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Ecology, 93(7), 2012, pp. 1683–1694� 2012 by the Ecological Society of America
Above- and belowground responses of arctic tundra ecosystemsto altered soil nutrients and mammalian herbivory
LAURA GOUGH,1,5 JOHN C. MOORE,2,3 GAUIS R. SHAVER,4 RODNEY T. SIMPSON,3 AND DAVID R. JOHNSON1,6
1Department of Biology, University of Texas, Arlington, Texas 76019 USA2Department of Ecosystem Science and Sustainability, Colorado State University, Fort Collins, Colorado 80523 USA
3Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, Colorado 80523 USA4Ecosystems Center, Marine Biological Laboratory, Woods Hole, Massachusetts 02543 USA
Abstract. Theory and observation indicate that changes in the rate of primary productioncan alter the balance between the bottom-up influences of plants and resources and the top-down regulation of herbivores and predators on ecosystem structure and function. TheExploitation Ecosystem Hypothesis (EEH) posited that as aboveground net primaryproductivity (ANPP) increases, the additional biomass should support higher trophic levels.We developed an extension of EEH to include the impacts of increases in ANPP onbelowground consumers in a similar manner as aboveground, but indirectly through changesin the allocation of photosynthate to roots. We tested our predictions for plants abovegroundand for phytophagous nematodes and their predators belowground in two common arctictundra plant communities subjected to 11 years of increased soil nutrient availability and/orexclusion of mammalian herbivores. The less productive dry heath (DH) community met thepredictions of EEH aboveground, with the greatest ANPP and plant biomass in the fertilizedplots protected from herbivory. A palatable grass increased in fertilized plots while dwarfevergreen shrubs and lichens declined. Belowground, phytophagous nematodes alsoresponded as predicted, achieving greater biomass in the higher ANPP plots, whereaspredator biomass tended to be lower in those same plots (although not significantly). In thehigher productivity moist acidic tussock (MAT) community, aboveground responses werequite different. Herbivores stimulated ANPP and biomass in both ambient and enriched soilnutrient plots; maximum ANPP occurred in fertilized plots exposed to herbivory. Fertilizedplots became dominated by dwarf birch (a deciduous shrub) and cloudberry (a perennial forb);under ambient conditions these two species coexist with sedges, evergreen dwarf shrubs, andSphagnum mosses. Phytophagous nematodes did not respond significantly to changes inANPP, although predator biomass was greatest in control plots. The contrasting results ofthese two arctic tundra plant communities suggest that the predictions of EEH may hold forvery low ANPP communities, but that other factors, including competition and shifts invegetation composition toward less palatable species, may confound predicted responses tochanges in productivity in higher ANPP communities such as the MAT studied here.
Key words: Arctic LTER, Toolik Lake, Alaska, USA; arctic tundra ecosystem; biomass; caribou;EEH, exploitation ecosystem hypothesis; food web; herbivory; nematode; nutrients; predators; productivity;vole.
INTRODUCTION
Oksanen et al. (1981) developed the Exploitation
Ecosystem Hypothesis (EEH) to describe how food
chains develop along aboveground net primary produc-
tivity (ANPP) gradients based on relatively low-produc-
tivity subarctic ecosystems supporting vertebrate
herbivores and predators. As ANPP increases from a
minimal level, plant biomass also increases until a
threshold is reached where herbivore populations can be
sustained. At that level of ANPP, plant biomass
stabilizes while ANPP continues to increase; the
additional productivity is consumed by herbivores so
that consumer biomass increases but plant biomass does
not. Similar patterns are predicted for further increases
in ANPP that will add additional trophic levels to the
system.
These patterns predicted by EEH have been validated
in several instances in terrestrial ecosystems (reviewed in
Wardle 2002), although they have not been explicitly
tested along above- or belowground productivity
gradients very often, perhaps because ecologists felt
that EEH was too simplistic. For example, the EEH
system was described as a linear food chain or series of
coupled linear food chains, wherein each trophic level
was treated as a single population and selective
Manuscript received 9 September 2011; revised 20 December2011; accepted 1 February 2012. Corresponding Editor:H. A. L. Henry.
5 E-mail: [email protected] Present address: Department of Biological Sciences,
University of Texas, El Paso, Texas 79968 USA.
1683
herbivory was ignored. Additionally, trophic cascades
have often been considered to be weak in terrestrial
ecosystems (e.g., Strong 1992; but see Schmitz et al.
2004). Fraser and Grime (1999) argued that some tests
of EEH were overcriticized because of individual biases
against terrestrial trophic cascades, whereas their
terrestrial mesocosm results point to the existence of
strong trophic cascades that follow the predictions of
EEH. Certainly there have been many tests of the
interactive effects of adding nutrients (increasing pro-
ductivity) and herbivory (e.g., Gruner et al. 2008) in
terrestrial ecosystems including tundra (e.g., Grellmann
2002), but these studies usually have not been examined
in the context of EEH.
Recently, Aunapuu et al. (2008), conducting a series
of studies in a subarctic Scandinavian heath in which the
number of trophic levels or soil nutrients were experi-
mentally manipulated, found support for EEH. When
nutrients were added, plant biomass remained similar to
control levels, whereas rodent herbivore activity and
biomass significantly increased. Vegetation that had
been transplanted to islands with both herbivores and
secondary consumers maintained greater biomass than
vegetation transplanted to islands with only herbivores.
These results confirm that subarctic tundra can behave
according to the assumptions of EEH.
Here we test the predictions of EEH in two common
low-productivity Alaskan tundra communities, dry
heath (DH) and moist acidic tussock (MAT), subject
to manipulations of soil nutrients and mammalian
herbivory for 11 years. MAT and DH tundra differ in
ANPP, biomass, plant species composition, response to
added nutrients, and herbivore activity (e.g., Shaver et
al. 2001, Gough et al. 2002, 2007). We developed an
extension of EEH to simultaneously study aboveground
and belowground responses to changes in plant produc-
tivity and herbivory using the framework presented by
Schmitz (2008). Such studies that simultaneously exam-
ine soil fauna, vegetation, and mammalian herbivores
aboveground are quite rare (reviewed in Bardgett and
Wardle 2010), yet are crucial to better understand how
arctic ecosystems function (Post et al. 2009, Wookey et
al. 2009).
We predicted that both aboveground and below-
ground responses to manipulations would result from a
combination of direct and indirect effects of production
and consumption, with the magnitude of the responses
being dependent on the allocation of production within
the plants to shoots and roots. Because productivity in
our study system is low, we expect that two trophic
levels dominate aboveground interactions (predators are
relatively rare). We also assume that because our
experimental plots are relatively small, altering produc-
tivity in situ will not affect population structure of
herbivores at the landscape scale, but will affect activity
of herbivores in the plots themselves. Our aboveground
predictions (denoted ‘‘A’’) follow directly from EEH
(Fig. 1A):
H1A: When nitrogen and phosphorus (þNP) are
added to the soil, ANPP increases, but biomass does not
because herbivores consume the additional productivity.
H2A: When mammalian herbivores are removed
(�H), aboveground biomass increases because some of
the productivity will now be able to accumulate as
standing crop, but ANPP will not change.
H3A: When nutrients are added and herbivores are
removed (þNP�H), ANPP and biomass exceed the
combined levels of the other two treatments alone (a
superadditive interaction, sensu Gruner et al. 2008). This
assumes that herbivory and nutrients interact such that
mammals are attracted to fertilized plots; protecting
fertilized plants from herbivory allows the plant
community to increase both ANPP and biomass.
Our belowground predictions (denoted ‘‘B’’; Fig. 1B)
incorporate both belowground herbivores and their
FIG. 1. Hypothesized responses of (A) aboveground plantbiomass and (B) belowground consumer biomass (herbivoresand their predators) to changes in productivity (ANPP) causedby experimental treatments in the Arctic LTER, Toolik Lake,Alaska, USA. HA and HB, respectively, are hypotheses foraboveground and belowground responses. Treatment abbrevi-ations are: CT, control; þNP, added soil nitrogen andphosphorus; �H, mammalian herbivores excluded. The H2B(arrow from CT to�H, where B indicates belowground) is notshown as no change is predicted from control levels. SeeMethods: Study site and experimental treatments for details.
LAURA GOUGH ET AL.1684 Ecology, Vol. 93, No. 7
predators and are based on how our experimental
manipulations are predicted to alter ANPP in accor-dance with EEH for a system with up to four trophic
levels, and on expected changes in the allocation ofproductivity between shoots and roots. We assume from
previous studies in these communities (e.g., Gough et al.2002, van Wijk et al. 2003, Hobbie et al. 2005) thatfertilization will increase ANPP and root production,
but that removal of mammalian herbivores alone (�H)will not have an effect on root production. The
hypotheses for belowground response are:H1B: In fertilized plots, belowground herbivore
biomass (phytophagous nematodes) and predator bio-mass increase.
H2B: When mammals are removed, no change in thebiomass of belowground herbivores or predators occurs.
H3B: When nutrients are added and herbivoresremoved, belowground herbivore biomass and predator
biomass increase more than under H1B.
METHODS
Study site and experimental treatments
This research was conducted at the Arctic Long-
Term Ecological Research (LTER) site at Toolik Lake,Alaska (68.28 N, 149.68 W, 760 m a.s.l.). In 1996 a
factorial design was implemented in both MAT andDH to determine how the presence or absence ofmammals affected vegetation and soil responses to
added nutrients (10 g�m�2�yr�1 as NH4NO3 and 5g�m�2�yr�1 as P2O5 applied annually in granular form in
early June following snowmelt). Treatment plots of 53
20 m were replicated within four blocks at MAT and
three blocks at DH. For this experiment, one plotwithin each block was randomly assigned N and P
addition (þNP) and another had no nutrients added asa control (CT).
Half of each 5 3 20 m plot in each block was leftunfenced so that mammals could easily access the
vegetation, while the remaining 5 3 10 m was enclosedin a large-mesh fence designed to exclude caribou (15.2
315.2 cm openings, ;1.2 m in height). Half of the area(5 3 5 m) within the 5 3 10 m fence was additionally
enclosed by a small-mesh fence (1.33 1.3 cm openings,;0.8 m in height). The small-mesh fence was buried in
the soil at least 10 cm at construction to preventanimals from burrowing into the plots and wasdesigned to additionally exclude small mammals
including ground squirrels, voles, and lemmings. Forthis study, we did not consider the effects of small and
large mammals separately; thus all data were collectedfrom unfenced areas and areas with both small- and
large-mammal exclusion (designated as�H for lackingherbivory). Each block thus contained plots with four
possible combinations of fence and fertilization: CT,þNP, �H, and þNP�H. Although there are herbivo-
rous insects in these communities, their effect on leafbiomass appeared to be minimal (L. Gough and D. R.
Johnson, personal observations). These plots may
retain snow on the immediate northern edge of fences
for 2–3 days early in the season relative to unfenced
areas (L. Gough and D. R. Johnson, personal
observations). To avoid this snow accumulation, all
sampling was conducted at least 0.5 m from the edge of
the fence.
Aboveground communities
Mammalian herbivores.—Five species of microtine
rodents have been recorded on the North Slope of
Alaska (Batzli et al. 1980): three species of voles
(Microtus oeconomus, M. miurus, and Clethrionomys
rutilis) and two lemming species (Dicrostonyx rubricatus
and Lemmus trimucronatus). The tundra vole (M.
oeconomus) and singing vole (M. miurus) are common
in communities near the Arctic LTER (Batzli and
Lesieutre 1995). Specifically, tundra voles are commonly
seen at MAT (L. Gough and D. R. Johnson, personal
observations), as is evidence of their presence (hay piles,
trails, and fecal deposits) during cyclical outbreak years.
Singing voles and collared lemmings (D. rubricatus) have
been found in rocky areas very near DH (Batzli and
Henttonen 1990; L. Gough and D. R. Johnson, personal
observations). Batzli and Henttonen (1990) suggested
that density of these rodents is limited by food
availability but may also be restricted top-down by
predators similar to lemmings in coastal tundra (Batzli
et al. 1980).
Although they are transient, caribou are commonly
sighted near the Arctic LTER (L. Gough and D. R.
Johnson, personal observations). Toolik Lake lies within
the range of the Central Arctic Herd (Lenhart 2002), but
the herd’s primary calving grounds are far to the north.
Thus caribou are not thought to be common foragers of
plants in MAT. In DH however, caribou feces are
frequently seen following snowmelt. Thus, DH may be
an important winter habitat for caribou because snow
cover is often less there than in surrounding areas
(Cheng et al. 1998; see also Gough et al. 2008).
Mammalian activity was estimated in all plots in an
area of 8 m2 when vegetation was sampled nondestruc-
tively for relative abundance in late July 2006. Observers
noted the percentage of ground surface on which signs
of activity were seen, including vole trails, hay piles, and
fecal piles, evidence of litter that had been chewed by
mammals, and caribou fecal pellets.
Plant biomass
To estimate ANPP and leaf and shoot biomass, we
harvested four 20 3 20 cm quadrats located randomly
along a 5-m transect in each treatment plot in each block
in DH and in three blocks in MAT in late July 2006.
Each quadrat was cut 10–20 cm deep to sample all
rhizomes, and we considered aboveground plant bio-
mass ‘‘within’’ the quadrat if plants were associated with
a meristem inside the quadrat. We sorted all vascular
plants to species in a field laboratory and lumped mosses
and lichens. Vascular species were then sorted into tissue
July 2012 1685ABOVE- AND BELOWGROUND TEST OF EEH
type, including new leaves, new stems, old leaves, old
stems, and rhizomes (as appropriate for particular
growth forms). All samples were dried at 608C to a
constant mass and were weighed to the nearest
milligram. ANPP was determined separately by growth
form. Graminoid and forb ANPP was calculated as the
sum of all leaves and aboveground stems that had been
produced that year. Deciduous and evergreen shrub
ANPP was calculated by summing new leaf mass, new
stem mass, and an estimate of stem secondary growth
calculated as a percentage of old stem mass following
relationships for control andþNP treatments established
in Bret-Harte et al. (2002). Moss and lichen productivity
was not determined.
We took a separate set of samples to estimate root
biomass. At DH, a 5 cm diameter soil corer was used to
extract a soil core adjacent to each location where a
quadrat was taken as described previously; maximum
core depth was 10 cm, as no roots were seen below that
depth. At MAT, a 53 10 cm piece of tundra was cut out
adjacent to each aboveground sampling quadrat to the
depth of permafrost. In the laboratory each sample was
separated into organic and mineral horizons and then
was sliced into 5-cm increments. Roots were extracted
from each section, carefully washed, and separated to
genus or species when possible before being dried for at
least three days at 608C and weighed. Because sampling
roots from all plots was not logistically possible, we only
sampled one block of �H and þNP�H treatments in
each community.
All plant tissues were shipped back to the University
of Texas at Arlington where they were dried again,
lumped by block, and then analyzed for C and N
content using a Perkin Elmer Series 2200 CHN Analyzer
(Perkin Elmer, Waltham, Massachusetts, USA).
Belowground communities
The organic horizons and upper 5 cm of the mineral
horizon were sampled in MAT and DH in late July
2006. In control plots, the organic horizon at MAT
often reaches 15 cm in depth, whereas at DH it averages
2–3 cm depth (J. C. Moore, unpublished data). In MAT
we stratified our sampling to include tussock areas,
taken immediately adjacent to a tussock of the sedge
Eriophorum vaginatum, and inter-tussock areas, mossy
depressions between the tussocks, because of the distinct
microtopographic differences between the two. Because
E. vaginatum covers approximately one-third of the
ground surface in MAT control plots (Hobbie et al.
2005), we weighted the paired tussock samples at 1/3
and the inter-tussock samples at 2/3 to determine
abundance at the square-meter scale. In DH samples
were taken at random because the plots were carpeted
with lichens, with no discernible difference in micro-
topography.
In both MAT and DH, two 10310 cm columns of the
organic horizon through the upper 5 cm of the mineral
soil layer were taken in each sampling location. The
sample pairs from each plot were sliced in half, with one
half kept intact and used to extract microarthropods and
the other half passed through an 8-mm sieve for
additional sampling (not presented here). All biomass
estimates are reported on a ‘‘per gram of dry soil’’ basis
before being converted to mg C/m2. Dry mass values for
soils used to extract microarthropods were estimated by
the difference between the pre- and post-extraction mass
of the soils from which the microarthropods were
extracted, as this process involved heating the soils from
above until they were dry.
Invertebrate biomass.—Biomass (mg C/m2) was esti-
mated from the counts and morphometric conversions
for each functional group assuming 50% C content and
an estimate of the bulk density of the soil (Hunt et al.
1987, Doles 2000). The functional groups reported here
include phytophagous nematodes and nematode preda-
tors extracted from soils using techniques that will be
described. To estimate biomass of the predators of the
phytophagous nematodes, the biomass of predatory
nematodes, predatory tardigrades, and predatory mites
(nematophagous Mesostigmata, Prostigmata, and As-
tigmata) were summed within each soil sample.
Nematodes were isolated from 20 g of sieved soil
using Baermann funnels (Baermann 1917). After three
days on the apparatus, nematodes that were collected
were preserved in formalin and sorted into functional
groups. The phytophagous nematodes (plant-feeding
and root-associate) and predatory nematodes are
reported here. The phytophagous nematodes, members
of the family Tylenchidae, were subdivided into free-
living plant feeding nematodes and root-associate
nematodes using the criteria of Yeates et al. (1993)
based on the morphology of their mouthparts and
feeding habits. The mouthparts of free-living plant
feeding nematodes possess robust stylets for feeding on
plant roots, root hairs, and rhizomes, whereas root-
associate nematodes possess fine stylets and feed on root
epidermal cells, root hairs, lichens, fungi, and algae.
Tardigrades were isolated from 5 g of sieved soil
placed in a 100 mm diameter petri dish and immersed in
deionized water. The submerged soils sat for 5 minutes
at room temperature after which coarse organic debris
was rinsed to release the tardigrades into the dish; the
organic debris was then removed. The dishes were
placed under a dissecting microscope and live tardi-
grades were counted.
Microarthropods were heat-extracted into 90% etha-
nol, 1% glycerine from soils using Tullgren funnels
(Moore et al. 2000). The intact sample pairs from each
plot were wrapped together in cotton cheesecloth,
weighed, placed over a funnel, and heated with a 9-W
incandescent lightbulb for 5 days until dry. The dry soil
and cheesecloth were reweighed to determine the dry
mass of soil per sample and the soil moisture content.
The collected arthropods were sorted into taxonomic
and functional groups (sensu Moore et al. 1988).
LAURA GOUGH ET AL.1686 Ecology, Vol. 93, No. 7
Statistical analyses
Analysis of variance was used to assess plant and soil
organism responses to the fertilization and grazing
treatment. All statistical tests were run using SAS
(Version 9.2, SAS Institute, Cary, North Carolina,
USA). For all variables, results were analyzed separately
for DH and MAT communities. Within each commu-
nity, a two-way randomized-block design ANOVA was
conducted with fertilization and herbivory as the main
effects, quadrat nested in block, and block included. For
the microarthropods and plant tissue analysis, the
design did not include the nested term because the
samples were bulked for extraction or analysis. Data
were natural log-transformed as needed to meet
parametric model assumptions. Tukey’s post hoc
comparisons were used to determine significant pairwise
differences. All data are reported as mean 6 SE.
RESULTS
Mammal activity
Adding nutrients resulted in an increase in mamma-
lian activity in both communities. At DH, caribou feces
were evident in open plots (3% 6 1% in CT and 1% 6
0% in þNP). Caribou litter (pieces of the grass
Hierochloe alpina that had been removed from the plant
via trampling) was present in 11% 6 6% of the area of
þNP plots. Evidence of vole hay piles was also found in
the þNP plots.
At MAT, recent vole activity was seen in the open
plots, with 2% 6 1% of the area of CT plots and 4% 6
2% of þNP plots affected as evidenced by vole fecal
pellets, runways, and litter. Eriophorum tussocks showed
direct signs of vole damage including hay piles and
tunnels, with more extreme effects, e.g., killing of
sections of or entire tussocks by winter consumption
of rhizomes and leaf bases, observed in the þNP plots.
Plant productivity and tissue nutrient content
In DH, the pattern of ANPP across treatments
followed predictions (see Plate 1), but there was no
significant effect of any treatment on total vascular
ANPP (Fig. 2A). Fertilization resulted in significantly
lower evergreen ANPP (F1,31 ¼ 46.91, P , 0.0001) and
greater graminoid ANPP, primarily Hierochloe (F1,33 ¼37.87, P , 0.0001; Fig. 2A). Evergreen shrub ANPP was
also marginally higher in plots protected from herbi-
vores (F1,31¼ 3.52, P¼ 0.07), suggesting a benefit to this
group from the exclosures. Fertilization decreased the
C:N ratio of total vascular ANPP (F1,8 ¼ 253.11, P ,
0.0001), while excluding herbivores had the opposite
effect and increased C:N (F1,8¼ 9.32, P¼ 0.02; Table 1).
In contrast, vascular ANPP at MAT was significantly
greater in plots subject to fertilization (F1,31¼56.56, P ,
0.0001) and those exposed to herbivores (F1,31¼ 4.95, P
¼ 0.03), with no interaction between these main effects
(Fig. 2B). A herbivore effect was also not detected for
ANPP of any of the growth forms when analyzed
separately (Fig. 2B). As at DH, evergreen shrubs at
MAT had lower ANPP in fertilized plots (F1,32¼ 22.48,
P , 0.0001), whereas deciduous shrubs and forbs had
greater ANPP in those plots (F1,32 ¼ 17.09, P ¼ 0.0002
and F1,33¼13.78, P¼0.0008, respectively). Although the
graminoid ANPP means were different (Fig. 2B),
substantial within-treatment variation precluded the
detection of any significant effects. The C:N of total
vascular ANPP was also significantly reduced by
fertilization (F1,8 ¼ 28.28, P ¼ 0.0007), but showed no
effect of herbivore exclosure (Table 1).
Plant biomass
At DH, total biomass was significantly greater inside
herbivore exclosures than outside (F1,29¼ 4.83, P¼ 0.04;
Fig. 3A). This pattern was driven by positive responses
to herbivore exclosure by mosses and deciduous shrubs
(marginally significant, P , 0.10). Woody stem biomass
(summed across all woody species; data not shown) was
also marginally greater inside exclosures (F1,31¼ 3.66; P
FIG. 2. Aboveground net primary productivity (ANPP;mean 6 SE) after 11 years of experimental manipulation in (A)dry heath tundra and (B) moist acidic tussock tundra.Treatment abbreviations are as in Fig. 1. See Results forstatistical results by growth form.
July 2012 1687ABOVE- AND BELOWGROUND TEST OF EEH
¼ 0.06), probably reflecting subtle responses by shrubs
to long-term removal of herbivore pressure.
Fertilization induced significantly less total live
biomass at DH (F1,29 ¼ 6.95, P ¼ 0.01), probably due
to its significant negative effects on evergreen and lichen
biomass (F1,31¼ 29.81, P , 0.0001 and F1,33¼ 70.33, P
, 0.0001, respectively; Fig. 3A). Graminoid biomass
was significantly greater in fertilized plots (F1,33¼ 37.61,
P , 0.0001), but this was not enough to offset the losses
of other groups. Woody stem biomass was greater in
control than fertilized plots (F1,31 ¼ 5.00, P ¼ 0.03),
suggesting that fertilization caused a loss of wood
biomass at DH.
Root biomass at DH was greater in fertilized plots
(F1,17¼7.43, P¼0.01; Fig. 4A) and extended deeper into
mineral soil (data not shown). This partly resulted from
greater biomass of grass (Hierochloe) roots inþNP plots
(Fig. 4A). There were no significant effects of herbivory
on root biomass. To a lesser extent than for ANPP,
fertilization reduced overall root C:N (F1,4¼ 11.15, P¼0.03), but mammal exclosures had no effect (Table 1).
At MAT there were also no significant interactions
between herbivory and nutrient addition for any of the
biomass variables examined. In contrast to DH,
aboveground biomass (both including mosses and
lichens and when restricted to vascular species) was
significantly lower inside herbivore exclosures (F1,32 ¼4.50, P ¼ 0.04 and F1,32 ¼ 5.27, P ¼ 0.03, respectively;
Fig. 3B). Fertilization as a main effect caused more
dramatic responses. Aboveground vascular biomass and
vascular total biomass were greater in fertilized plots
relative to controls, driven by greater deciduous shrub
and forb (Rubus chamaemorus) biomass (all P , 0.05).
In particular, aboveground biomass of the dwarf
deciduous shrub Betula nana was significantly greater
in fertilized plots (F1,33 ¼ 14.82, P ¼ 0.0005). Other
groups were negatively affected; evergreen shrubs,
mosses, and lichens had less biomass in the fertilized
plots (all P , 0.05). In contrast with DH, woody stem
biomass was greater in fertilized plots (F1,31¼ 30.02, P¼0.0001).
The response of root biomass to fertilization and
herbivore exclusion was variable in MAT (Fig. 4B).
Total root biomass was not significantly affected by any
TABLE 1. Carbon to nitrogen (C:N) ratios for new shoot tissues (new leaves and new stems) and root tissues for the entire plantcommunity sampled in each quadrat or soil core after 11 years of experimental treatment in the Arctic LTER, Toolik Lake,Alaska, USA.
Tissue Site
C:N ratio, by treatment (mean 6 SE)
CT þNP �H þNP�H
New shoot DH 31a 6 1 12b 6 1 36a 6 1 14b 6 2MAT 24a 6 2 17b 6 1 24a 6 2 17b 6 1
Root DH 36 6 3 24 6 3 36 20MAT 34 6 5 27 6 4 38 25
Notes: Sites and sample sizes are dry heath (DH; n¼ 3 blocks) and moist acidic tussock (MAT; n¼ 4 blocks), except where noerrors are presented (n¼1 block); seeMethods for details. Treatment abbreviations are : CT, control;þNP, added soil nitrogen andphosphorus; �H, mammalian herbivores excluded. Within each row, different superscript letters indicate that the means aresignificantly different at P , 0.05.
FIG. 3. Above- and belowground plant biomass (mean 6SE for vascular plants aboveground, total abovegroundbiomass, and vascular plants belowground) after 11 years ofexperimental manipulation in (A) dry heath tundra and (B)moist acidic tussock tundra. The x-axis represents the groundsurface; on the y-axis, values above and below the x-axis,respectively, indicate aboveground and belowground rhizomebiomass; root biomass is presented in Fig. 4. Treatmentabbreviations are as in Fig. 1. See Results for statistical resultsby growth form.
LAURA GOUGH ET AL.1688 Ecology, Vol. 93, No. 7
treatment, although the sedge Eriophorum had margin-
ally significantly greater biomass in fertilized plots (F1,17
¼ 3.86, P ¼ 0.06). Total root C:N appeared lower in
fertilized plots, although not significantly (Table 1).
Soil herbivores and predators
In DH, soil herbivores responded as predicted to
changes in ANPP. Phytophagous nematodes (plant-
feeding and root-associate forms) had greater biomass in
all treatments relative to control values (main effect of
grazing and fertilization were marginally significant; P
, 0.10); the greatest herbivore biomass occurred in the
þNP�H treatment, where ANPP was also greatest
(Table 2). Within the phytophagous nematode grouping,
the root-associate nematode biomass was greater in
fertilized plots (F1,13 ¼ 4.03, P ¼ 0.06). The addition of
soil nutrients appeared to suppress predator biomass
(predatory nematodes, predatory mites, and tardi-
grades), although not significantly (Table 2). However
within the predator functional group, the tardigrades
exhibited a grazing effect (F1,14 ¼ 4.74, P ¼ 0.05) with
lower biomass in plots from which grazers were excluded
(Table 2).
At MAT, phytophagous nematode biomass was
similar to that in control plots at DH but showed no
response to fertilization or grazing and subsequent
changes in ANPP (Table 2). A significant interaction
between fertilization and grazing affected belowground
predator abundance (F1,12 ¼ 7.52, P ¼ 0.02), as did the
main effects of fertilization (F1,12¼ 11.16, P¼ 0.02) and
grazing (F1,12 ¼ 7.65, P ¼ 0.02), with lower biomass in
the experimental manipulations relative to control plots
(Table 2). Within the predators, fertilization reduced the
biomass of tardigrades (F1,12 ¼ 4.34, P ¼ 0.06). The
biomass of nematophagous mites was lower in the
grazing exclosures (F1,9 ¼ 3.48, P ¼ 0.10).
DISCUSSION
In our study, as in similar simultaneous manipulations
of herbivore pressure and nutrient availability in other
terrestrial ecosystems (see meta-analysis by Gruner et al.
2008), fertilization and herbivore exclosure generally did
not interact statistically to affect ANPP or biomass.
These findings run counter to the EEH predictions that
assume that with increased soil nutrients and ANPP,
effects of herbivory should be more pronounced. That
said, we did see trends suggesting such interactions, but
variability in response within treatments was frequently
too large to detect significant effects.
Dry heath responded as predicted by EEH
When presented graphically, aboveground biomass in
the DH plots appeared to respond as predicted by EEH
(Fig. 5A), demonstrating that productivity increases
caused by greater soil nutrient availability were only
manifested as increases in biomass when mammals were
excluded from the plots (supporting H1A [þNP] and
H3A [þNP�H]). However, vascular biomass did not
significantly increase as a result of herbivore exclosure
alone; thus H2A (�H) was not supported. These results
suggest that herbivores are not very important in
ambient nutrient plots, but are attracted to fertilized
plots in this community (also see Grellmann 2002). Not
only does the abundance of the highly palatable grass,
Hierochloe, increase, but also overall C:N of ANPP
declines and less wood is produced in fertilized plots.
These changes together suggest that with increased soil
nutrients at DH, both quantity and quality of forage
improve for mammals.
Herbivores have been shown to stimulate plant
productivity in other arctic systems by promoting
growth of graminoids (Olofsson et al. 2004, van der
Wal and Brooker 2004, van der Wal 2006) and may
convert heathland to grassland (Olofsson et al. 2001,
2004, Stark et al. 2002). Those European communities
have a significant moss component, so that one
mechanism of stimulation is via trampling by herbi-
vores, which negatively affects mosses, resulting in
increased soil temperatures that benefit graminoids
(Gornall et al. 2009). In the DH tundra studied here,
mosses do not occur in ambient nutrient plots, so other
aspects of animal activity, such as local concentration of
nutrients via feces or urine (van der Wal et al. 2004),
FIG. 4. Root biomass (mean 6 SE) after 11 years ofexperimental manipulation; values below the x-axis simplyindicate belowground measurements. In �H and þNP�Htreatments, roots were only sampled from one block so thereare no error bars. Note the difference in y-axis scales betweensites. See Results for statistical results by growth form.
July 2012 1689ABOVE- AND BELOWGROUND TEST OF EEH
must be involved in the graminoid stimulation that we
detected.
The belowground herbivores in DH also responded as
predicted by EEH but with high variability (Fig. 5B).
This high variability was not entirely unexpected, given
the complex nature of the belowground interactions
(i.e., potential number of trophic levels and feeding
pathways). For example, if we trace the pathways from
roots to phytophagous nematodes to predators using the
functional groups that we have designated here, the
system has as few as three trophic levels. If we
disaggregate the predators into the separate functional
groups (predatory nematodes, tardigrades, and preda-
tory mites; see Table 2) and retrace the paths, there are
between three and six trophic levels due to intraguild
predation, yielding an average and median number of
levels of 4.5. If we focus on the dominant predator
groups (predatory mites and tardigrades) based on our
biomass estimates, and retrace the paths, the mean and
median number of trophic levels is 4 (also see Moore
and de Ruiter 2012, in press).
Under the assumption of four trophic levels, the
caveats previously discussed notwithstanding, phytoph-
agous nematodes appeared to follow trends in ANPP
more closely than patterns of root biomass. Specifically,
the root-associate nematodes appeared to increase in
biomass as a result of improved forage quality
(decreased C:N) and quantity in fertilized plots,
consistent with De Deyn et al. (2004). Predators,
however, had similar or lower biomass in all treatments
compared with control plots (Fig. 5C), with the lowest
biomass in þNP�H where the greatest phytophagous
nematode biomass was recorded. One possible explana-
tion for this result is that the conversion to a grassland
in the DH creates an inhospitable environment for these
predators or shifts feeding patterns by other inverte-
brates, thus depriving this group of a key source of prey.
Another possibility is that the predators faced increased
competition and intraguild predation under these
experimentally induced conditions. Because the bio-
masses of the dominant group (tardigrades and preda-
tory arthropods) changed as a proportion of total
predator biomass (Table 2), the changes in phytopha-
gous nematode densities and predator densities are
indicative of a shift in the balance between bottom-up
and top-down controls on trophic structure consistent
with predictions of EEH.
At MAT mammalian herbivores stimulated ANPP
and biomass
In contrast with DH, MAT productivity and biomass
in both ambient and fertilized plots were stimulated by
the presence of herbivores (Fig. 5A), supporting studies
in other systems of overcompensation (e.g., Hilbert et al.
1981, Hik and Jefferies 1990, Leriche et al. 2001) and
counter to EEH and related hypotheses (Gruner et al.
2008). The MAT responses were driven by different
species, but primarily dwarf birch, B. nana. Betula is
known to contain numerous phenolic compounds in its
leaves, ostensibly making it less desirable to herbivores
(Graglia et al. 2001), but has also responded positively
to reindeer/caribou exclosure in other parts of the Arctic
(e.g., Pajunen et al. 2008, Post and Pedersen 2008,
Olofsson et al. 2009). To our knowledge, our results are
some of the first to suggest a potential stimulation of
Betula by the presence of mammalian herbivores, either
indirectly or directly.
Belowground, biomass of phytophagous nematodes
did not respond to experimental treatments at MAT,
just as root biomass did not (in contrast with Sullivan et
al. 2007), despite the large shifts in aboveground
productivity and root C:N caused by the experimental
treatments (Fig. 5B). Total predators, however, exhib-
ited lower biomass in all the treatment plots at MAT,
similar to the response at DH (Fig. 5C). This might be
related to the increase in Betula and Rubus and the
demise of Eriophorum and Sphagnum mosses. Betula
nana possesses more structurally recalcitrant roots than
Eriophorum and lower quality plant litter (higher C:N)
than co-occurring species (Hobbie 1996), produces
secondary phenolic plant compounds (Graglia et al.
2001), and is highly ectomycorrhizal (Clemmensen et al.
2006). The observed shift in the plant community
essentially transformed the belowground resource base
TABLE 2. Belowground consumer biomass (mean 6 SE) at the two site types.
Belowground consumers
Consumer biomass in DH (mg C/m2)
CT þNP �H þNP�H
Plant-feeding nematodes 0.052 6 0.032 0.151 6 0.126 0.230 6 0.117 0.378 6 0.240Root-associate nematodes 0.035 6 0.017 0.054 6 0.054
Total phytophagous nematodes 0.052 6 0.032 0.185 6 0.109 0.230 6 0.117 0.432 6 0.294
Predatory mites 17.5 6 13.9 10.6 6 9.7 18.0 6 10.0 3.9 6 0.8Nematophagous mites 0.3 6 0.2 0.2 6 0.1 0.1 6 0.1 0.1 6 0.1Predatory nematodesTardigrades 8.0 6 6.1 1.8 6 1.8 0.0 6 0.0 0.7 6 0.7
Total predators 25.8 6 12.5 12.6 6 9.0 18.1 6 10.0 4.7 6 0.3
Notes: Sample size is n¼3 blocks for DH; n¼4 blocks for MAT (see Results: Soil herbivores and predators). Abbreviations are asin Table 1. Within each row, different superscript letters indicate significantly different means at P , 0.05; see Results forstatistically significant main effects. Blank cells indicate that a particular consumer was not found for the specified treatment.
LAURA GOUGH ET AL.1690 Ecology, Vol. 93, No. 7
in ways that may not provide suitable forage for soil
organisms adapted to living within and feeding on
sedges or mosses.
Interacting effects of changes in ANPP, species
composition, tissue quality, and herbivory
One of the most important findings of the work
reported here is how distinctly both nutrients and
mammalian herbivores affected these two communities,
with DH following the predictions of EEH and MAT
responding quite differently. Although we only focused
on two sites for this research, they are representative of
these community types in northern Alaska and thus we
are confident that the differences between the two would
occur at a larger scale. Several reasons seem to be at
play. First, the disparity between aboveground results in
the two communities may stem from the presence of
different herbivores and different plant growth forms in
the two communities. At DH, mammalian herbivores do
not seem to play an important role unless soil nutrients
are added, at which point the newly abundant grasses
provide important resources to caribou and small
mammals. In contrast, at MAT, caribou are transient,
whereas small mammals are important herbivores in
years of high abundance regardless of soil nutrients. Our
results suggest that mammals at MAT may be stimulat-
ing deciduous shrub growth by reducing competition for
nutrients for Betula, because voles selectively target
Eriophorum for food and shelter. A similar competitive
release result has been seen in a removal experiment
conducted in the same community (Bret-Harte et al.
2008).
Second, EEH addresses how an ecosystem responds
along a gradient of productivity. At extremely low
productivity, trophic levels are added with increased
productivity in a stair-stepped fashion. With further
increases in productivity, in the absence of the addition
of a new upper trophic level, biomass is eventually
transferred to upper levels. These changes in structure
are not gradual or linear along the gradient. Rather,
they exhibit a stair-stepped response with the addition of
new trophic levels and sigmoid response in terms of the
accumulation of total biomass, with the more pro-
nounced changes occurring at the low end of the
productivity gradient (Moore et al. 2003). At ;50
g�m�2�yr�1, the DH community is at the low end of the
global ANPP range where significant changes in
ecosystem structure with increased ANPP would be
expected (Moore et al. 1993). At ;150 g�m�2�yr�1, theMAT community is positioned on the response curve
where the observed response to increased ANPP at the
MAT sites would be proportionally less than that
observed in the DH sites; our results confirm these
predictions.
Third, interpreting the results strictly in terms of EEH
is problematic as the hypothesis assumes, if not
implicitly, that the species traits in the community
FIG. 5. Responses of aboveground productivity and (A)aboveground plant biomass, (B) root-feeding nematode bio-mass, and (C) belowground predator biomass to 11 years oftreatment. Solid symbols and solid lines are for DH (dry heath);open symbols and dashed lines are for MAT (moist acidictussock); error bars indicate 6SE.
TABLE 2. Extended.
Consumer biomass in MAT (mg C/m2)
CT þNP �H þNP�H
0.034 6 0.015 0.016 6 0.005 0.046 6 0.036 0.023 6 0.0140.007 6 0.007 0.009 6 0.009
0.034 6 0.015 0.023 6 0.009 0.056 6 0.045 0.023 6 0.014
57.4 6 21.5 3.7 6 1.8 8.8 6 2.0 4.3 6 2.91.4 6 0.9 0.2 6 0.1 0.1 6 0.1 0.2 6 0.20.6 6 0.4 0.2 6 0.2 0.2 6 0.27.6 6 2.6 1.3 6 1.3 4.6 6 2.0 2.9 6 1.5
69.8a 6 21.1 5.7b 6 0.8 13.7b 6 2.3 6.2b 6 2.1
July 2012 1691ABOVE- AND BELOWGROUND TEST OF EEH
remain constant. Both the DH and MAT systems
exhibited shifts in the aboveground communities with
significant declines in species richness caused by
fertilization (Johnson 2008), but did so in ways that
elicited different ecosystem responses. As previously
described, nutrient additions and the removal of
herbivores in DH precipitated a shift in the plant
community from one dominated by lichens and ever-
greens to one with abundant grass, whereas at MAT the
community changed from one of mixed growth forms
(including Sphagnum mosses) to dominance by a dwarf
deciduous shrub and a perennial forb. Another impor-
tant difference between the two sites was that in DH the
increased ANPP accompanied a loss of woody tissues
and a large decrease in C:N, whereas at MAT more
wood was produced, resulting in a proportionally
smaller decrease in C:N. The changes in ANPP at DH
thus follow expected changes along a natural produc-
tivity gradient of an increase in plant productivity and
palatability, whereas at MAT there was less of an
improvement in tissue quality. Evidence suggests that
plant tissue quality can partly control trophic structure
of an ecosystem (Cebrian et al. 2009); thus the different
degree of changes in this factor is likely to partly explain
our overall results.
Finally, we did not see a clear correlation between
changes in belowground herbivores and their predators
and aboveground responses to our treatments. There are
multiple reasons why soil communities may not respond
to increases in ANPP as predicted by EEH (reviewed in
Allison 2006). The suggestion from our study that at
DH phytophagous nematodes increased with fertiliza-
tion while they did not respond in MAT probably also
resulted from changes in the plant community and the
associated rhizosphere. Future studies will continue to
shed light on patterns of belowground consumers in
response to changes in ANPP.
In conclusion, our results demonstrate that the tenets
of EEH can hold in low-productivity terrestrial ecosys-
tems such as the DH studied here, but that in higher-
productivity communities, responses to changes in
ANPP are more complex. In many ways, elements of
the ideas of trophic control and regulation presented by
Hairston et al. (1960), the theory of biogeography (sensu
MacArthur and Wilson 1967), and the strategy of
ecosystem development (Odum 1969) seem appropriate
here. The responses within DH, particularly below-
PLATE 1. Installing an arthropod pitfall trap in early June 2006 before leaf green-up in a fertilized dry heath treatment plot. Theplot is dominated by grasses as a result of long-term nutrient addition; the fence in the background is one of the mammalianherbivore exclosures. Photo credit: R. T. Simpson.
LAURA GOUGH ET AL.1692 Ecology, Vol. 93, No. 7
ground responses, typify those that are bottom-up
driven and resemble the transitions in communities that
occur during the initial developmental phases where
available space allows colonization to outstrip extinc-
tion, and the processes associated with the linkages
among species are quite fluid. The responses in MAT
resemble a community at later stages of development
where species turnover occurs and competition and
predation play a more important role. These findings
suggest that as climate change proceeds in areas such as
arctic tundra, community-level processes that include
higher trophic level responses must be incorporated into
observations, experiments, and models to best predict
community and ecosystem changes.
ACKNOWLEDGMENTS
We gratefully thank Jim Laundre for long-term maintenanceof these experiments and the many field and lab assistantsinvolved in this project, including: Amie Treuer, CarolMoulton, Charla Jordan, Jef Knight, Brian Moon, Karl Wyant,and Greg Selby. Funding for this research was provided by theNational Science Foundation (OPP-0425827 to L. Gough,OPP-0425606 to J. C. Moore, and multiple grants to the MarineBiological Laboratory in support of the Arctic LTER, includingDEB-0423385). Logistic support was provided by Toolik FieldStation, University of Alaska, Fairbanks, and VECO PolarServices. Use of the CHN analyzer for plant tissues wasprovided by Tom Chrzanowski.
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