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Applied Vegetation Science 16 (2013) 438–447
Impacts of Tamarix-mediated soil changes on
restoration plant growth
Erik A. Lehnhoff & Fabian D. Menalled
Keywords
Exotic plants; Impacts; Invasive species;
Non-indigenous species; Plant-soil feedbacks;
Restoration; Riparian; Saltcedar;Tamarisk
Abbreviations
AMF = arbuscular mycorrhizal fungi; NIS =
non-indigenous plant species; PGC = plant
growth centre; PSF = plant-soil feedb acks; S:R
= ratio of shoots to roots; RGR = relative
growth rate
Nomenclature
USDA, NRCS (2012). The PLANTS Database
(http://plants.usda.gov, 5 November 2012)
National Plant Data Team, Greensboro, NC,
USA
Received 16 April 2012
Accepted 11 October 2012
Co-ordinating Editor: Amy Symstad
Lehnhoff, E.A. (corresponding author,
erik.lehnhoff@montana.edu) & Menalled, F.D.
(menalled@montana.edu): Department of Land
Resources and Environmental Sciences,
Montana StateUniversity, Bozeman, Montana,
USA
Abstract
Question: Do soils impacted by Tamarix spp. affect the growth of plants used for
restoration through altered soil chemistry and/or plant-soil feedbacks?
Location: The Bighorn River, the Yellowstone River and the Fort Peck Reser-
voir, Montana, western USA.
Methods: Soil was collected from paired subsites where Tamarix was either
present or absent along three water bodies. To evaluate chemical and biological
soil effects on plant growth, eight plant species (Achnatherum hymenoides,Astraga-
lus cicer,Dalea candida,Elymus lanceolatus,Leymus cinereus,Pascopyrum smithii,
Ratibida columnifera and Trifolium pratense) commonly used in restoration pro-
jects at Tamarix-invaded sites were grown in the collected soil. Plant-soil feed-
backs were evaluated by growing two species (D. candida and P. smithii)in
greenhouse soils inoculated with small amounts of the field soils. Germination,
emergence and growth characteristics were compared between Tamarix-invaded
and un-invaded subsites and across water bodies.
Results: Seedling emergence and plant relative growth rate, total biomass pro-
duction and allocation of resources to roots and shoots were not negatively
affected in field soils or in greenhouse soil inoculated with soil from areas where
Tamarix was present. In fact, overall, plants emerged earlier and produced more
biomass in soils affected by Tamarix than in soils from where Tamarix was not
present. These results indicate that for sites in the northern range of Tamarix,res-
toration would not be inhibited by Tamarix-induced soil changes.
Conclusions: Tamarix is a relatively new invader in the northern USA, and little
is known about its impacts in this area or the potential implications for restoration.
However, our results indicate that neither altered soil chemistry nor plant-soil
feedbacks negatively impact native plant growth, and restoration efforts would
not be hindered by Tamarix-induced changes to soil chemistry or microbiota.
Introduction
Restoration of plant communities after the removal of
non-indigenous plant species (NIS) is complicated by
many factors, including potential changes in soil properties
(Weidenhamer & Callaway 2010), depletion of the native
species seed bank (French et al. 2011) and increased
resource availability that promotes colonization by other
NIS (Davis et al. 2000). Also, microbe-mediated plant-soil
feedbacks (PSF) may condition the soil in a manner that
alters its suitability for the same and other plant species
(Bever et al. 1997). Plant-soil feedbacks can determine
subsequent plant growth, abundance, persistence and
competitive success through changes in decomposition
rates (Hobbie 1992; Knops et al. 2002), resource availabil-
ity (Vinton & Burke 1995; Ehrenfeld et al. 2001; Clark
et al. 2005) and/or pathogenic and mutualistic interactions
(Hamel et al. 2005; Wolfe et al. 2005).
Legacy effects of PSF are important in invaded plant
communities as they could either enhance or decrease the
performance of plants (Callaway et al. 2004; Kulmatiski &
Beard 2011). Positive PSF occur when plants accumulate
beneficial microbes in their rhizosphere, including mycor-
rhizal fungi and nitrogen-fixing bacteria, which enhance
the growth and competitive ability of conspecifics relative
to other plant species. On the other hand, negative PSF
enhance species turnover rates through the accumulation
of pathogenic microbes, parasites and herbivores in the
Applied Vegetation Science
438 Doi:10.1111/avsc.12011 ©2012 International Association for Vegetation Science
rhizosphere. In nature, positive and negative PSF seldom
occur in isolation, and there is ample evidence that the net
effect of these co-occurring events plays a vital role in eco-
system organization, functioning and dynamics (Harrison
& Bardgett 2010).
The control of Tamarix chinensis and T. ramosissima,and
hybrids of the two (Gaskin & Schaal 2002), hereafter
referred to as Tamarix, and restoration of Tamarix-invaded
sites has recently become the focus of many western land
managers (Shafroth & Briggs 2008). Tamarix are shrubs or
small trees native to Asia that have invaded riparian areas
in the southwestern and more recently the northern and
northwestern USA (Pearce & Smith 2007; Lehnhoff et al.
2011). Once established in riparian areas, Tamarix can limit
recruitment of native Populus and Salix species (Shafroth
et al. 1995) and become the dominant tree (Friedman
et al. 2005). Tamarix can alter soil chemistry by increasing
soil salinity and nutrient content (Bagstad et al. 2006;
Lehnhoff et al. 2012), reducing soil pH (Ladenburger et al.
2006) and decreasing the abundance of arbuscular mycor-
rhizal fungi (Beauchamp et al. 2005; Lehnhoff et al.
2012). While the effects of Tamarix-altered soil chemistry
on native plant establishment have been studied, the
impacts of PSF on the success of restoration plants at
Tamarix-occupied sites have not.
Restoration of Tamarix-impacted sites is difficult, and
may be unsuccessful because of interacting many factors.
Tamarix invasion is often closely related to anthropogenic
alterations of river hydrology (Stromberg et al. 2007).
Because of altered hydrology, simply removing Tamarix via
burning, herbicide or mechanical means may not lead to
the desired changes in plant communities (McDaniel &
Taylor 2003; Harms & Hiebert 2006). Invasion by other
NIS after Tamarix removal is also a concern that affects res-
toration success. In a review of restoration projects at 28
Tamarix sites in the southwestern USA, Bay & Sher (2008)
found that 19% of plant species colonizing the sites were
NIS. Finally, while it is difficult to decouple Tamarix-
induced changes to soil properties from the effects of flow
alteration, soil chemistry and PSF may have effects on the
establishment and growth of restoration plants. Indeed,
ecosystems may be altered, either directly by anthropo-
genic changes or indirectly by NIS through modified soil
chemistry or PSF, to the point where they can be consid-
ered ‘novel’ (Seastedt et al. 2008), thereby further compli-
cating restoration by making restoration targets
ambiguous.
To maximize the probability of successful restoration
after NIS management, it is crucial to first understand the
implications of such potentially novel ecosystems, includ-
ing altered soil chemistry and PSF, and second, to select
plant species adapted to the conditions present, including
both altered soil and hydrology. This study focused on
evaluating plant performance in soils altered by the pres-
ence of Tamarix. The specific objectives of this work were
to (1) assess the suitability of eight plant species (seven
indigenous and one not indigenous to Montana) for
growth at Tamarix-invaded sites on three water bodies
with different hydrology, and (2) investigate the existence
of Tamarix-induced PSF. For the first objective, we hypoth-
esized that plant species performance would vary between
soils from different water bodies because of differences in
soil biological and chemical characteristics. While there is
evidence that Tamarix increases soil nutrients (Ladenburg-
er et al. 2006; Lehnhoff et al. 2012; Meinhardt & Gehring
2012), which could be beneficial for plant growth, we
tested the common assumption that plants would perform
worse in soils from where Tamarix was present because of
increased salinity. For the second objective, no a priori
hypotheses were developed due to the lack of pre-existing
information on the potential impacts of Tamarix on PSF.
However, previous research has shown a variety of impacts
of Tamarix on soil biota that could potentially lead to nega-
tive PSF. For example, Meinhardt & Gehring (2012)
showed that the presence of Tamarix reduced the coloniza-
tion of neighbouring Populus trees by beneficial arbuscular
mycorrhizal fungi (AMF), and Moseman et al. (2009)
found altered diversity and activity of nitrogen-fixing
bacteria in Tamarix-invaded wetlands.
Methods
Site descriptions and soil collection
Three replicate sites were selected along each of three
water bodies with contrasting hydrology in Montana: the
dam-controlled Bighorn River, which experiences annual
flooding; the unregulated Yellowstone River, which also
floods annually but with higher flow than the Bighorn
River; and the Fort Peck Reservoir, which has fluctuating
water levels (Fig. 1). The Bighorn River sites included the
public access points of Arapooish, General Custer and
Grant Marsh. The Yellowstone River sites included the
public access points of Bundy Bridge, Duck Creek Bridge
and Isaac Homestead. Finally, the Fort Peck Reservoir sites
included the Dam, Dry Arm and Sand Arroyo. The oldest
living Tamarix trees at the Yellowstone, Bighorn River and
Fort Peck Reservoir sites were 23, 37 and 15 yr respectively
(Lehnhoff et al. 2011). At each of these sites we selected
two subsites –one with Tamarix present and one without
Tamarix. Vegetation at the adjacent subsites was similar,
with invaded subsites with Tamarix simply adding to the
species richness but not otherwise changing species com-
position or diversity (Lehnhoff et al. 2012). At each sub-
site, 20 aliquots of soil, including the overlying plant litter,
were collected with a shovel at randomly located positions
to a depth of 15 cm and placed into two 18.9-L plastic
Applied Vegetation Science
Doi: 10.1111/avsc.12011©2012 International Association for Vegetation Science 439
E.A. Lehnhoff & F.D. Menalled Tamarix-affected soil
buckets. At the subsites with Tamarix present, soil was col-
lected from directly under Tamarix trees, where there was
generally no other vegetation present. Composite soil sam-
ples from each subsite were collected from the buckets and
analysed for organic matter (OM), nitrate (NO
3), phos-
phorus (P) and potassium (K
+
) concentrations. In a previ-
ous study, samples were also collected and analysed for
electrical conductivity (EC), pH, calcium (Ca
2+
), K
+
,
sodium (Na
+
)andmagnesium(Mg
2+
), and the sodium
adsorption ratio (SAR) was calculated. These data were
previously reported in Lehnhoff et al. (2012; Table 1).
Buckets of soil were taken to the Montana State University
Plant Growth Center (PGC) and kept in cold storage
(12.8 °C) until the experiments began ca. 4 wk later.
Plant growth in field-collected soils
The species for this study were all mycorrhizal and
included (1) four grasses –Leymus cinereus (Scribn. & Merr.)
A. Love (basin wildrye), Achnatherum hymenoides Roem. &
Schult. (Indian ricegrass), Elymus lanceolatus (Scribn. & J.G.
Sm.) Gould subsp. Lanceolatus (thickspike wheatgrass) and
Pascopyrum smithii (Rydb.) A. Lo
¨ve (western wheatgrass),
and (2) four forbs –Ratibida columnifera (Nutt.) Woot. &
Standl. (stillwater prairie coneflower), Astragalus cicer (Cic-
er milkvetch), Trifolium pratense L. (red clover) and Dalea
candida (Michx.) ex Willd. (antelope prairie clover). Except
for T. pratense, all species are indigenous to Montana and
all of them are commonly used for restoration. The four
grasses are specifically recommended by the Montana Nat-
ural Resources Conservation Service for re-vegetation of
Tamarix-invaded areas in Montana (USDA 2010), and the
forbs are commonly used in restoration of prairie sites that
are similar to areas above the typical river high water levels
and in the reservoir drawdown area. Seeds for all species
were obtained from the Bridger Plant Materials Center in
Bridger, Montana.
To evaluate the germinability of seeds, 20 seeds of each
species were placed on germination paper (regular weight
blue paper; Anchor Paper Co., St. Paul, MN, USA) in 11 9
11 93.5 cm germination trays, with three replicates for
each species. The trays were covered with lids, kept in the
greenhouse in ambient light and at temperatures of 21 °C
(day, 16 h) and 16.5 °C (night, 8 h), and the germination
paper was moistened daily with distilled water. The total
number of germinants in each tray was recorded at 11 d.
The growth study evaluated the joint biologically and
chemically mediated impacts of Tamarix on plant seedling
emergence and growth. Eight plant species were grown in
soils collected fromthe nine field sites (18subsites) as a com-
pleteblock,randomizeddesigntoassessthespecies’potential
for restoration planting at Tamarix-invaded areas. For these
experiments, subsite soils were individually placed into 3.8-cm
diameter by 21-cm deep pots (Ray Leach ‘Cone-tainer’,
model SC10,hereafter ‘conetainer’), with four replicates for
each species-subsite combination. Five seeds were planted
per conetainer, daily seedling emergence was recorded, and
seedlings were subsequently thinned to one per pot. Plants
were grown for 10 wk in the PGC with ambient light and
temperatures of 21 °C (day, 16 h) and 16.5 °C(night,8 h),
and watered threetimes daily with anautomatic mistingsys-
tem. Plants were then removed from the conetainers,
washed over a screen to remove soil from the roots, and the
above-and below-groundportions of theplants placedsepa-
rately into envelopes for drying. Plant material was dried at
40 °Cfor1 wk and weighedtothenearest0.001 g.
Seed germinability was calculated as the mean number
of seeds that had germinated at the end of 11 d. For seeds
in conetainers, the mean time (days) to >50% emergence
was calculated as in Menalled et al. (2005) to provide a
relative assessment of species emergence times in different
soils, with the assumption that earlier emerging species
would have a competitive advantage over undesirable
weedy species at restorations sites. Effects of the different
soils on seedling emergence were evaluated with a nested
ANOVA with subsite nested within water body. The ratio
of above- to below-ground biomass, i.e. shoot to root ratio
(S:R), was calculated as the shoot biomass divided by root
Fig. 1. Soil collection locations on the Fort Peck Reservoir, Bighorn River and Yellowstone River sites in Montana, USA.
Applied Vegetation Science
440 Doi:10.1111/avsc.12011 ©2012 International Association for Vegetation Science
Tamarix-affected soil E.A. Lehnhoff & F.D. Menalled
biomass. Nested ANOVA models were also used to evalu-
ate plant biomass and S:R, and data were log transformed
prior to analysis to meet the assumptions of normality. All
data analyses were performed in R (R version 2.12.1; R
Foundation for Statistical Computing, Vienna, AT).
Plant-soil feedback
The PSF study addressed the Tamarix biologically mediated
effects on plant growth. The study was conducted as a
complete block, randomized design with soil from the 18
subsites, two soil treatments, two plant species, two plant
harvest times and four replicates. One half of the soil from
each subsite was steam-pasteurized (Lindig soil treatment
system, 1 h at 70 °C) and the other half was untreated.
Pots (10-cm base, 16-cm top, 41-cm high; I.E.M. Plastics,
Reidsville, NC, US) were filled with a 1:1:1 mix of mineral
soil, Canadian sphagnum peat moss and washed sand, all
pasteurized. All pots were then inoculated with the field
soil, with half of them randomly receiving steamed soil
and the other half untreated soil. Soil inoculation was con-
ducted by mixing 69 cm
3
(ca. 1% of the pot volume) of the
field-collected soil within the top 2 cm of the greenhouse
soil mix and then watering. The small amount of inoculum
was used to avoid altering the chemical properties of the
greenhouse soil, while adding the soil microbiota occurring
at the field subsites. Pots were then planted with seeds of
either the forb D. candida or the grass P. smithii. Green-
house conditions were maintained at 23.9 °C (day, 16 h)
and 20 °C (night, 8 h), with light supplemented with mer-
cury vapour lamps (165 lmolm
2
s
1
). To assess changes
in relative growth rate as a function of PSF, half of the
plants were harvested at 55 d after planting and the
remaining plants were harvested at 80 d after planting.
The shoot to root ratio, S:R, was calculated as above,
and relative growth rate (RGR) was calculated as:
RGR ¼lnðB2ÞlnðB1Þ
T2T1
ð1Þ
where B
1
was the total biomass (both roots and shoots) at
the initial harvest, B
2
was the total biomass at the final
harvest, T
1
is the number of days until the initial harvest,
and T
2
is the number of days until the final harvest. Total
biomass and S:R were log transformed prior to analysis to
meet the assumptions of normality. Differences in S:R,
RGR and total biomass across soil treatments and species
with subsites nested within water bodies were evaluated
Table 1. Soil chemistry at sites with and without Tamarix.
Soil parameter Tamarix status Water body
Fort peck reservoir Bighornriver Yellowstone river
2009 soil samples
EC (dSm
1
)Absent 0.48 (0.21) 0.85 (0.42) 1.16 (0.72)
Present 0.97(0.78) 1.01 (0.30) 1.50 (1.22)
pH (standard units) Absent 7.84 (0.31) 7.54 (0.18) 7.78 (0.19)
Present 7.77 (0.32) 7.41 (0.21) 7.64 (0.16)
Ca
2+
(mmol l
1
)Absent 1.96 (1.37) 4.62 (0.68) 7.92 (5.88)
Present 5.32(6.60) 5.58 (1.62) 9.44 (8.97)
K
+
(mmol l
1
)Absent 0.56 (0.36) 2.34 (0.80) 0.45 (0.36)
Present 1.02(0.75) 2.56 (0.69) 0.56 (0.34)
Na
+
(mmol l
1
) Absent 1.17 (1.25) 0.29 (0.15) 1.43 (1.04)
Present 0.95 (0.75) 0.76 (0.46) 2.63 (3.47)
Mg
2+
(mmol l
1
)Absent 1.05 (0.61) 1.63 (0.30) 2.92 (2.27)
Present 2.89(3.43) 2.20 (0.67) 3.30 (3.04)
SAR Absent 1.29 (1.79) 0.17 (0.08) 0.63 (0.23)
Present 0.52 (0.38) 0.39 (0.25) 0.89 (0.92)
2010 soil samples
NO
3(mgkg
1
) Absent 3.50 (1.80) 11.17 (1.89) 2.83 (1.53)
Present 18.67 (27.15) 24.67 (2.52) 14.83 (15.46)
K
+
(mgkg
1
) Absent 229.67 (111.38) 281.33 (100.07) 150.33 (51.03)
Present 224.67 (57 .47) 530.00 (83.86) 220.67 (85.34)
P(mgkg
1
) Absent 4.00 (2.00) 6.67 (0.58) 6.67 (3.06)
Present 6.33 (4.93) 27.00 (4.00) 9.00 (2.65)
OM (%) Absent 1.20 (0.36) 2.50 (0.79) 0.77 (0.21)
Present 1.37 (0.21) 3.37 (1.66) 1.07 (0.64)
Means are presented with SD in parentheses. Bold indicates significant differences (P=0.05) of soil property between Tamarix-occupied and unoccupied
subsites.Data adapted from: Lehnhoff et al. (2012).
Applied Vegetation Science
Doi: 10.1111/avsc.12011©2012 International Association for Vegetation Science 441
E.A. Lehnhoff & F.D. Menalled Tamarix-affected soil
with generalized linear models (GLMs) because of missing
values (i.e. plants that did not grow). Model simplification
was implemented by removing non-significant terms and
conducting ANOVA between the models with a Chi-
squared distribution. If the P-value was >0.05, the test indi-
cated that removing the terms did not decrease the model’s
explanatory power, and the simpler model was retained.
Results
Plant growth in field-collected soil
From the germination test, the percentage (±SD) of seeds
that germinated for each species at 11 d was: L. cinereus,
41.7 ±17.6; A. hymenoides,0.0±0.0; E. lanceolatus,
30.0 ±13.2; P. smithii,28.3±7.6; D. candida,45.0±0.0;
A. cicer,3.3±2.9; T. pratense,58.3±7.6; and R. columnif-
era,95.0±0.0. The fact that A. hymenoides did not germi-
nate in the germination test (which was conducted on
germination paper rather than soil) indicated that the
seeds were either dormant or had very low viability.
A. hymenoides also exhibited very poor emergence across
all subsites in subsequent experiments; therefore, data for
this species were not included in further analysis. A. cicer
also had low germination at 11 d, but more seeds germi-
nated over time (data not shown); therefore it was
included in further analysis.
For the number of days to 50% emergence of seedlings
in the conetainers, the three-way interaction of species,
water body and subsite (i.e. the presence or absence of
Tamarix) was significant (F
18,462
=2.43, P=0.001). To
investigate these complex interactions, the species at indi-
vidual water bodies were examined separately. Only
L. cinereus (F
1,22
=337.5, P=0.011) and D. candida
(F
1,22
=580.2, P=0.004) at the Bighorn River, and
D. candida (F
1,22
=408.4, P=0.023) at Fort Peck Reservoir
exhibited differences in emergence time between subsites,
emerging a mean of 7.5, 9.8 and 8.3 d earlier, respectively,
in soil from subsites with Tamarix present.
PlantsgrowninsoilfromsiteswhereTamarix was pres-
ent generally had a higher S:R and produced more total
biomassthanthosegrowninsoilfromsubsiteswhere
Tamarix was absent (Table 2), although there were interac-
tions between species and water bodies (Table 3). Again, to
explore these interactions, species at individual water
bodies were examined separately. At the Bighorn River,
D. candida (F
1,20
=7.76, P=0.011) and T. pratense
(F
1,22
=12.75, P=0.002) allocated more resources to
above-ground biomass in soil collected from subsites with
Tamarix present, while the allocation pattern was the oppo-
site for A. cicer (F
1,21
=5.12, P=0.034) at the Yellowstone
River. At Fort Peck Reservoir, all species except T. pratense
(F
1,21
=0.17, P=0.684) allocated more resources to
above-ground biomass in soils from subsites with Tamarix.
At the water body level, with all species included, more
biomass was produced in soil from subsites where Tamarix
was present than where it was absent for all three water
bodies, but the difference was higher at FortPeck Reservoir
(+147%) than at the Bighorn (+68%) or Yellowstone
Rivers (+50%) (Table 2). At Fort Peck Reservoir, S:R was
also higher at the subsites with Tamarix than at those with-
out it.
For individual species, more total biomass was produced
in soils from subsites with Tamarix at the Bighorn River for
L. cinereus (F
1,22
=18.10, P<0.001), E. lanceolatus (F
1,22
=
7.84, P=0.010), P. smithii (F
1,22
=13.05, P=0.002) and
A. cicer (F
1,19
=17.40, P=0.001) than from susbsites
where Tamarix was absent. At the Yellowstone River,
A. cicer (F
1,21
=15.49, P=0.001), R. columnifera (F
1,21
=
8.80, P=0.007), L. cinereus (F
1,22
=18.26, P<0.001) and
E. lanceolatus (F
1,22
=18.86, P<0.001) also produced
more biomass in soils from subsites with Tamarix.This
same pattern was true at Fort Peck Reservoir for T. pratense,
R. columnifera,L. cinereus,E. lanceolatus and P. smithii.For
soils only from subsites where Tamarix was present, species
biomass production differed by water body (F
2,228
=47.03,
P<0.001), with biomass generally being the highest at
the Bighorn River, although there were interactions
between site and species (F
12,228
=4.52, P<0.001; Fig. 2).
Within water bodies at Tamarix-present subsites, there
were few differences in species performance, although
T. pratense produced more biomass than the other species
at the Bighorn (F
6,75
=7.21, P<0.001) and Yellowstone
River (F
6,77
=11.86, P<0.001) sites, and D. candida pro-
duced less biomass than E. lanceolatus or P. smithii
(F
6,76
=3.00, P=0.011) at Fort Peck Reservoir (Fig. 3).
Plant-soil feedback study
The ANOVA comparisons between RGR models indicated
that removing interaction terms between subsite (Tamarix
presence or absence) nested within water body and steam
pasteurization and species did not reduce the explanatory
power of the model (P=0.603, df
full model
=145, df
reduced
model
=160), and thus the simpler model was retained.
Removing steam pasteurization from the simplified model
reduced its explanatory power (P=0.040, df
model with
steam
=160, df
model without steam
=162), indicating that
steam pasteurization of soil inoculum affected RGR. Pas-
teurization of the soil increased RGR (P=0.020) from
0.064 to 0.084 gg
1
d
1
, suggesting that soil microbes
negatively affected plant RGR. However, the lack of signifi-
cance in interaction terms indicated that the presence or
absence of Tamarix at subsites did not affect the growth of
either species when soil from the subsites was used as inoc-
ulum for greenhouse soils. ANOVA results for S:R models
showed that neither steam pasteurization (P=0.140,
Applied Vegetation Science
442 Doi:10.1111/avsc.12011 ©2012 International Association for Vegetation Science
Tamarix-affected soil E.A. Lehnhoff & F.D. Menalled
df
model with steam
=160, df
model without steam
=162), nor the
interaction terms (P=0.626, df
full model
=145, df
reduced
model
=160) were significant. Results were similar for total
biomass, with non-significant steam pasteurization
(P=0.893, df
model with steam
=160, df
model without
steam
=162) and the interaction (P=0.502, df
full
model
=145, df
reduced model
=160) terms. These results indi-
cate that soils from subsites with and without the presence
of Tamarix did not have different effects on plant S:R or
total biomass growth.
Discussion
Plant growth results from the conetainer experiment are
not consistent with the hypothesis that plants grown in
Tamarix-affected soil would grow more poorly than in
non-affected soil; rather, they indicate either that Tamarix
conditioned the soil in a manner to make it more suitable
for growth of other plants, or that Tamarix had colonized
and occupied more fertile soils. The former possibility is
supported by numerous studies showing that NIS have leg-
acy effects on soils (Ehrenfeld 2010). For example, N-fixing
NIS can alter ecosystem nutrient dynamics by directly
increasing N levels (Vitousek & Walker 1989), litter
decomposition rates can be increased (Liao et al. 2008)
providing more nutrients, and soil chemistry can be chan-
ged through altered pH or redistribution of salts from the
lower soil profile (Vivrette & Muller 1977; Conser & Con-
nor 2009). Soil samples collected from the subsites
(Table 1) showed that concentrations of NO
3,K
+
and P at
the Bighorn River, and Ca
2+
,K
+
and Mg
2+
at Fort Peck Res-
ervoir, were over twice as high at subsites with Tamarix
than without it. Yellowstone River soils showed a similar
pattern of nutrient concentrations between Tamarix pres-
ent and absent sites, although the results were not statisti-
cally significant. Higher nutrient concentrations under
Tamarix stands have been observed by others (Bagstad
et al. 2006; Xu et al. 2006; Yin et al. 2010) and may
explain differences in plant growth in our conetainer
study. Native plant species germination and growth in
Tamarix-affected soils may be negatively affected by elevated
soil salinity [measured as electrical conductivity (EC)]. For
example, plant communities separated along salinity
gradients (EC up to 15 and 12.8 dSm
1
) in north-central
Table 2. Mean ratio of shoots to roots (S:R) and total biomass produced by plants grown in soils from subsites with or without Tamarix present.
Species S:R Total Biomass (g)
Tamarix absent Tamarix present Tamarix absent Tamarix present
Species differences
Dalea candida 1.27 (0.36) 1.56 (0.48) 0.10 (0.05) 0.12 (0.06)
Leymus cinereus 0.92 (0.36) 0.99 (0.33) 0.07 (0.05) 0.19 (0.13)
Astragalus cicer 1.41 (0.58) 1.41 (0.52) 0.07 (0.05) 0.14 (0.09)
Trifolium pratense 1.25 (0.49) 1.42 (0.40) 0.27 (0.23) 0.42 (0.40)
Ratibida columnifera 0.66 (0.22) 0.64 (0.25) 0.12 (0.09) 0.17 (0.11)
Elymus lanceolatus 0.91 (0.34) 1.10 (0.47) 0.12 (0.08) 0.21 (0.10)
Pascopyrum smithii 0.90 (0.32) 1.00 (0.33) 0.10 (0.06) 0.21 (0.12)
Combined vegetation 1.04 (0.46) 1.16 (0.50) 0.12 (0.12) 0.21 (0.20)
Water body differences
Bighorn river 1.16 (0.43) 1.35 (0.65) 0.19 (0.16) 0.32 (0.27)
Yellowstone river 1.09 (0.50) 1.00 (0.35) 0.10 (0.10) 0.15 (0.13)
Fort peck reservoir 0.87 (0.39) 1.13 (0.40) 0.07 (0.03) 0.17 (0.13)
SD in parentheses; bold indicates significant biomass differences (P0.05) between Tamarix-occupied and -unoccupied subsites.
Table 3. ANOVA table for shoot to root ratio (S:R) and total biomass of
restoration plant species (Dalea candida, Leymus cinereus, Astragalus
cicer, Trifolium pratense, Ratibida columnifera, Elymus lanceolatus and
Pascopyrum smithii) grown in soil collected from subsites with or without
Tamarix at three water bodies (Bighorn River, Fort Peck Reservoir and
Yellowstone River).
Source of variation df Sum
squares
Mean
square
FP
S:R
Species 6 33.775 5.629 61.021 <0.001
Water body 2 4.136 2.068 22.420 <0.001
Water body 9soil 3 3.303 1.101 11.935 <0.001
Species 9sater body 12 1.987 0.166 1.795 0.047
Species 9water body
9soil
18 2.261 0.126 1.361 0.146
Residuals 450 41.512 0.092
Total biomass
Species 6 49.664 8.227 21.490 <0.001
Water body 2 68.689 34.345 89.168 <0.001
Water body 9Soil 3 51.636 17.212 44.687 <0.001
Species 9water body 12 49.132 4.094 10.630 <0.001
Species 9water b ody 18 14.565 0.809 2.101 0.005
Residuals 459 173.325 0.385
Applied Vegetation Science
Doi: 10.1111/avsc.12011©2012 International Association for Vegetation Science 443
E.A. Lehnhoff & F.D. Menalled Tamarix-affected soil
Utah and on the Colorado River, respectively (Carman &
Brotherson 1982; Busch & Smith 1995). However, EC lev-
els at the water bodies we studied were all less than 2.0
dSm
1
, which is considered below the level at which
plants experience detrimental effects (Taylor & McDaniel
1998). In accordance, seedling emergence in our study
Fig. 2. Comparison of individual plant species biomass growing insoils collected from sites where Tamarix was present at three water bodies in Montana.
Shaded barsare the mean and error barsrepresent 1 SE. Within species, siteslabelled with different letters have significantly different (P<0.05) means.
Fig. 3. Comparison of plant species biomass within individual water bodies. Plants grown in conetainers in soil collected from subsites where Tamarix was
present at three water bodies in Montana. Shaded bars are the mean and error bars represent 1 SE. Within sites, species labelled with different letters have
significantly different (P<0.05) means.
Applied Vegetation Science
444 Doi:10.1111/avsc.12011 ©2012 International Association for Vegetation Science
Tamarix-affected soil E.A. Lehnhoff & F.D. Menalled
was not negatively impacted when growing in Tamarix-
invaded soils.
Results from the PSF study indicated that negative feed-
backs from Tamarix on the growth of native species did not
exist. PSF may be observed deeper in the soil profile where
soils are more affected by Tamarix roots than by plant litter.
However, PSF in the 0–15 cm depth that we investigated
are more directly related to restoration, as this is the depth
important for initial establishment and subsequent rooting
of the forb and grass restoration species. The results gener-
ally indicated that any biological differences in the soil
between sites where Tamarix was present and absent were
not enough to stimulate differences in plant growth. A bio-
logical factor that could potentially alter plant growth is
the presence or absence of AMF in the soil. Pringle et al.
(2009) showed that plant–mycorrhizal symbioses are
affected by NIS, with implications for the plant-soil ecosys-
tems including alteration of the microbial community
(Mummey & Rillig 2006), influences on nutrient availabil-
ity, and disruption of symbiosis (Stinson et al. 2006).
Beauchamp et al. (2005) showed that Tamarix is non-my-
cotrophic, suggesting that sites occupied by Tamarix would
have lower levels of AMF propagules. Lehnhoff et al.
(2012) found that soils with Tamarix present had reduced
numbers of mycorrhizal propagules in the soil, although
this did not appear to cause differences in plant growth in
this study.
Our study addressed Tamarix impacts on soil chemistry
and microbially mediated PSF, and results indicated that
all species studied (with the exception of A. hymenoides,
which had poor germination) would be suitable for resto-
ration planting in Tamarix-impacted soil. However, water
body differences in soil and hydrology may also be impor-
tant in species success. Nutrient concentrations were gen-
erally higher at the Bighorn River than at the other water
bodies (Lehnhoff et al. 2012), and these differences could
be driving the biomass differences observed. Site hydrol-
ogy, and specifically water availability during the growing
season, was not addressed in this study, but should be con-
sidered when choosing restoration plant species. Bay &
Sher (2008) showed that proximity to perennial water was
an important factor in establishment of native species in
Tamarix site restoration. In sites located at a considerable
distance from perennial water, such as at the Fort Peck
Reservoir when the reservoir is in a period of drawdown,
drought-tolerant species would be required for restoration.
Flood-tolerant species would be necessary for the free-
flowing systems such as the Yellowstone River. Along the
dam-controlled Bighorn River, where flooding does not
occur annually, a mix of drought- and flood-tolerant spe-
cies may be more appropriate. In future research, the spe-
cies used in this study should be tested at field sites to
evaluate their performance.
Finally, it should be recognized that Tamarix is a rela-
tively new invader in the northern and northwestern
USA, being present in Montana for ca. 50 yr, and for only
15–37 yr at the study sites, so the time Tamarix has had to
affect soils is limited. Soil impacts, including both chemical
and PSF, could be important factors in the future. None-
theless, with the annual flooding of the Yellowstone River,
the periodic flooding of the Bighorn River and the periodic
rise and fall of the water level in Fort Peck Reservoir,
Tamarix effects on the soil are expected to be minimal as
compared with rivers in the southwestern USA where
stream flow patterns have been greatly altered and flows
reduced (Stromberg et al. 2007). Overall results indicate
that Tamarix-affected soil does not inhibit the growth of
other plant species at sites in its northern range where it is
a relatively new invader.
Acknowledgements
This work was funded by a grant from the Montana Nox-
ious Weed Trust Fund (MDA-061 G). We thank Cathy
Zabinski for review of an earlier version of this manuscript,
and Dan Campbell and Kimberley Taylor for assistance
with soil collection and greenhouse work. Patricia Gilbert
(US Army Corps of Engineers, Fort Peck Reservoir) pro-
vided invaluable assistance in accessing sites and collecting
soil samples at Fort Peck Reservoir. We also thank two
anonymous reviewers and the associate editor for com-
ments that improved this manuscript.
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