Journal of
Ecology 0887\
75\ 338Ð350
An experimental test of limits to tree establishment in
Arctic tundra
SARAH E[ HOBBIE and F[ STUART CHAPIN III
Department of Integrative Biology\ University of California\ Berkeley CA 83619Ð2039\ USA
Summary
0 Five treeline species had low seed germination rates and low survivorship and
growth of seedlings when transplanted into Alaskan tundra[ Seed germination of all
species increased with experimental warming\ suggesting that the present treeline may
in part result from unsuccessful recruitment under cold conditions[
1 Growth\ biomass and survivorship of seedlings of treeline species transplanted into
tundra were largely una}ected by experimental warming[ However\ transplanted
seedlings of three species "Betula papyrifera\ Picea glauca and Populus tremuloides#
grew more when below!ground competition with the extant community was reduced[
All three measures of transplant performance were greater in shrub tundra than in
the less productive tussock or heath tundra[ Establishment of trees in tundra may
thus be prevented by low resource availability and competition[
2 Two species "Alnus crispa and Populus balsamifera# had low seed germination and
survivorship of germinated seeds^ transplants of these species did not respond to
the manipulations and lost biomass following transplanting into tundra[ Isolated
populations of these two species north of the present treeline in arctic Alaska probably
became established during mid!Holocene warming rather than in recent times[
3 Of all the species studied here\ Picea glauca was the most likely to invade intact
upland tundra[ Its seeds had the highest germination rates and it was the only species
whose seedlings survived subsequently[ Furthermore\ transplanted seedlings of Picea
glauca had relatively high survivorship and positive growth in tundra\ especially in
treatments that increased air temperature or nutrient availability\ two factors likely
to increase with climate warming[
Keywords] Alaskan treeline\ climate change\ Picea glauca\ tree establishment\ tundra
Journal of Ecology "0887# 75\ 338Ð350
Introduction
Both past and present evidence suggest that tem!
perature is a proximate factor limiting the position of
the northern treeline[ For example\ during the middle
Holocene\ when summer temperatures were higher
than they are today\ the treeline extended north of its
present position "Ritchie et al[ 0872^ COHMAP 0877^
MacDonald et al[ 0882#[ Recent warming "during the
past century# has been associated with increased
growth of trees at treeline "Innes 0880^ Jacoby +
D|Arrigo 0884#\ increases in tree densities in forest
stands at treeline "Payette + Filion 0874^ Szeicz +
MacDonald 0884# and northward expansion of tree!
line "F[ Suarez\ D[ Binkley and R[ Stottlemyer\
Þ 0887 British
Ecological Society
Present address] Department of Biological Sciences\
Stanford University\ Stanford CA 83294\ USA[
unpublished data#[ There is also a compelling present!
day correlation between position of treeline and tem!
perature "Sveinbjornsson 0881#[
Numerous hypothesized mechanisms by which
temperature limits treeline have been proposed "Ste!
vens + Fox 0880^ Sveinbjornsson 0881#[ Some of these
mechanisms involve the direct e}ects of low tem!
perature on physiology "e[g[ photosynthesis\ growth\
and nutrient and water uptake# whereas others
involve the indirect e}ects of low temperature on
plant performance "e[g[ negative carbon balance
resulting from the short growing season\ low nutrient
availability resulting from cold soils#[ However\ little
experimental evidence exists to evaluate these hypoth!
eses[
Given the past association of changes in treeline
with climate warming\ future climate warming is also
likely to cause northward treeline expansion "Star_eld
349
Establishment of
trees in Alaskan
tundra
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
+ Chapin 0885#[ Despite the lack of understanding of
current treeline\ elucidating the factors that control
the rate of this expansion is important for several
reasons[ First\ because of the relatively low albedo of
boreal forest\ replacement of tundra by boreal forest
is likely to exacerbate warming that results from the
rising concentrations of greenhouse gases "Bonan
et al[ 0881^ Foley et al[ 0883#[ Secondly\ knowing the
future areal extent of the boreal forest is necessary
for predicting future carbon storage by the biosphere
"Prentice + Fung 0889^ Smith + Shugart 0882#[ Third\
boreal forests are of large economic interest[
In this study\ we examined limitations to tree estab!
lishment in Alaskan tundra\ where\ at present\ north!
ern treeline coincides with the south slope of the
Brooks Range and the range limit of Picea glauca
"Viereck 0868#[ We hypothesized that\ although
warmer temperatures would directly enhance seed
germination\ the survivorship and growth of seedlings
would be limited by factors that in~uence below!
ground resource availability\ namely competition
with tundra species and site fertility[ We focused our
study on four trees "Betula papyrifera Marsh\ Picea
glauca "Moench# Voss\ Populus balsamifera L[\ and
Populus tremuloides Michx[# and one shrub "Alnus
crispa "Ait[# Pursh# that currently exist at treeline in
northern Alaska[ Two of these species "P[ balsamifera
and A[ crispa# also occur in isolated stands north
of the Brooks Range "Viereck 0868^ Murray 0879^
Edwards + Dunwiddie 0874#[
Fairbanks\ and examining genotypic variation in
response to our manipulations was beyond the scope
of this study[
Materials and methods
SEED!SOWING EXPERIMENT
Our experimental site at Toolik Lake\ Alaska
"57>27?N\ 038>23?W\ elevation 659 m a[s[l[#\ is in the
northern foothills of the Brooks Range[ Treeline pre!
sently occurs 49 km south of Toolik Lake\ on the
southern slope of the Brooks Range\ although iso!
lated populations of both A[ crispa and Populus bal!
samifera occur within 19 km of Toolik Lake[ Tree
seeds for all experiments were obtained primarily
from Fairbanks\ Alaska "53>42?N\ 036>34?W#[ The
remote location of the Alaskan treeline made it
impossible to collect adequate seed there\ particularly
given the large number of experimental treatments
and species compared "see below#[
Fairbanks has a warmer climate than the treeline\
which in turn is warmer than our study site in the
northern foothills[ Comparative climate data for
0864Ð65 indicate that the number of thawing degree
days were 39Ð099) and 09Ð59) greater at Fairbanks
and treeline\ respectively\ than in the Toolik region
for these two years "Haugen 0868#[ Measurements
made in 0883 indicate a growing season "01 JuneÐ20
July# air temperature at Toolik Lake of 09[6 >C\ while
for the same period air temperature was 00[6 >C at
treeline and 05[1 >C in Fairbanks "D[ U[ Hooper\
unpublished data#[ Little is known about genetic
di}erentiation among populations from treeline and
To examine temperature limitation to seed ger!
mination in tundra\ we obtained seeds of Betula\ Pop!
ulus balsamifera and P[ tremuloides\ and Picea near
the University of Alaska\ Fairbanks\ and seeds of
Alnus from tundra near Slope Mountain "57>44?N\
037>49?W# on the north slope of the Brooks Range[
Seeds were collected in 0889 from multiple individuals
in single populations and prechilled over winter by
storing them frozen until sowing[
Seeds were sown on 10 June 0880 into a 4 × 1 fac!
torial species × warming experiment in gently sloping
upland tussock tundra[ Four control and four green!
house!covered plots were randomly assigned to each
of the _ve species[ We estimated seed viability immedi!
ately prior to sowing by determining maximum ger!
mination rates for each species on moist _lter paper
in Petri dishes in the laboratory[ Within each plot we
sowed 499 viable seeds into each of two 399 cm1
subplots located in moss mats "dominated by Hyl!
ocomium splendens and Aulacomnium turgidum#[
Because of low germination rates "and thus lack of
su.cient seeds#\ we sowed only 149 viable seeds into
Alnus crispa plots[ We watered seeds once\ on 13 June
0880\ with 049 ml lake water subplot−0[ These seed
densities generally fall within the range of natural seed
rains found in interior Alaska for these species^ they
ESTABLISHMENT OF PLOTS
We established plots in three tundra vegetation types]
a relatively dry lichen!heath tundra\ a more mesic
acidic tussock tundra\ and a wet acidic shrub tundra[
All three sites are within 9[4 km of one another in
the vicinity of Toolik Lake\ Alaska[ The lichen!heath
tundra is located on a well!drained slope at the bound!
ary between two adjacent glacial surfaces "Itkillik I
and II# "Walker et al[ 0884#[ The tussock and shrub
tundra are located on the older of these two surfaces[
The tussock tundra is located on a gentle slope\ but
drainage is impeded by underlying permafrost[ The
shrub tundra occurs along a water track that pri!
marily drains acidic tussock tundra and ~ows into
Toolik Lake[
Within each tundra type\ we established 19 split!
plots[ One half was left uncovered as a control that
experienced ambient climate^ the other half was desig!
nated for cover with a polyethylene greenhouse that
warmed the air[ We constructed polyethylene green!
houses by stapling 9[04 mm polyethylene to irrigation!
tube frames[ Greenhouses were 9[4 m tall^ they were
placed on warmed plots each spring following snow!
melt "mid!June# and removed at the end of each grow!
ing season "mid!August#[
340
S[E[ Hobbie +
F[S[ Chapin
are higher than natural seed rains of Picea glauca and
lower than those of B[ papyrifera "Zasada et al[ 0881#[
To determine seed germination rate\ we counted
seedlings on 29 June\ 01 July\ 20 July and 09 August
0880[ Additional germination occurred in the spring
of 0881 for all but the Populus species[ We counted
seedlings on 0 July\ 00 July\ 11 July and 1 August
0881\ distinguishing new from previous year|s ger!
minants[ We calculated the maximum germination
rate as the sum of maximum numbers of seedlings
counted during 0880 and 0881 divided by the number
of viable seeds sown[ Seedlings were counted again
on 12 July 0882\ 17 June 0883 and 15 July 0884[ We
determined survivorship in any given year by dividing
the number of live seedlings by the maximum ger!
mination[ We compared arcsine square root!trans!
formed maximum germination rates among species
and between treatments using two!way analysis of
variance "ANOVA#[ Low survivorship precluded a sta!
tistical comparison of seedling survivorship[
SEEDLING TRANSPLANT EXPERIMENT
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
We compared direct limitation by temperature with
limitation by competition and site characteristics to
growth and survivorship of seedlings transplanted
into tundra[ We transplanted 1!year!old seedlings of
all _ve species into control and greenhouse!covered
plots in all three di}erent tundra vegetation types
in August 0889[ Seedlings were obtained from seed
collected in Fairbanks and grown for 1 years at the
Alaska State Forest Nursery "Palmer\ Alaska#[ At
the time of transplanting\ randomly selected seedlings
were harvested to determine pretransplant biomass
"n 4 for Populus spp[\ n 09 for all other species#[
Because of the di.culty of warming individual seed!
lings\ we set up a somewhat complicated split!split!
split plot design[ The _rst split refers to the tem!
perature treatment "see establishment of plots#\ the
second split refers to the species of seedling\ and the
third split refers to the competition treatment[
Each split!plot was further split by species] two
seedlings of each of the _ve species were transplanted
into each half of each split!plot[ Because of a shortage
of transplants\ Populus tremuloides and P[ balsamifera
were only planted in 01 randomly chosen plots of the
total of 19 plots within each vegetation type[ Split!
plots containing three species were 9[7 × 9[4 m^ those
containing all _ve species were 0[2 × 9[4 m[
We randomly chose one member of each pair for
a reduced below!ground competition treatment\ and
cut vertically into the peat with a serrated knife down
to mineral soil in an 07!cm circle centred on this
seedling[ Cutting severed the roots of adjacent indi!
viduals in the extant tundra community[ To prevent
root regrowth\ we inserted a sheet of 9[04!mm poly!
ethylene to 09 cm depth in the vertical cut\ except in
the heath site where sheets were inserted to 4 cm depth
because of the rocky soil and shallow organic layer[
We scored transplants for survivorship at the end
of each growing season "late July to mid!August# in
0880Ð82[ We also measured height and the length of
the current year|s growth increment on 09 August
0880 and 20 July 0881[ In early August 0882 we har!
vested all transplants to determine biomass[ We dug
around individual seedlings to recover as much of the
below!ground biomass as possible[ Harvested plants
were divided into above! and below!ground "root#
biomass[ Roots were frozen and returned to the Uni!
versity of California\ Berkeley\ where they were sep!
arated from soil by gently washing them in a water
bath[ Root nodules of A[ crispa were separated from
root biomass[ We separated current from previous
year|s above!ground biomass[ All plant parts were
dried "54 >C# and weighed[
We compared survivorship of transplants among
species\ sites\ warming treatment and competitive
regimes to 0882 using log!linear analysis[ To deter!
mine if survivorship was independent of species or the
various treatments\ we _rst constructed a complete!
independence model "Selvin 0884# that included sur!
vival\ species\ site\ greenhouse treatment and com!
petition treatment[ The model also included all poss!
ible interactions "two!\ three! and four!way# between
species\ site\ greenhouse treatment and competition
treatment\ since the margins were _xed for these fac!
tors by the experimental design[ For this model\ all
possible interactions "two!\ three!\ four! and 4!way#
between survival and the various treatments were set
equal to zero[ If the complete!independence model
did not su.ciently _t the data\ all interaction terms
were added back to the model\ and each was then
eliminated in turn to determine which interaction
terms were necessary to ensure good model _t
"assessed using both log!ratio and chi!square analy!
ses#[
We compared transplant height and current year|s
growth "0880 and 0881# and biomass "0882# for each
species separately using split!split plot analysis of
variance "SSP ANOVA#\ with site as a main e}ect\ the
greenhouse treatment as a split!plot e}ect\ and the
competition treatment as a split!split!plot e}ect[ Low
survivorship of some species prevented analysis of the
data as a complete split!split!split!plot design with
species as the split!split!plot e}ect[ In 0880\ the main
stems of most Populus balsamifera individuals died
back and they resprouted from buds at the base of
the stem[ Since height was almost always equal to
current year|s growth\ only growth was analysed for
this species[ Low survivorship prevented us from
including the heath site in the split!split!plot analysis
for P[ balsamifera in 0881 and for B[ papyrifera in
both 0881 and 0882[ Low survivorship prevented us
from using split!split!plot analysis altogether for P[
balsamifera in 0882 and A[ crispa in 0881 and 0882[
When split!split!plot analysis was impossible\ we
averaged growth\ height or biomass over the two lev!
els of the competition treatment "when both members
341
Establishment of
trees in Alaskan
tundra
of a species!pair survived# and compared sites and
the greenhouse treatment using split!plot analysis of
variance "SP ANOVA#\ with site as a main e}ect and
the greenhouse treatment as a split!plot e}ect[ All
heights\ growth and biomass measures were ln!trans!
formed for statistical analyses[
To serve as a control for possible transplant e}ects
on survivorship and biomass\ we transplanted seed!
lings of each species into a site near Fairbanks\ Alaska
"where these species establish naturally# in mid!July
0889 "n 09#[ The site was located on an upland
south!facing slope above the Tanana River in the
Bonanza Creek Long!Term Ecological Research
"LTER# site UP0 A[ The site burned in 0872 and is
currently dominated by P[ balsamifera trees with scat!
tered A[ crispa seedlings and an understorey of Cal!
amagrostis canadensis[ We scored transplants for sur!
vivorship and harvested them for above!ground
biomass in mid!August 0882[
SITE MEASUREMENTS
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
To characterize the three di}erent sites\ we measured
percentage cover of the dominant plant species\ soil
moisture\ soil pH\ depth to mineral soil and accumu!
lation of nutrients on ion!exchange resins[ To charac!
terize the e}ects of the greenhouse treatment\ we mea!
sured air and soil temperature\ depth of thaw to
permafrost\ and accumulation of nutrients on ion!
exchange resins in greenhouse and control plots in all
three sites[
We visually estimated percentage cover of all plant
species in two 399!cm1 quadrats randomly located
within each control plot[ Values for the two quadrats
were averaged before averaging all plots for a site[
We measured soil moisture gravimetrically "54 >C\ 4Ð
09 cm below the moss or soil surface# in mid!July 0882
at six points in each of the three sites[ At the same
time\ we also measured depth of the organic mat "from
the moss or soil surface#[ pH was measured in soil
collected from the bottom of the live vegetation to
4 cm depth in _ve randomly positioned cores in each
site in late August[ Soil "1 g oven!dry equivalent mass#
was shaken in 19 ml 9[90 M CaCl1 for 29 min before
measuring with a pH meter "Orion Instruments#[ Soil
moisture\ organic horizon depth and pH were com!
pared among sites using one!way ANOVA[
From 0 to 7 August 0882\ we measured air tem!
perature 04 cm above the canopy in heath tundra
"n 3# and shrub and tussock tundra "n 1 for con!
trols\ n 2 for greenhouses#[ Concurrently\ we mea!
sured soil temperature 09 cm below the moss surface
in heath "n 2 for controls\ n 3 for greenhouses#\
tussock "n 2# and shrub tundra "n 1 for controls\
n 2 for greenhouses#[ Temperatures were measured
in randomly chosen control or greenhouse plots using
copper!constantan thermocouples attached to data!
loggers "Campbell CR09 or 10X^ Campbell Scienti_c\
Logan\ UT# that recorded hourly and daily means of
0!min measurements^ replication was limited by the
number of channels available on the datalogger[ Daily
mean air and soil temperatures were compared among
sites and between treatments using repeated!measures
ANOVA\ with day as a repeated measure[
We measured depth of thaw to permafrost twice in
each plot in late July 0882 using a stainless steel probe[
The two measurements were averaged before statis!
tical analysis[ We compared sites and the greenhouse
treatment using split!plot ANOVA with site as a main
e}ect and the greenhouse treatment as a split!plot
e}ect[ Because of the rocky soils in the heath site\ we
were unable to measure thaw depth in this site\ and
we have excluded it from the analysis[
We assessed nutrient availability in the plots using
ion!exchange resins "Giblin et al[ 0883#[ Seven milli!
litres of acid!washed "09) HCl# anion or cation exch!
ange resins were placed in 14!cm1 acid!washed nylon
bags "Dowex 49 W!X7 19Ð49 mesh H¦ or 0!X7 19Ð
49 mesh Cl−\ respectively#[ We placed anion and cat!
ion resin bags at 4Ð09 cm depth in randomly chosen
control and greenhouse plots in each site in mid!June
0881 "n 6 in heath and shrub tundra\ n 5 in tuss!
ock tundra#[ At the end of July 0881\ we replaced
those resin bags with fresh resin bags that we har!
vested the following spring "mid!June 0882#[ After
each harvest\ resins were frozen until extraction with
099 ml of 1 N NaCl "in 9[0 N HCl# through a 29!ml
−
column[ Extracts were analysed for NH¦
3 \ NO2 and
−
PO3 colorimetrically on the Lachat QuickChem
Autoanalyser[ We compared sites and the greenhouse
treatment for each ion separately using split!plot
ANOVA with site as a main e}ect and the greenhouse
treatment as a split!plot e}ect[ Values were ln!trans!
formed for analyses[
Statistical analyses were done using SYSTAT "SYS!
TAT 0881# and JMP Start Statistics "Sall + Lehman
0885#[
Results
ENVIRONMENT
The three sites di}ered in both vegetation and soil
parameters "Tables 0 and 1#[ The heath site was domi!
nated by the ericaceous shrub\ Vaccinium uliginosum\
lichens\ and the mosses Hylocomium splendens and
Aulacomnium turgidum[ The shrub site was dominated
by two deciduous shrubs\ Betula nana and Salix
pulchra\ and the mosses Hylocomium splendens and
Sphagnum spp[ The tussock site was dominated by
species in several di}erent growth forms\ including
mosses "Sphagnum spp[ and Hylocomium splendens#\
deciduous shrubs "Betula nana#\ evergreen shrubs
"Vaccinium vitis!idaea# and the tussock!forming
sedge\ Eriophorum vaginatum[ The heath site had
drier\ slightly less acidic soils and a thinner organic
horizon than the shrub and tussock sites "Table 1#[
The shrub site had greater accumulation of
342
S[E[ Hobbie +
F[S[ Chapin
Table 0 Areal cover ")# of plant species in the three tundra types into which seedlings were transplanted[ Those species whose
cover was ³4) are indicated by dashes[ Values are means "SE#
Tundra type
Species
Heath
Shrub
Tussock
Deciduous shrub
Betula nana
Rubus chamaemorus
Salix pulchra
Ð
Ð
Ð
29[4 "2[7#
5[0 "0[5#
11[9 "2[4#
07[2 "1[9#
4[3 "0[2#
Ð
Evergreen shrub
Vaccinium uli`inosum
Cassiope tetra`ona
Ledum palustre
Vaccinium vitis!idaea
08[1 "1[1#
6[2 "1[2#
Ð
5[1 "0[5#
Ð
Ð
Ð
5[0 "0[1#
Ð
Ð
8[3 "0[1#
09[3 "1[9#
Graminoid
Carex bi`elowii
Eriophorum va`inatum
Ð
Ð
Ð
5[9 "0[1#
02[5 "1[6#
Non!vascular
Aulocomnium tur`idum
Dicranum spp[
Hylocomium splendens
Spha`num spp[
Lichens
00[0 "2[9#
7[8 "1[5#
04[8 "4[2#
Ð
05[4 "1[2#
4[2 "0[8#
Ð
14[8 "6[5#
49[0 "6[8#
Ð
Ð
Ð
6[8 "0[4#
5[9 "0[3#
10[2 "4[9#
Ð
Table 1 Soil properties in the three tundra types into which seedlings were transplanted[ Values are means "SE#[ Di}erent
letters within a row indicate signi_cantly di}erent means "Tukey|s HSD\ a 9[94#
Tundra type
Soil property
Heath
Shrub
Tussock
Organic horizon depth "cm#
pH
Soil moisture ")#
2[2 "9[5#a
2[8 "9[0#a
051 "18#a
09[5 "0[0#b
2[5 "9[0#ab
415 "86#b
00[7 "1[2#b
2[2 "9[0#b
234 "53#ab
ammonium and nitrate on ion!exchange resins during
winter "including spring thaw^ Table 2^ SP ANOVA\
P 9[90 for ammonium and nitrate#[
The greenhouse treatment primarily altered the
above!ground environment "Table 3#[ Air tem!
peratures were signi_cantly warmer in the green!
Table 2 Nutrient accumulation on ion exchange resins "mmol ion bag−0# in three sites and in control and greenhouse treatments
during the growing season "summer# and over winter "which includes soil freeze!up and spring thaw#[ Values are means "SE#
Heath
Nutrient
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
Control
Shrub
Greenhouse
Control
Tussock
Greenhouse
Control
Greenhouse
Summer
Phosphate
9[95 "9[92#
Ammonium 6[03 "9[85#
Nitrate
9[00 "9[90#
9[92 "9[91#
6[27 "0[05#
9[25 "9[13#
9[91 "9[90#
6[90 "9[59#
9[07 "9[96#
9[90 "9[99#
5[87 "9[82#
9[00 "9[91#
9[90 "9[90#
6[20 "9[42#
9[98 "9[91#
9[91 "9[90#
4[63 "9[07#
9[98 "9[90#
Winter
Phosphate
9[08 "9[09#
Ammonium 4[58 "9[18#
Nitrate
9[08 "9[92#
9[55 "9[07#
6[89 "0[06#
9[15 "9[96#
9[01 "9[93#
10[61 "5[15#
4[41 "3[57#
9[07 "9[94#
02[20 "1[29#
4[38 "4[91#
9[33 "9[24#
01[64 "6[12#
9[15 "9[94#
9[43 "9[29#
5[48 "9[38#
9[12 "9[93#
343
Establishment of
trees in Alaskan
tundra
Table 3 Air and soil temperature and thaw depth in control and greenhouse treatments in the three transplant sites[ Air and
soil temperatures are 0!week means of daily means measured from 0 August to 7 August[ Thaw depth was measured in mid!
July[ Values are means "SE#
Site
Greenhouse
Air temperature ">C#
Heath
Shrub
Tussock
7[48 "9[92#
7[72 "9[92#
7[07 "9[92#
8[21 "9[91#
8[30 "9[98#
8[51 "9[12#
Soil temperature ">C#
Heath
Shrub
Tussock
4[38 "9[45#
5[67 "9[69#
4[14 "9[74#
4[09 "9[10#
5[01 "9[64#
4[96 "9[85#
Thaw depth "cm#
Heath
Shrub
Tussock
houses by about 0 >C on average "repeated!measures
ANOVA\ F0\01 099[03\ P ³ 9[990#\ comparable to the
di}erence in mean growing season temperature
between Toolik and treeline south of Toolik "D[ U[
Hooper\ unpublished data#[ Soil temperatures did not
change with greenhouse warming "repeated!measures
ANOVA\ F0\01 9[42\ P 9[37#[ Consistent with the
lack of e}ect on soil temperatures\ greenhouses did
not alter thaw depth "SP ANOVA\ F0\27 0[29\
P 9[15# or the amount of nitrogen accumulated on
ion!exchange resins as ammonium or nitrate "Tables 2
and 3#[ Phosphate was signi_cantly higher in green!
houses in winter "SP ANOVA\ P 9[991#[ Although we
did not measure it\ the greenhouses probably reduced
photosynthetically active radiation by about 19)
"Chapin et al[ 0884^ Hobbie + Chapin 0887#[
SEED GERMINATION AND SURVIVORSHIP
Air warming approximately doubled seed ger!
mination for all _ve species "Fig[ 0^ F0\29 4[53\
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
Control
Ð
12[8 "0[3#
14[5 "0[3#
Ð
14[5 "0[9#
15[1 "0[7#
P 9[91#[ Species also di}ered signi_cantly in their
maximum seed germination rates "F3\29 5[86\
P ³ 9[990#[ Picea glauca and Betula papyrifera had
the highest germination rates\ between 4) and 19)[
All other species had germination rates less than 4)[
By 0884\ most germinants had died "Fig[ 1#[ Only
Picea glauca had signi_cant survivorship of ger!
minants _ve growing seasons after seeds were sown[
TRANSPLANT SURVIVORSHIP AND GROWTH
Three growing seasons after transplanting "i[e[ in
0882#\ seedlings of all species had greater than 79)
survivorship when transplanted into a site where they
would naturally establish "Fairbanks\ Alaska#\ indi!
cating little mortality due to transplanting alone
"Fig[ 2#[ However\ when transplanted into tundra\
survivorship was quite variable[ Survivorship di}ered
signi_cantly among sites\ and was lowest in the heath
site\ particularly for Alnus crispa\ Betula papyrifera
and Populus balsamifera "Fig[ 2 and Table 4^ sig!
Fig[ 0 Maximum seed germination rates of seeds of _ve species sown in tussock tundra in control and greenhouse!treated
plots[ Values are means ¦0 SE[ P[ Populus[
344
S[E[ Hobbie +
F[S[ Chapin
Fig[ 1 Survivorship of those seeds that germinated in tussock tundra in control and greenhouse!treated plots[ Values are
means[ P[ Populus[
Fig[ 2 Survivorship of seedlings transplanted in control and greenhouse!treated plots in three tundra vegetation types[ Sur!
vivorship in the Fairbanks site is included for 0882 only for qualitative comparison[ Survivorship is pooled over the levels of
the competition treatment[ CT control\ GH greenhouse[ Values are means[
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
ni_cant survivorship × site and survivorship ×
species × site interactions#[ Survivorship was also
lower in the greenhouse treatment for all species
except Populus tremuloides "Table 4^ signi_cant sur!
vivorship × species × temperature interaction#[ The
competition treatment had no e}ect on survivorship
of any species "Table 4#[
All species accumulated biomass when trans!
planted into the Fairbanks site "Fig[ 3#[ However\ only
Picea glauca and Populus tremuloides accrued above!
ground biomass when transplanted into tundra[
Above!ground biomass of the other three species
decreased in tundra[
All species except Populus balsamifera responded
signi_cantly to warming in terms of growth "length of
current year|s growth increment# in the _rst and
second years after transplanting "SP ANOVA\
P ¾ 9[90\ data not shown#[ Picea glauca was the only
species that responded signi_cantly to warming in
terms of total biomass by the third year\ having gre!
ater biomass in the greenhouses "Fig[ 4^ SSP ANOVA]
P 9[90#[
Three species responded positively in terms of
growth "current year|s biomass# to decreased below!
ground competition and site variation in productivity[
Betula papyrifera and Picea glauca had signi_cantly
greater growth in the reduced competition treatment
"Fig[ 5^ SSP ANOVA\ P ³ 9[990#[ Betula\ Picea and
Populus tremuloides all had signi_cantly greater
growth in the shrub site "Fig[ 5^ SSP ANOVA\
P ³ 9[90#^ for Betula\ the site di}erences were greater
in the greenhouses "SSP ANOVA\ site × greenhouse
345
Establishment of
trees in Alaskan
tundra
Table 4 Log!linear analysis of survivorship for transplanted seedlings to 0882[ u0 survivorship\ u1 species\ u2 site\
u3 temperature treatment\ u4 competition treatment[ Y1 likelihood ratio statistic^ x1 Pearson chi!square
0882
Term set equal to zero
d[f[
Y1
P
x1
P
All of the below
"complete independence#
u0 × u1 × u2 × u3 × u4
u0 × u1 × u2 × u3
u0 × u1 × u2 × u4
u0 × u1 × u3 × u4
u0 × u1 × u2
u0 × u1 × u3
u0 × u1 × u4
u0 × u2 × u3
u0 × u2 × u4
u0 × u3 × u4
u0 × u1
u0 × u2
u0 × u3
u0 × u4
48
01
19
17
29
27
31
31
33
35
36
36
38
36
37
263[21
09[19
04[63
20[19
22[54
40[13
50[85
41[03
46[71
47[55
47[55
47[55
026[49
47[55
48[58
³9[990
9[59
9[62
9[20
9[29
9[96
9[91
9[03
9[97
9[09
9[01
9[01
³9[990
9[01
9[01
221[00
09[51
04[60
21[00
23[10
42[73
53[09
42[12
59[22
59[84
59[83
59[83
018[02
59[83
51[58
³9[990
9[45
9[62
9[16
9[16
9[94
9[91
9[01
9[94
9[96
9[97
9[97
³9[990
9[97
9[97
Fig[ 3 Above!ground biomass of seedlings before transplanting "initial# and after the _nal harvest "0882# in control plots in
the Fairbanks taiga site and the three tundra vegetation types[ Values are means ¦0 SE[ Missing values indicate no survivorship
in the control plots in a particular site[ P[ Populus[
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
interaction\ P 9[998#[ Betula\ Picea and Alnus crispa
had greater total biomass in the shrub site "Fig[ 4^ SSP
ANOVA\ P ³ 9[990 for Betula and Picea^ SP ANOVA\
P 9[90 for Alnus#[ For Populus tremuloides the total
biomass response was complicated by a signi_cant
site × temperature × competition interaction "SSP
ANOVA\ P 9[995#[ Populus balsamifera responded
little\ if at all\ to any of the treatments in terms of
growth or biomass "Figs 4 and 5#[ None of the species
responded to treatments with change in relative allo!
cation to roots and shoots\ except Betula papyrifera\
for which warming signi_cantly increased the root]
shoot ratio\ particularly in the tussock site "Fig[ 6^
SSP
ANOVA\
site × greenhouse
interaction\
346
S[E[ Hobbie +
F[S[ Chapin
Fig[ 4 Total biomass of seedlings transplanted in tundra in
control and greenhouse treatments and with and without
reduced competition 0882[ For Betula papyrifera\ Alnus cri!
spa and Populus balsamifera\ the heath site is excluded due
to low survivorship[ For A[ crispa and P[ balsamifera\ low
survivorship precluded comparing competition treatments[
Where seedlings in both competition treatments survived\
their biomass was averaged for analyses comparing control
and greenhouse treatments and sites[ ¦comp with com!
petition\ −comp without competition[ Values are means
¦0 SE[
P 9[994^ site × greenhouse × competition inter!
action\ P 9[90#[
Discussion
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
This study suggests that treeline in part results from
the inability of trees to establish in tundra\ even if
dispersal is adequate[ The species examined showed
limited potential for recruitment into upland tundra\
the most widespread tundra community type in
Alaska[ All had generally poor seed germination and
little or no survivorship of seedlings after germi!
Fig[ 5 Current year|s biomass of seedlings transplanted in
tundra in control and greenhouse treatments and with and
without reduced competition in 0882[ For Betula papyrifera\
Alnus crispa and Populus balsamifera\ the heath site is
excluded due to low survivorship[ For A[ crispa and P[
balsamifera\ low survivorship precluded comparing com!
petition treatments[ Where seedlings in both competition
treatments survived\ their growth was averaged for analyses
comparing control and greenhouse treatments and sites[
¦comp with competition\ −comp without compe!
tition[ Values are means ¦0 SE[
nation[ Furthermore\ seedlings transplanted into tun!
dra had poor growth relative to those transplanted
into a site where these species establish naturally[ Our
experiments suggest that recruitment of trees in tun!
dra is currently prevented both directly and indirectly
by cold temperatures[ Seed germination appears to be
directly temperature!limited\ while seedling growth
and survivorship of at least some treeline species is
limited by the availability of below!ground resources\
as indicated by the response of the transplants to site
di}erences and reduced competition[
The positive response of seed germination to warm!
347
Establishment of
trees in Alaskan
tundra
Fig[ 6 Root]shoot ratios of seedlings transplanted in tundra
in control and greenhouse treatments and with and without
reduced competition in 0882[ For Betula papyrifera\ Alnus
crispa and Populus balsamifera\ the heath site is excluded
due to low survivorship[ For A[ crispa and P[ balsamifera\
low survivorship precluded comparing competition treat!
ments[ Where seedlings in both competition treatments sur!
vived\ their root]shoot ratios were averaged for analyses
comparing control and greenhouse treatments and sites[
¦comp with competition\ −comp without compe!
tition[ Values are means ¦0 SE[
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
ing is consistent with previous studies showing that
seed germination of boreal species is generally tem!
perature!limited "Black + Bliss 0879^ Zasada et al[
0881#[ However\ the fairly low germination rates and
survivorship of germinants even in the greenhouse
treatment suggest that either higher temperatures
than those imposed by our manipulation or other
factors besides warm temperatures are also required
for successful recruitment of these species in tundra[
This seems particularly true of Alnus crispa and Pop!
ulus spp[\ whose germination rates even in the green!
houses were less than 4) of viable seed[
An additional factor that may limit seed ger!
mination of trees in tundra is the availability of suit!
able substrate[ Many studies have shown that ger!
mination rates of boreal species are often lower on
organic than on mineral substrates "Putnam + Zasada
0875^ Walker et al[ 0875^ Zasada et al[ 0881#[ The moss
substrate of tussock tundra may have been sub!
optimal for seed germination\ and _res\ which are
important in creating suitable seed beds in boreal
forest "Walker et al[ 0875#\ are rare in tundra "Wein
0865#[ Successful recruitment may be restricted to
relatively rare areas of exposed mineral soil\ such as
stabilized frost boils\ within upland tundra "Gartner
et al[ 0875#[
In contrast to seed germination\ the growth and
survivorship of tree seedlings in tundra were not
directly limited by cold air temperatures[ In fact\
survivorship was reduced by the warming treatment[
The only positive response to temperature manipu!
lation was a growth response in the _rst 1 years
after transplanting[ That the response disappeared
within 2 years suggests that tree seedlings could only
respond to warming while they still had access
to reserves accumulated prior to transplanting[ In
contrast to the other species\ Picea glauca showed
an increase in biomass with warming after 2 years\
suggesting that cold temperature directly limits its
growth at treeline[
For three of the species studied\ Betula papyrifera\
Picea glauca and Populus tremuloides\ seedling growth
and survivorship appeared limited by the availability
of below!ground resources[ Growth of these three
species was greater when below!ground competition
with the extant community was reduced\ suggesting
that soil resources were limiting their growth[
Although we did not distinguish experimentally
between competition for water or nutrients\ water is
unlikely to limit growth in wet tundra soils "Ober!
bauer + Dawson 0881#[ In contrast\ nutrients often
limit plant growth in tundra "Chapin + Shaver 0874^
Shaver et al[ 0875^ Chapin + Shaver 0885#\ so com!
petition for nutrients is likely[
Further evidence for limitation by nutrient avail!
ability comes from the patterns of biomass\ growth
and survivorship of these species among the di}erent
vegetation types[ Growth\ biomass and survivorship
were generally highest in the shrub site and lowest in
the heath site[ The shrub tundra site di}ered from
the other sites primarily in its higher N availability\
although its soils were also wetter than those of the
other two sites[ Other studies have shown that shrub
tundra has higher nutrient availability "Kielland 0889#
and is more productive "Shaver + Chapin 0880# than
tussock or heath tundra[ In addition\ the shrub tundra
site studied here occurred along a water track^ water
tracks have higher productivity than the surrounding
tundra\ and this higher productivity has been attri!
buted to greater nutrient mineralization and bulk ~ow
of nutrients within water tracks "Chapin et al[ 0877#[
348
S[E[ Hobbie +
F[S[ Chapin
Þ 0887 British
Ecological Society\
Journal of Ecology\
75\ 338Ð350
Fertilizer studies have demonstrated that productivity
of heath tundra is extremely nutrient!limited] heath
tundra responds the most and shrub tundra the least
to nutrient addition "Chapin et al[ 0881#[ Low nutrient
availability has also been shown to limit growth of
adult trees at treeline in Sweden "Sveinbjornsson et al[
0881#[
Two of the species studied\ Populus balsamifera
and Alnus crispa\ responded little\ if at all\ to the
manipulations and had generally poor growth and
survivorship[ This suggests that some other factor
besides air temperature or below!ground resource
availability was limiting their growth and survivor!
ship[ One possible limiting factor that was not
manipulated here is cold soil temperature[ Root
growth and nutrient and water uptake in boreal forest
trees are all inhibited at low temperatures "Tryon +
Chapin 0872^ Goldstein et al[ 0874^ Chapin et al[
0875#[ Moreover\ isolated tundra populations of Pop!
ulus balsamifera are generally restricted to warm
springs or steep\ south!facing slopes where soil tem!
peratures are relatively warm "Murray 0879#[
It is unclear whether our choice of seed prov!
enances "from single populations in Fairbanks# has
biased our results in any way[ Studies of isozyme
variation in several of the species studied reveal little
genetic di}erentiation among populations across
broad boreal and subboreal regions\ perhaps because
of high gene ~ow "promoted by wind pollination and
seed dispersal# combined with the relatively recent
arrival of these species to boreal regions "Alden +
Loopstra 0876^ Farmer et al[ 0877^ Lund et al[ 0881#[
On the other hand\ isozyme variation may be a poor
indicator of genetic variation in response to environ!
mental factors[ Some research has shown di}erences
in growth potential of Picea glauca that correlate with
provenance latitude "Li et al[ 0886#[ However\ we are
unaware of studies speci_cally examining genotype
by environment interactions for traits related to
migration in boreal species[
The current distribution of isolated tree popu!
lations in the Alaskan Arctic shows little relationship
to the species di}erences in establishment success that
we observed[ Alnus crispa and Populus tremuloides\
the two treeline species that have been reported
repeatedly in arctic Alaska "see the Introduction#\
were the two species least successful in establishing in
our experiments[ Thus these isolated populations are
probably relics\ maintained by clonal growth\ of
populations that established during mid!Holocene
warming[
Given adequate seed dispersal\ future warming will
likely increase the probability that seeds of the species
studied here will germinate in tundra[ However\ the
probability of those seedlings establishing will prob!
ably increase only if warming increases nutrient avail!
ability\ or possibly growing season length "not studied
here#[ This is particularly true for Betula papyrifera\
Picea glauca and Populus tremuloides[ Because of low
availability of suitable sites for germination\ recruit!
ment may be generally low\ except along riparian
zones or unless _re frequencies increase[
If establishment of seedlings proves to be an impor!
tant bottleneck to treeline expansion\ Picea glauca
will probably invade tundra more readily than the
other species studied here[ Picea glauca is more likely
than other species to establish from seed in intact
upland tundra vegetation since it had relatively high
germination rates and was the only species whose
seedlings survived during the study once seeds had
germinated[ Furthermore\ P[ glauca transplants had
relatively high survivorship and positive growth in
tundra and responded both to increased temperature
and to treatments that probably increased nutrient
availability\ a situation likely to occur with climate
warming[ Root growth and nutrient uptake are less
sensitive to temperature in P[ glauca than in the other
species we studied "Tryon + Chapin 0872^ Chapin
et al[ 0875#[ Our suggestion that P[ glauca will prob!
ably invade tundra with warming is consistent with
other studies showing establishment of Picea glauca
north of treeline in northern Alaska during recent
warm decades "Cooper 0875^ F[ Suarez\ D[ Binkley
and R[ Stottlemyer\ unpublished data#[ Because P[
glauca is one of only two evergreen species occurring
at North American treeline\ its expansion could sig!
ni_cantly decrease regional albedo with implications
for the global climate[
Acknowledgements
We thank Jennifer Dekker and Eric Stendell for help
processing samples\ Chris Lund and Anna Shevtsova
for help in the _eld\ and the Toolik Lake LTER pro!
gram for use of their dataloggers[ Funding was pro!
vided by an NSF predoctoral fellowship\ a NASA
Global Change Fellowship\ and an NSF Doctoral
Dissertation Improvement Grant "BSR 80!11680# to
SEH and an NSF Grant "BSR 76!94212# to FSC[
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Received 13 April 0886
revision accepted 06 November 0886