren 1991). We assume thatthe
grass requirementfor nutrientsis ng = 1, that trees have a lower nutrientrequirement
because of theirslower biomass turnover(nt = 1/3)(Berendse et al. 1987; Chapin 1993),
and thatmoss growthis not nutrientlimited(n,,,= 0.01) (Skre and Oechel 1979).
Effectsof Grazers
We assume thatthe rate of biomass loss to mammaliangrazersis proportionalto grazer
biomass, which, in turn,is proportionalto biomass of theirfood, which consists, by
of biomass for grasses,
definition,mainlyof grass (Bg). Thus, consumption/destruction
mosses, and trees are (fromeq. [B11])cg *Bg, C,2 Bg, and ct * Bg, respectively,where ci
is the sensitivityof each species to a given grazer biomass. We assume that over long
timeperiods (decades to centuries)predatorskeep herbivoredensityat a level optimalfor
grass growthso thatovergrazingdoes not occur. Since moderategrazingpromotesgrowth
of grasses in tundra(Peshkova and Andreiashchkina1983; Kucheruk 1985), the negative
impact of grazers on grasses is compensatedby a positive one, so that cg = 0; that is,
grazers have no long-termdirect effecton grass biomass. The net result is that in an
ecosystem in which there is no huntingand grazers are in equilibriumwith theirfood
supply,grazers have an intermediateeffecton mosses (c,,, = 0.5), which decline (ct 0.2) whenlargegrazersare absent(i.e., whenonlysmallgrazerslike lemmingsare present).
Lastly, we assume thattrees are an orderof magnitudeless sensitiveto the presence of
grazers than are mosses (ct = 0.1 * c,72).
We did an extensiveanalysis of the sensitivityof our model resultsto our assumption
thatgrazers have no long-termdirecteffecton grass biomass. For each set of conditions
illustratedin figure3, cg was varied from -0.1 c cg C 0.1, in incrementsof 0.05, and
compared to finalbiomass when cg = 0. The maximumbiomass differencewas less than
10% and did not change any of the patternswe observed when cg = 0.
The CommunityModel
Combiningthe above equations, we can include the effectsof competitionand grazing
on changes in biomass of each functionalgroup:
dBg
dt= (ag - rg- dg - C ' Bg) BV B g- 0,
(BlIla)
HERBIVORE-DRIVEN
dt = (a,12-r,1 -d,7
-
BIOME SHIFT
789
>
(Bllb)
C,i Bg), B,2 B, ?0
and
dB
dt
(at
- it-
BtBt:-0
d, - ct Bg
Bg)B1,B10,
(Bllc)
where
a,=a?
,(11-
ag=a*(u-ag
at=a,*(u-at*B
B,7 -kg,1 *ag*Bg - kt,,*at.
Bg-k,g *a,
-k,1
, -
B,)/i
,
kg aB)u,
a,* B,1 -kg'
ag *Bg)/u,
and ui = V/fQ,which is the maximumpotentialgross productivitycorrespondingto complete consumptionof the limitingresource.
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