Biogeochemical impacts of the northward expansion of kudzu
under climate change: the importance of ecological context
JONATHAN E. HICKMAN1,3, 2
AND
MANUEL T. LERDAU2
1
Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York 11794-5245 USA
Departments of Environmental Sciences and Biology, University of Virginia, Charlottesville, Virginia 22904 USA
Citation: Hickman, J. E., and M. T. Lerdau. 2013. Biogeochemical impacts of the northward expansion of kudzu under
climate change: the importance of ecological context. Ecosphere 4(10):121. http://dx.doi.org/10.1890/ES13-00142.1
Abstract. Climate change is generally expected to push plant species to higher latitudes and elevations;
how the climate-induced migrations of disruptive invasive species may affect higher-latitude ecosystems
has not been widely examined. Kudzu (Pueraria montana) has large impacts on nitrogen (N) cycling and
trace N gas emissions in the southeastern United States. To understand how its projected northward
migration under climate change will impact ecosystems in the northeastern United States, we examine the
impacts of kudzu in the Mid-Atlantic region, near kudzu’s northern invasion front. We pair plots invaded
by kudzu with adjacent uninvaded plots, and examine rates of leaf litter decomposition, soil nitrogen pools
and net cycling rates, N trace gas emissions, and microbial dynamics. Kudzu litter has more N and
decomposes faster than litter from co-occurring species. Unlike in Georgia, near the center of kudzu’s
current range in the United States, kudzu invasion in the Mid-Atlantic has very small ecosystem impacts,
causing significant increases only in the sizes of soil nitrate pools. These Mid-Atlantic ecosystems may be
buffered against invasion impacts, creating a lag between changes in the plant community and
biogeochemical changes. A combination of factors, including time since establishment, soil types, growing
season length, and temperatures, may limit kudzu’s biogeochemical impacts along its invasion front.
Key words: climate change; invasive species; kudzu; Maryland; nitric oxide; nitrogen cycling; nitrous oxide; Pueraria
montana var. lobata; range expansion.
Received 17 April 2013; accepted 5 June 2013; final version received 18 July 2013; published 14 October 2013.
Corresponding Editor: N. Barger.
Copyright: Ó 2013 Hickman and Lerdau. This is an open-access article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided
the original author and source are credited. http://creativecommons.org/licenses/by/3.0/
3
Present address: The Earth Institute at Columbia University, Palisades, New York 10025 USA.
E-mail: [email protected]
INTRODUCTION
reshuffling of communities is how species—
including invasive species—that play important
roles in biogeochemical processes will respond to
the changing climate (Walther 2009), and how
this interaction between climate change and
species invasions will affect ecosystem processes.
While field, greenhouse, and modeling studies
have examined the physiological and distributional responses of species and communities to
changes in climate and atmospheric CO2 concentrations (e.g., Sasek and Strain 1988, Higgins and
Harte 2006), the question of how species—
Plant invasions and climate change are two
major global change factors threatening ecosystems, and there may be important interactions
between the two. Populations are generally
expected to migrate to higher latitudes or higher
elevations as warmer winters allow species to
expand their ranges, and higher summer temperatures make lower latitudes or elevations less
habitable (e.g., Kingsolver et al. 1992, Parmesan
and Yohe 2003). One question in climate change’s
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HICKMAN AND LERDAU
particularly those with physiological characteristics likely to disrupt biogeochemical processes—
will affect ecosystems as they expand into higher
latitudes has not received the same attention.
Community composition and individual species are important drivers of ecosystem processes, along with other factors, such as soil and
climate (e.g., Vitousek and Walker 1989, Hobbie
1992, Hooper and Vitousek 1998, Erickson et al.
2001). But community composition and species
effects on ecosystem processes can vary depending on the environmental context. For example,
outside of climate’s direct effect on soil nutrient
cycling (e.g., the direct effects of temperature on
enzyme activity), it can also have indirect effects
through its influence on broad and speciesspecific plant physiology, modulating community and species-specific impacts on ecosystems
(e.g., temperature and freezing event effects on
nodulation rates in legumes). In addition, ecosystems may be buffered against species-induced
changes to ecosystem processes such as nutrient
cycling, with lags in ecosystem responses to
changes in community composition (e.g., Wardle
et al. 1999, Compton et al. 2004, Latty et al. 2004,
Hamman and Hawkes 2012). These interactions
between climate and plant physiology and the
buffering capacity of ecosystems are not as well
studied as the independent direct effects of
climate or species, but may be equally important.
These effects can be particularly important in the
application of ecosystem models to understand
how plant invasions and changes in community
composition are likely to affect ecosystems (e.g.,
Levine et al. 2006). If models do not incorporate
buffering effects or the interactions between
climate and the physiology of key invasive
species that move northward with climate
change (e.g., ecosystem buffering against N
inputs or the effects of temperature on root
nodulation rates), they may severely under- or
over-estimate species and community effects on
ecosystem processes.
Kudzu (Pueraria montana), a fast-growing
leguminous vine native to Asia, is expected to
move northward by hundreds of kilometers as
global temperatures increase, and it is likely to
have a range of ecosystem impacts throughout its
new distribution (Sasek and Strain 1991). Vines
are notoriously susceptible to freezing embolisms, and warmer winters are expected to allow
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kudzu to expand northward in coming decades
(Wechsler 1977, Sasek and Strain 1991, Schnitzer
and Bongers 2002). This expansion may be aided
by increasing CO2 concentrations: vines in
general have shown larger and more sustained
growth responses to increased CO2 than trees
(Hattenschwiler and Korner 2003), and the
growth responses of N-fixers such as soybean
have shown little acclimation to elevated CO2
(Ainsworth et al. 2002).
Currently estimated to be spreading by 50,000
ha yr1, kudzu already covers over 3 million ha
in the southeastern United States, roughly
equivalent to the acreage of soybean agriculture
in the region, making it the dominant nitrogenfixer in the southeastern United States of America
(USDA 2002, Forseth and Innis 2004). Kudzu
exhibits a high degree of nodulation and nitrogenase activity in the United States, and a
capacity for high rates of nitrogen (N) fixation
has been observed in its native range (Lynd and
Ansman 1990, Forseth and Innis 2004). Although
fixation rates have not been measured in the U.S.,
kudzu is accelerating N mineralization and
nitrification rates in Georgia soils, sometimes by
an order of magnitude (Hickman et al. 2010).
Kudzu’s impact may extend to the atmosphere
by contributing to increased concentrations of
tropospheric ozone, an important air pollutant in
terms of its impacts on human health and
agriculture (Hickman et al. 2010). Kudzu’s
physiology is unusual in that it can increase
ecosystem-scale emissions of the key precursors
to tropospheric ozone formation: it is a moderateto high-emitter of the biogenic VOC isoprene,
(C5H8) and has been shown to double soil
emissions of nitric oxide (NO) (Sharkey and
Loreto 1993, Hickman et al. 2010).
Though kudzu’s expansion northward is well
documented and understood (Wechsler 1977,
Sasek and Strain 1991, Ainsworth et al. 2002,
Lamont and Young 2004), and it has large
impacts on N cycling and NO emissions in
Georgia (Hickman et al. 2010), it is difficult to
predict how kudzu will affect ecosystems in the
northeastern United States. As described above,
when kudzu expands into new areas, differences
in climate and growing season length will alter
its physiology and may moderate its inputs of N
to ecosystems. Soils may be buffered against
kudzu N inputs, and interactions with native
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HICKMAN AND LERDAU
litter may retard nutrient release during decomposition, so that biogeochemical impacts may lag
considerably behind changes in community
composition (e.g., Wardle et al. 1999, Compton
et al. 2004, Hamman and Hawkes 2012, Hickman
et al. 2013).
We examine how kudzu invasions affect a
range of ecosystem properties at the northern
edge of its distribution as a guide for understanding possible impacts from its future expansion into the Northeast. We expect the cooler
temperatures that predominate in the northern
part of kudzu’s distribution to limit kudzu
productivity and reduce N-fixation rates on a
per unit area basis. These effects, in combination
with the later establishment of kudzu in the MidAtlantic, are likely to reduce potential differences
in N cycling and trace N gas production between
invaded and uninvaded soils relative to the
differences observed in the southern United
States. While a decadal scale common garden
experiment is essential for distinguishing climatic
from buffering effects on kudzu’s impacts, a field
study such as is reported here is necessary to
understand the scope and magnitude of these
two important questions.
MATERIALS
AND
We selected three sites where kudzu was wellestablished: McKee-Beshers Wildlife Management Area in western Montgomery County,
MD (N 39 05.107, W 077 25.871), the Summit
Hall Turf Farm, also in Montgomery County (N
39 05.315, W 077 26.556), and the Smithsonian
Environmental Research Center (SERC) in Anne
Arundel County, MD (N 38 51.945, W 076
33.815). Kudzu was well-established at SERC
by 1975 (D. Whigham, personal communication), is
believed to have established at McKee-Beshers
before 1983 (K. D’Loughy, personal communication), and is believed to have established at
Summit Hall before 1970 (D. Wilmot, personal
communication).
Experimental design
The paired-site design has become common in
studies of the effects of N-fixers on soil N studies
and gas fluxes (e.g., Ashton et al. 2005). At each
site, an invaded location was established within a
stand of kudzu, and an uninvaded location was
established in an area where kudzu had not
invaded, within 40–200m of the kudzu stand, for
a total of six paired locations. At SERC, the
invaded location was within a former agricultural field where kudzu has been present for over 30
years. The uninvaded location was established on
a former agricultural field abandoned 30 years
ago, cleared 10 years later, and allowed to begin
secondary succession during the last 20 years (D.
Whigham, personal communication). Soils in both
the invaded and uninvaded plots at SERC were a
well-drained Marr-Dodon complex, derived from
loamy fluviomarine deposits, with a slope of 2–58
(USDA 2008). Soils at all plots in McKee-Beshers
and Summit Hall were well-drained Penn silt
loam. At McKee-Beshers, both plots had 3–88
south-facing slopes; the plots at Summit Hall had
15 to 25 degree slopes (USDA 2008). The area
adjacent to these plots has been managed as a
flooded bottomland swamp for over 40 years; no
management is conducted in the area where the
plots are located (K. D’Loughy, personal communication). Plant cover at the sites was characterized in September 2005 and was described by
Hickman and Lerdau (2006). In invaded locations at all three sites, kudzu cover ranged from
80% to 100%. Uninvaded locations at all three
sites contained primarily herbaceous species,
though the woody shrub Rosa multiflora was
METHODS
Sites
We selected sites in Maryland where winter
temperatures tend to be colder than in the center
of kudzu’s current distribution and that are
within the range that northeastern winter temperatures are expected to reach within the next
100 years. In Baltimore, MD, at a latitude where
kudzu has been successfully established for
decades, mean minimum January temperatures
were 4.78C from 1961 to 1990, roughly intermediate between means for southern sites where
kudzu is established (0.18 and 1.88C in Athens,
GA and Montgomery, AL), and means for
northern sites within the range of kudzu’s
expected expansion (9.88C to 9.28C in Poughkeepsie, NY, Worcester, MA, and Hartford, CT
[NOAA/ESRL 2008]). Minimum temperatures in
the northeastern United States are expected to
increase by roughly 2–68C by the end of the
century, making northeastern winter temperatures similar to those currently experienced in
Maryland (NCDC 2008).
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present in the uninvaded location at SERC.
Although the defined uninvaded location contained only herbaceous species at McKeeBeshers, the surrounding area contained more
and larger trees than were present in the
uninvaded areas at SERC and Summit Hall.
Senesced litter collected in litter traps (see below)
was used to evaluate community differences in
invaded and uninvaded sites. When kudzu is
excluded from the genera of litter collected in the
sites, there was no difference in the plant
communities in invaded and uninvaded plots
either on the basis of the presence/absence of
genera (P ¼ 0.277) or litter abundance by genera
(P ¼ 0.062).
bags, and major rocks, roots, and invertebrates
were removed. Subsamples from each core were
taken for laboratory analysis of moisture content,
total C and N, initial nitrate and ammonium,
microbial biomass, net mineralization and nitrification potential, and denitrification enzyme
assays (details below). Soil moisture content (g
H2O g1 dry soil) was determined by drying a
subsample at 1058C until soils were no longer
decreasing in weight. Total carbon (C) and N
content of dried, ground samples was determined using a CE Flash EA 1112 Elemental
Analyzer (CE Instruments, Milan, Italy).
Inorganic N pools
Inorganic N was extracted from soils by
placing a 10 g subsample of soil from each core
in a 120 ml polypropylene specimen cup with 50
ml 2M KCl, and shaking the cups for 60 minutes.
The soils were allowed to settle for another 60
minutes after shaking. The KCl solution from
each cup was filtered using Whatman #42 filter
paper and frozen in a 40 ml glass scintillation vial
until determinations of NO3/NO2-N and NH4þN content were made using a Lachat autoanalyzer (Lachat Quickchem Systems, Milwaukee,
Wisconsin, USA). These measurements also serve
as the initial or ‘‘pre-incubation’’ inorganic N
concentrations for the calculations of net N
mineralization and net nitrification rates.
Sample collection and preparation
Soil sampling was conducted nine times
starting in March 2006: bimonthly from March
through September in 2006 and 2007, and once in
December 2006. At each sampling time, soil cores
were taken from all sites within a single day, with
the exception of September 2007, when soils from
SERC were taken on 5 September 2007, and soils
from the other sites were taken on 6 September.
Three soil cores were taken randomly from an
area measuring 5 m 3 10 m in each location, for a
total of 18 cores per sampling time (3 cores is a
commonly-adopted sampling size in studies such
as this [Martin et al. 2003, Hawkes et al. 2005,
Haubensak and Parker 2004]). The one exception
was sampling in September 2007, when four
cores were taken per location, for a total of 24 soil
cores. At sampling, the top litter layer was
removed, and a PVC pipe (5 cm internal
diameter 3 20 cm long) was driven 12 cm into
the ground and removed with the core intact.
The cores contained little or no organic layer, so
they were not separated into different horizons
before being placed in separate polyethylene
bags. The cores were kept cool until transferred
to a refrigerator in the lab. Most lab analyses
were started within three days of soil collection,
but the denitrification assays were usually
conducted four to six days after sampling, and
analysis of soils from September 2007 were
conducted approximately two weeks after sampling. Since precipitation can stimulate microbial
activity (Paul and Clark 1996), samples were
taken at least 24 hours after any major rain event.
Soils were homogenized by hand in Ziploc
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Net N mineralization and net nitrification
Concurrent with subsampling for the initial
KCl extractions, a second 10 g soil subsample
was taken and sealed in a mason jar with a gastight lid fitted with a rubber septum. The jars
were incubated at 20–228C. After 10 days,
inorganic N was measured as described above;
these extractions represent the ‘‘post-incubation’’
inorganic N content. Net mineralization was
calculated as the difference in total inorganic N
concentrations in the pre-incubation and postincubation extractions; net nitrification was calculated similarly, as the difference in NO3-N þ
NO2-N concentrations in pre- and post-incubation soil extractions.
Soil microbial biomass
The determination of total microbial biomass
was made using the chloroform fumigation
incubation method (Voroney and Paul 1984). A
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10 g subsample of soil from each core was
fumigated for 12–18 hours. The 10 g samples of
fumigated soils and a 0.1 g fresh soil inoculum
from the same core were placed in a quart-sized
mason jar and sealed with a gas-tight lid fitted
with a rubber septum. After a 10 day incubation
at 20 –228C, a 9 ml gas sample from the
headspace of each mason jar was transferred to
an evacuated glass vial. The vials were stored at
room temperature until CO2 concentrations were
determined by gas chromatography using a
Shimadzu GC-14 GC fitted fitted with a thermal
conductivity detector. Microbial biomass-C was
calculated as the CO2-C per unit dry weight of
soil in fumigated samples, divided by a constant
(0.41) representing the fraction of biomass mineralized to CO2.
between 10 am and 6 pm to limit variation in
temperature between chambers. Sampling protocols were similar to those developed and
described in Hickman et al. (2010). Briefly, in
each invaded and uninvaded location, four
beveled, Teflon-coated PVC rings (25.5 cm
diameter) were randomly inserted several centimeters into the soil. At least 30 minutes after
inserting the ring, a Teflon-coated, molded PVC
chamber top fitted with a gas-sampling port was
inserted over the ring and made gas-tight.
Emissions of NO were measured in situ using a
portable chemiluminescent analyzer equipped
with a CrO3 filter that converts all NO to NO2
(Unisearch Associates model LMA-3D, Concord,
Ontario, Canada). Standard curves were conducted in the field before and after each set of
four measurements using a standard gas with a
known NO2 concentration (0.01 ppm, ScottMarin, Riverside, CA). Ambient NO2 concentrations were low but detectable, so NO2 concentrations within the chamber were measured
immediately before and after NO measurements
in order to measure the consumption of ambient
NO2 by soils, which was assumed to be linear.
NO emissions were measured as the linear
increase in NO concentrations in the chamber
over four minutes, and were corrected for the
consumption of ambient NO2 during that fourminute period (Hall and Matson 2003).
To measure N2O emissions, a Teflon-coated,
molded PVC chamber top fitted with a septum
was placed over each ring and made gas-tight.
Using polypropylene syringes, 9 ml gas samples
were taken from the chamber at zero, 10, 20, and
30 minutes, and transferred to evacuated glass
vials. The vials were stored at room temperature
until analysis for N2O by gas chromatography
using a Shimadzu GC-14 GC fitted with an
electron capture detector. The N2O flux was
calculated using the linear increase in N2O
concentration, the chamber volume, and the soil
surface area.
Denitrification enzyme activity
The denitrification potential of soils was
determined using the Dentrification Enzyme
Activity method (Smith et al. 1978). A medium
containing 0.72 g KNO3 and 0.5 g glucose per
liter of Nanopure H2O was created; 0.125 g
choloramphenicol was added to inhibit microbial
growth. A 5 g subsample was taken from each
homogenized soil core and placed with 10 ml
medium into a 125 ml Erlenmeyer flask with a
ground glass neck and sealed with a rubber
stopper. Flasks were made anaerobic with
repeated evacuations and flushes with N2 gas,
and 4 ml acetylene was added to each flask to
inhibit the transformation of N2O to N2 by
denitrifying bacteria. The flasks were placed on
an orbital shaker, and 9 ml samples of the
headspace of each flask were taken using a
polypropylene syringe and transferred to evacuated gas vials after one and three hours. The N2O
concentration of each vial was determined by gas
chromatography using a Shimadzu GC-14 GC
fitted with an electron capture detector. The
change in N2O concentration from time zero
through three hours was used to calculate the
denitrification rates.
Litter decomposition
Trace N gas emissions
In October 2006, newly senesced leaf litter was
collected from kudzu and 6 co-occurring woody
species (Acer rubrum, A. negundo, Carya glabra,
Fagus grandifolia, Quercus alba, and Sassafras
albidum). Litter was collected along a transect
approximately 500 m in length encompassing
The invaded and uninvaded locations at SERC
and Summit Hall were sampled for NO and N2O
emissions on 5 and 6 September 2007. Gas
measurements for each site were conducted on
the same day, and all sampling was conducted
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both invaded and uninvaded areas in the McKeeBeshers Wildlife Management Area, and running
across Penn silt loam soils. Litter bags were
constructed from nylon 1/32 inch (0.79 mm)
square mesh, measuring 15.5 cm by 12 cm along
the interior edges. Enough bags were constructed
to allow for the destructive sampling of three
replicates of each species at 18, 32, 44, and 53
weeks. Leaves were dried at room temperature,
and 2.5 g of dried litter from a single species was
placed in each mesh bag and weighed. Three 2.5
g air-dried samples from each species were
weighed, dried at 608C, and weighed again to
calculate the weight difference between air-dried
and oven-dried litter.
The litter bags were placed in the field 6
December 2006. Replicates were allocated randomly to each of three blocks located approximately 10 m apart from one another in an area of
uninvaded forest in McKee-Beshers. Within a
block, litter bags were placed randomly on a 3 m2
grid at 0.5 m intervals. At each harvest time, bags
were collected, dried at 608C, weighed, and
ground for analysis of C and N content using a
CE Flash EA 1112 Elemental Analyzer (CE
Instruments, Milan, Italy).
sary to establish new sampling locations within
some sites. Consequently, two separate analyses
were conducted: one for the 2006 growing
season, and one for the 2007 growing season.
Split-plot ANOVA’s were conducted on mean
response variables for each season, in which site
was included as a whole plot factor, and kudzu
invasion as a within plot factor. Single outliers
were excluded from the analyses of net N
mineralization and the NO3 pools in 2006, and
of net nitrification in 2007.
Analyses of the NO and N2O fluxes were also
conducted using split plot ANOVA, including
site and kudzu invasion as whole and within plot
factors, respectively. For the decomposition experiment, mass loss was analyzed in a three-way
mixed model ANOVA, including block as the
random factor, and species and harvest date as
the fixed factors. The weight of N lost from litter
over the first year was analyzed as a two-way
mixed model ANOVA, including block as the
random factor, and species as the fixed factor.
When necessary, data were log transformed or
rank transformed to meet the assumptions of
ANOVA.
RESULTS
Litter deposition
The decomposition and nutrient dynamics of
kudzu litter was clearly different from that of
native species present at the sites in Maryland.
Leaf litter from kudzu lost mass more quickly
than six co-occurring tree species in 2007 (P ,
0.0001, Fig. 1). By the end of one year, kudzu had
lost most of its mass (56.2% 6 2.3% of starting
mass), while on average, litter from each of the
other species lost between 14.0% 6 1.0% and
38.0% 6 3.0% of its initial mass. Patterns of N
loss, both as a percentage of starting N and in the
net release of N to the soil, also showed
significant differences between kudzu and the
native species (P , 0.0001). While kudzu litter
lost an average of 40.3% 6 2.38% of its starting N
after one year, litter from all but one of the native
species experienced net immobilization of N; on
average, litter from native species accumulated
34.9% more N than at the start of decomposition,
even as the mass of litter decreased (Fig. 1). In
addition, kudzu had significantly higher starting
concentrations of N, averaging more than twice
as much N as the co-occurring tree species (2.56%
Five 30.5 3 61 cm litter traps were placed in
each of the invaded and uninvaded locations in
each site (30 litter traps total) in September 2007.
Litter was collected from the traps weekly or biweekly through December 2007 and allowed to
air-dry. Litter was separated by genus, dried at
608C, and weighed. Subsamples of litter from
each genus across multiple sampling dates were
ground for analysis of C and N content using a
CE Flash EA 1112 Elemental Analyzer (CE
Instruments, Milan, Italy). The mean C and N
concentrations for each genus was calculated for
each site across sampling dates, and N inputs
were calculated for each location by multiplying
the mean N concentration for a genus by the
weight of litter deposited by that genus during
litter collection. A mean C:N for deposited litter
in each location was also calculated.
Statistical analyses
Because of site disturbances in which plot
markers were removed or destroyed between
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during both years. Where differences were
significant, the differences were in the direction
expected for a scenario in which kudzu adds N to
invaded soils: nitrate levels were 200% higher in
invaded areas across all dates (P ¼ 0.069 in 2006
and P ¼ 0.074 in 2007; Fig. 2), net N mineralization and net nitrification rates were higher under
kudzu in 2007, but not significantly so (P ¼ 0.155
and P ¼ 0.176 in 2007, respectively; Fig. 3), and
denitrification enzyme activity was lower under
kudzu in 2007, but also not quite significantly so
(P ¼ 0.11; Fig. 4). But kudzu invasion failed to
affect net N mineralization, soil ammonium, total
soil C, total soil N, microbial biomass, N2O
fluxes, or NO fluxes across sites (Figs. 2, 3, 4, and
5). We were unable to test for interactions
between site and kudzu presence, though visual
inspection of the data suggests that there may
have been some substantial effects of kudzu at
SERC during 2007 for rates of net N mineralization, net nitrification, and nitrogen oxide emissions (Figs. 5 and 6). Soil moisture did not differ
between invaded and uninvaded areas in either
year.
DISCUSSION
With its much higher leaf litter N content and
considerably faster rates of leaf litter decomposition than co-occurring species’ (Fig. 1), kudzu is
a picture-perfect example of a fast-cycling species
invading a community with more recalcitrant
litter and slower rates of nutrient cycling. Its litter
has more than twice as much N as litter from cooccurring native species, and while litter from
these native species exhibits substantial net
immobilization of N over the course of a year,
kudzu releases 40% of its initial N. Within the
framework described by Hobbie (1992), a species
such as kudzu that is able to cover large fractions
of a landscape, and which has such strikingly
different patterns of decomposition and nutrient
release to the ecosystem, should be expected to
reinforce faster rates of nutrient cycling as it
becomes established in new ecosystems.
Although kudzu leaf litter is releasing N to
soils at faster rates than the co-occurring species
and invaded sites exhibited larger total N inputs
in litter than uninvaded sites, kudzu invasion in
Maryland has not yet resulted in the consistent
increases in N cycling that have been observed in
Fig. 1. Mass loss (a) and N loss (b) during
decomposition of leaf litter from kudzu and six cooccurring woody species in Maryland during 2007.
Values are means 61 SE.
6 0.34% N for kudzu versus 1.08% 6 0.067% for
native species).
Total input of N was higher in invaded plots
than uninvaded plots (P ¼ 0.05, one-tailed test,
Table 1), but there were no differences in the
mean litter C:N. The weight of kudzu litter input
was higher in SERC than in the other two sites in
2007 (P ¼ 0.004, Table 1).
The differences in decomposition rates between kudzu and co-occurring species and the
higher rates of N input in invaded plots have not
yet contributed to consistent differences in soil N
cycling and pools across the three Maryland sites
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Table 1. Comparison of litter chemistry and kudzu litterfall from September through December, 2007 in invaded
and uninvaded sites; means are presented with standard errors in parentheses.
Site
Invasion status
C:N
N input (gm2)
Kudzu litterfall (gm2)
McKee.Beshers
McKee.Beshers
SERC
SERC
Summit.Hall
Summit.Hall
invaded
uninvaded
invaded
uninvaded
invaded
uninvaded
42.42 (1.48)
47.41 (1.50)
26.61 (2.24)
36.80 (0.60)
33.08 (1.95)
39.69 (2.68)
1.86 (0.38)
1.06 (0.34)
2.57 (0.87)
0.84 (0.13)
0.68 (0.15)
0.89 (0.29)
40.47 (4.55)
N/A
67.24 (25.89)
N/A
22.78 (5.48)
N/A
Fig. 2. Soil pools of inorganic nitrogen at three sites in Maryland, from April, 2006 through September, 2007.
Values are means 61 SE.
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HICKMAN AND LERDAU
Fig. 3. Net N mineralization (a) and net nitrification rates (b) at three sites in Maryland from April, 2006
through September, 2007. Values are means 61 SE.
Georgia and that are consistent with the expected
impacts associated with the invasion of a typical
fast-cycling species. While net nitrification was
higher in invaded soils in 2007, and NO3 pools
were larger in invaded soils in both years, the
effects were inconsistent. The different impacts in
Maryland and Georgia highlight the importance
of ecology, climate, and history in mediating the
impacts that invasive species can have on
ecosystem processes and the importance of
considering context when developing models of
invasive impacts. The inconsistent or delayed
v www.esajournals.org
impacts of kudzu invasion on biogeochemistry
contrast sharply with its impacts on community
ecology. While community composition is directly and immediately altered by kudzu invasion
(Hickman and Lerdau 2006), biogeochemical
processes may change only after a significant
time lag. The application of biogeochemical or
other models using parameterizations based on
community-ecosystem interactions at the heart of
kudzu’s range (or the center of any species’
range) should be applied with caution in other
sites, particularly where other factors may
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HICKMAN AND LERDAU
Fig. 4. Denitrification enzyme activity (a) and microbial biomass (b) at 3 sites in Maryland in 2006 and 2007.
Values are means 61 SE.
of kudzu invasion in Maryland. We compared N
cycling and pools in the uninvaded soils from
our Maryland sites to those from uninvaded sites
in Georgia. Net N mineralization, net nitrification, denitrification enzyme activity, and pool
sizes of inorganic N did not differ in uninvaded
soils in the two states (P ¼ 0.56, P ¼ 0.55, P ¼ 0.28,
and P ¼ 0.51, respectively) for measurements
taken six days apart in July and 10 days apart in
September, 2007. However, the long history of N
deposition in more northern states may make it a
modulate the ability of species or communities to
drive changes in ecosystem processes.
Rates of atmospheric N deposition in Maryland are slightly higher than in Georgia (Holland
et al. 2005). While it is possible that higher rates
of atmospheric N deposition common in the
northeastern U.S. may accelerate N cycling in
uninvaded soils and reduce or inhibit N fixation
rates in N-fixers by increasing N availability in
soils (Lucinski et al. 2002), this does not seem to
be a likely explanation for the lack of a in impact
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October 2013 v Volume 4(10) v Article 121
HICKMAN AND LERDAU
Fig. 5. Emissions of N2O (a) and NO (b) at two sites in Maryland in September, 2007. Values are means 61 SE.
more important factor mediating kudzu’s impact
further north.
The ecological context within which an invasion occurs can strongly affect the consequences
of the invasion. In the case of Maryland kudzu,
the more nutrient-rich soils in Maryland as
compared to Georgia may bias the system
towards responding less strongly in terms of Ncycling impacts (Paul and Clark 1996, Potash and
Phosphate Institute 2005). Similarly, the cooler
climate (which can inhibit N-fixation activity)
and shorter growing season of Maryland (which
reduces the annual duration of N-fixation activv www.esajournals.org
ity) can act in concert to minimize the magnitude
and extent of N-fixation that occurs in the kudzuinvaded sites (Lindemann and Ham 1979, Fyson
and Sprent 1982, Ryle et al. 1989, Peltzer et al.
2002, Robin et al. 2005, Houlton et al. 2008,
Bedison and Johnson 2009).
Finally, and perhaps most importantly, simply
by being closer to the invasion front, the
Maryland kudzu populations are likely not to
have been extant for as long, and any buffering
capacity (e.g., Magill et al. 2004, Perakis et al.
2005) of the soils is that much less likely to have
been exceeded. The combination of a cooler
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HICKMAN AND LERDAU
Fig. 6. Net N mineralization (left column) and net nitrification (right column) at each of the three sites in
Maryland from April, 2006 through September, 2007. Values are means 61 SE.
climate and shorter time since establishment may
mean that kudzu stands in Maryland are not as
dense as established stands in Georgia. Erickson
et al. (2001) demonstrated that increased rates of
N cycling in successional tropical forests were
positively correlated to the abundance of naturalized N-fixing lianas, and a similar dynamic
may explain some of the differences between
Maryland and Georgia as well as among sites in
Maryland. More generally, many belowground
v www.esajournals.org
processes have been shown to lag considerably
behind changes in plant community composition
(Wardle et al. 1999, Habekost et al. 2008,
Holtkamp et al. 2008, Hamman and Hawkes
2012). These lags between changes in community
composition and subsequent changes in ecosystems processes are not yet commonly incorporated into invasion models, and they represent an
important scientific frontier in the development
of such models.
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Biology 8:695–709.
Ashton, I. W., L. A. Hyatt, K. M. Howe, J. Gurevitch,
and M. T. Lerdau. 2005. Invasive species accelerate
decomposition and litter nitrogen loss in a mixed
deciduous forest. Ecological Applications 15:1263–
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Bedison, J. E., and A. H. Johnson. 2009. Controls on the
spatial patterns of carbon and nitrogen in Adirondack forest soils along a gradient of nitrogen
deposition. Soil Science Society of America Journal
73:2105–2117.
Compton, J. E., L. S. Watrud, L. A. Porteous, and S.
DeGrood. 2004. Response of soil microbial biomass
and community composition to chronic nitrogen
additions at Harvard forest. Forest Ecology and
Management 196:143–158.
Erickson, H., M. Keller, and E. A. Davidson. 2001.
Nitrogen oxide fluxes and nitrogen cycling during
postagricultural succession and forest fertilization
in the humid Tropics. Ecosystems 4:67–84.
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tropical rain forests influences soil N dynamics
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Hamman, S. T., and C. V. Hawkes. 2012. Biogeochemical and microbial legacies of non-native grasses
can affect restoration success. Restoration Ecology
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Haubensak, K. A., and I. M. Parker. 2004. Soil changes
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Hawkes, C. V., I. F. Wren, D. J. Herman, and M. K.
Firestone. 2005. Plant invasion alters nitrogen
cycling by modifying the soil nitrifying community.
Ecology Letters 8:976–985.
Hickman, J. E., K. M. Howe, I. W. Ashton, and M. T.
Lerdau. 2013. The native-invasive balance—implications for accelerated nutrient cycling in ecosystems. Oecologia doi: 10.1007/s00442-013-2607-x
Hickman, J. E., and M. T. Lerdau. 2006. Nitrogen
Although kudzu may not soon be the threat to
northeastern ecosystems and regional air quality
that it is in the southeastern U.S., it is impossible
to dismiss the possibility that its establishment in
the Northeast may be accompanied by future
changes in N cycling and trace gas fluxes. Leaf
litter from kudzu loses mass and N at higher rates
than litter from co-occurring species, setting the
stage for a transition from a slower- to a fastercycling ecosystem. The possible differences in N
transformations and trace gas emissions observed
at SERC in 2007 and the sporadic increases in
inorganic N pools in invaded soils at all sites may
be indicative of ecosystems beginning this transition. Further studies that can distinguish the
effects of time since invasion, stand density, and
climatic and chemical effects on nitrogen fixation
rates in kudzu will be important for better
predicting its impacts as it migrates north.
Over time, the frequency of ecosystem impacts
can be expected to increase as northeastern
winters grow milder and growing seasons
become longer, creating an environment more
suitable to kudzu establishment and N-fixing
activity. An increase of 2–68C by the year 2100
would raise winter temperatures in Maryland
above those currently experienced in Georgia,
where kudzu’s impact on N cycling is large and
consistent. Elevated CO2 concentrations may
enhance this effect, both by having a fertilizing
effect on kudzu growth and by depleting soil N,
giving kudzu a stronger competitive advantage
over non-N-fixers. Though the full impact of
kudzu on the ecosystems and atmosphere of
northeastern states may not be experienced for
years or decades after it invades, preventing its
establishment will be essential to avoiding these
potentially damaging impacts in the long term.
ACKNOWLEDGMENTS
We thank Peter Groffman, Sharon Hall, and Blandy
Experimental Farm for the use of facilities and
equipment. This research was supported by the
Garden Club of America and a National Science
Foundation Dissertation Improvement Grant.
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