Inventory and Ventilation Efficiency of Nonnative
and Native Phragmites australis (Common Reed) in Tidal
Wetlands of the Chesapeake Bay
Mirela G. Tulbure &Dana M. Ghioca-Robrecht &
Carol A. Johnston &Dennis F. Whigham
Received: 19 July 2011 / Revised: 5 June 2012 / Accepted: 14 June 2012
#Coastal and Estuarine Research Federation 2012
Abstract Nonnative Phragmites is among the most in-
vasive plants in the U.S. Atlantic coast tidal wetlands,
whereas the native Phragmites has declined. Native and
nonnative patches growing side by side provided an
ideal setting for studying mechanisms that enable non-
native Phragmites to be a successful invader. We con-
ducted an inventory followed by genetic analysis and
compared differences in growth patterns and ventilation
efficiency between adjacent native and nonnative Phrag-
mites stands. Genetic analysis of 212 patches revealed
that only 14 were native suggesting that very few native
Phragmites populations existed in the study area. Shoot
densit y decreas ed toward s the periphe ry of nativ e
patches, but not in nonnative patches. Ventilation effi-
ciency was 300 % higher per unit area for nonnative
than native Phragmites, likely resulting in increased
oxidation of the rhizosphere and invasive behavior of
nonnative Phragmites. Management of nonnative Phragmites
stands should include mechanisms that inhibit pressurized
ventilation of shoots.
Keywords Patch inventory .Intragenic physiological
differences .Intrapatch biomass allocation .Pressurized
ventilation .Ventilation efficiency .Invasive wetland plants .
Phragmites .Chesapeake Bay
Phragmites australis (Cav.) Trin. ex Steud. is a perennial
grass found on every continent with the exception of
Antarctica (Tucker 1990). Phragmites can grow in a variety
of freshwater and brackish wetlands, but it can also colonize
and expand in drier conditions (Global Invasive Species
Database; http://www.issg.org/). Paleological evidence sug-
gests that Phragmites is native to North America (Niering et
al. 1977; Orson 1999) but was historically a minor constit-
uent of the U.S. wetlands (Chambers et al. 1999). Molecular
studies conducted by Saltonstall (2002) have shown that there
are three distinct lineages of Phragmites currently occurring in
North America: the native subspecies (Saltonstall et al. 2004),
the lineage introduced from Eurasia (hereafter nonnative
Phragmites), and the Gulf Coast lineage (Lambertini et al.
2012; Saltonstall 2002,2003). In recent years, the nonnative
Phragmites has proliferated in brackish and tidal freshwater
wetlands on the Atlantic coast (McCormick et al. 2010),
whereas the native Phragmites has declined in the same region
(Saltonstall 2003; Vasquez et al. 2005).
The recent expansion of Phragmites into brackish tidal
wetlands on the US East Coast has been attributed to the
introduction of the nonnative lineage, but factors such as
disturbance (Bart and Hartman 2000,2003; Minchinton and
Bertness 2003) and anthropogenic modifications within
wetlands (Johnston et al. 2008; Maheu-Giroux and de Blois
2007; McNabb and Batterson 1991) or on adjacent upland
areas (King et al. 2007; Minchinton and Bertness 2003;
M. G. Tulbure :D. M. Ghioca-Robrecht :C. A. Johnston
Department of Biology and Microbiology, South Dakota State
Brookings, SD 57007, USA
D. F. Whigham
Smithsonian Environmental Research Center,
Edgewater, MD 21037, USA
M. G. Tulbure (*)
Australian Wetlands, Rivers and Landscapes Centre,
School of Biological, Earth and Environmental Sciences,
University of New South Wales,
Sydney NSW 2052, Australia
Estuaries and Coasts
Tulbure 2008; Tulbure and Johnston 2010) facilitate Phrag-
mites invasion. Once established, nonnative Phragmites forms
large stands, with shoots up to 3–4 m tall. Nonnative Phrag-
mites has high biomass (Meyerson et al. 2000), displaces native
vegetation, and changes ecosystem processes (Chambers et al.
1999; Ehrenfeld 2003).
Situations where patches of native and nonnative Phrag-
mites grow side by side in the field represent a unique oppor-
tunity to study intraspecific differences because comparative
studies can provide important information on the invasive
behavior of introduced populations (Daehler and Strong
1996; Seliskar and Gallagher 2000; Seliskar et al. 2002).
Despite the potential benefits of understanding mechanisms
that impart invasiveness in Phragmites when conducting
studies comparing native and nonnative Phragmites, to our
knowledge, only a limited number of studies have been con-
ducted in the U.S.A., of which the majority were greenhouse
studies. These studies showed that nonnative Phragmites
emerges from rhizomes earlier in the season, grows taller,
and has greater biomass (Holdredge et al. 2010; League et
al. 2006; Meadows and Saltonstall 2007; Mozdzer et al.
2010), can tolerate higher salinity levels (Vasquez et al.
2005), and has higher rates of photosynthesis than native
Phragmites (Mozdzer and Zieman 2010).
We briefly outline the a priori theoretical and empirical
support for each of our goals and hypotheses which were to:
1. Identify native and nonnative Phragmites stands growing
side by side in the field: Finding stands of native and
nonnative Phragmites growing in close proximity was
not a trivial task as there are apparently few tidal wetlands
on the Mid-Atlantic Coast where native Phragmites occurs
(Saltonstall 2003; Vasquez et al. 2005). Because one of our
goals was to compare native and nonnative Phragmites
that occurred in the same wetlands, the first objective of
our study was to conduct a geographic survey and genetic
analysis of Phragmites in Chesapeake Bay to locate and
identify adjacent native and nonnative Phragmites stands.
2. Compare native and nonnative Phragmites patches that
were growing close to each other, a priori hypothesizing
(a) Nonnative Phragmites displays greater clonal growth
(i.e., produces more stems and biomass per unit area)
towards the edge of the clones: Phragmites can repro-
duce both sexually and vegetatively. Although the
ability to reproduce sexually increases the potential
for colonizing new sites, the shift in resource alloca-
tion towards clonal growth facilitates the establish-
ment and survival of populations (Sakai et al. 2001).
Plant species with clonal growth often exhibit greater
growth at the edge of patches (Lambrecht-McDowell
and Radosevich 2005; Parker 2000; Wikberg and
Svensson 2003), and rapid shoot initiation allows
ruderal species to spread (Grime 1977). Previous stud-
ies showed that nonnative Phragmites grows in denser
stands than does native Phragmites (Meadows and
Saltonstall 2007), but there have not been any studies
in which the shoot density between native and nonna-
tive stands has been compared at the leading edge of
the expansion of patches (i.e., density at the edge of a
patch versus density toward the center of the patch).
(b) Nonnative Phragmites has greater ventilation effi-
ciency per unit area than native Phragmites: The
mechanisms of internal pressurization and convec-
tive gas flow are important adaptations of wetland
plants to growth in anoxic substrates (Brix et al.
1992; Cronk and Fennessy 2001). Pressurized venti-
lation represents a bulk flow of oxygen and requires a
pressure gradient between two ends of a pathway
with an exit to the atmosphere (Colmer 2003). In
Phragmites, oxygen enters via the leaf sheath stoma-
ta of green stems, flows to the roots along the inter-
cellular spaces of the green shoots, and flows back
to the atmosphere via senesced culms (Armstrong
and Armstrong 1991; Colmer 2003; Rolletschek et
al. 1999). Therefore, high densities of pressurizing
living and dead culms play an important role in
delivering oxygen to belowground organs as well as
removing gases (e.g., carbon dioxide) associated with
belowground respiration. The convective flow-
through mechanism has been described for several
wetland species (Armstrong and Armstrong 1991;
Brix et al. 1992) and lower per stand ventilation
efficiency has been observed in declining Phragmites
stands in Europe (Ostendorp 1989). One factor be-
hind the recent expansion of nonnative Phragmites in
brackish tidal wetlands in the U.S.A. may be its
ability to more efficiently transport oxygen to roots.
The ability to efficiently deliver oxygen to roots
could be especially important in coastal wetlands that
are enriched by eutrophication and could result in a
decline in the native lineage for reasons similar to
those that have been responsible for the decline of
Phragmites in Europe—as the substrate becomes
more reduced due to eutrophication, Phragmites is
unable to supply enough oxygen to the rhizosphere
(van der Putten 1997).
Native and Nonnative Phragmites Survey and Study Site
A field survey of 212 Phragmites stands was conducted in
eastern Maryland U.S.A. (Fig. 1) during summer 2006. Leaf
samples were collected from the 212 Phragmites patches and
Estuaries and Coasts
identified as native or nonnative lineage using the genetic
analysis described in Tulbure et al. (2007) that was based on
Saltonstall’s (2002) protocol. The survey targeted suspected
locations of native Phragmites and was not intended to be
random or otherwise representative of the area.
We selected three pairs of native and introduced stands
identified during the survey that were located along King’s
Creek in Talbot County, Maryland (Fig. 1), northeast of the
town of Easton near the Nature Conservancy’s King’s Creek
Preserve site (The Nature Conservancy; www.nature.org).
The site is a tidal freshwater wetland that drains into the
Choptank River, a subestuary of Chesapeake Bay. The pairs
of stands selected were within meters of each other and
close to the creek, with no standing water present but wa-
terlogged soils. A previous study at the wetland showed that
there were no differences in porewater ammonium and
phosphate, the primary limiting nutrients to Phragmites,
between native and nonnative stands (Mozdzer and Zieman
2010). Therefore, we assume that any differences between
native and nonnative Phragmites would be due to genetic
Clonal Study and Pressurized Ventilation
A north–south transect was placed across each of the six
patches, and the transects were divided into three zones of
equal length. The zones are hereafter referred to as center,
intermediary, and edge. In August 2006, we harvested all
aboveground biomass in three 0.25-m
quadrats in each zone.
Biomass from each quadrat was divided into living (green)
and senesced (brown) shoots and then oven dried at 60 °C for
48 h. Gas flow parameters were measured on randomly cho-
sen stems (18 per lineage) in each stand following the meth-
odology described in Rolletschek et al. (1999). Pressurization
of the lacunal air in the shoots was measured with a digital
manometer (HM35, Revue Thommen AG, Switzerland) and
gas flow rate was measured with a flow meter (Gilmond
Instruments, Inc., USA). The static pressure differential of
the living culm (Pculm) and the cutoff at the base, the stubble
(Pstubble), was measured with a gas connection directly to the
manometer. The dynamic pressure differential (Pd) and the
gas flow rate (Fd) were measured with the culm connected to
the stubble with the manometer in parallel and the flow meter
in series (Rolletschek et al. 1999). Ventilation efficiency
(sensu Rolletschek et al. 1999) was determined as the effective
ventilation per unit area. The effective ventilation parameter,
Fd/(Pd−Pstubble) represents the flow rate (Fd) standardized
by the effective pressure differential (Pd−Pstubble). Shoot
height, circumference at the base of the stem, and number of
leaves per shoot were also recorded for the same stems used
in the ventilation study.
Biomass, density, and ventilation efficiency data were
analyzed using Generalized Linear Mixed-Effects Models
to examine how lineage (native or nonnative Phragmites)
and location within a patch (edge, intermediary, or center)
affect total stem density as well as new and old culm density,
biomass, and ventilation efficiency. Lineage was treated as a
fixed effect, while stand was treated as a random effect
nested in lineage. When testing several a priori working
hypotheses, AIC is the method of choice over null hypoth-
esis testing (Anderson et al. 2001). We used an information
theoretic approach based on the second-order Akaike’s In-
formation Criterion corrected for small sample size, AICc
(Burnham and Anderson 2002). Models were run using the
glmer function in the lme4 package in the software R (R
Development Core Team 2008).
Survey of Native and Nonnative Phragmites
PCR/RFLP genetic analysis of leaf samples revealed that only
14 Phragmites stands out of the 212 Chesapeake Bay stands
sampled were native. None of the samples collected from the
Fig. 1 Location of Phragmites stands sampled around Chesapeake
Bay. The three insets represent the areas where we identified native
Estuaries and Coasts
western shore of Chesapeake Bay (167) were native patches
(Fig. 1). Eleven native and 20 nonnative patches were
identified at the King’s Creek site and, as already described,
native and nonnative patches growing side by side were
identified. The other three native stands were from Tuckahoe
Creek (two stands) and Wicomico Creek (one stand). All
native patches identified as part of this study were located
on the eastern shore of Chesapeake Bay (Fig. 1).
Clonal Study and Pressurized Ventilation
The mean diameter of the nonnative stands was 30 % greater,
but the difference was not significant (Table 1). Shoot
circumference was 15 % greater for nonnative Phragmites,
the number of green leaves was 37 % greater, and the shoot
length was 16 % higher for nonnative than native Phragmites
(Table 1). Mean aboveground biomass was substantially
greater for nonnative than native Phragmites (Table 2), and
the difference was significant (F069.12, df 01, p-value0
0.01). Biomass per unit area decreased by 45 % from the
center towards the edge in patches of the native lineage and
differences between the three zones were significant (one-way
ANOVA F02.41, p-value00.1, df02; Table 2). There were
no significant biomass differences among zones within stands
of the nonnative lineage. The nonnative Phragmites always
had significantly greater biomass in each of the three
zones compared to the native lineage, and stem density was
significantly greater for the nonnative lineage (F09.75,
df 01, p-value 00.03) within each of the three zones
(Table 2). Nonnative Phragmites had almost twice as many
green stems as the native lineage (F06.16, df01, p-value0
0.06; Table 2). The standing dead density of stems was
appro ximately four times greater for the nonnative
lineage compared to the native Phragmites (F014.01,
df 01, p-value 00.02; Table 2). Information theoretic
model selection based on AICc revealed strong support
from the data for the influence of lineage (i.e., whether
Phragmites patches were native or nonnative) on biomass,
total stem density, new and old stem density, and ventilation
efficiency (Table 3). Ventilation efficiency was 300 % higher
for nonnative than native Phragmites (nonnative Phragmites,
1.85±0.5 mL min
; native Phragmites, 0.44 ±
0.4 mL min
), whereas effective ventilation of
single stems was approximately 200 % for nonnative than
native Phragmites (nonnative Phragmites, 0.016±0.004 mL/
; native Phragmites, 0.007± 0.004 mL/min Pa
This study advances scientific knowledge about Phragmites
in several ways. This is the first study showing differences
in ventilation efficiency between native and nonnative
Phragmites. Also, we inventoried the lineage of Phragmites
stands on both shores of Chesapeake Bay, expanding upon
earlier work characterizing the eastern shore (Meadows
and Saltonstall 2007 ). Finally, our Phragmites stand
characterization is novel in comparing the allocation of stem
density and biomass in native versus introduced Phragmites
Once established, Phragmites can change environmental
conditions to create more favorable conditions for growth and
reproduction (Rudrappa et al. 2007). We found that nonnative
Phragmites had greater ventilation efficiency per unit area
than native stands. This was likely created by the fact that
introduced Phragmites had higher pressurized gas flow rates,
denser growth pattern, and greater number of old culms which
act as efflux culms. The flow rates measured were at the lower
range of values measu red for P hragmites i n Europe
(Rolletschek et al. 1999). Results of the pressurized ventilation
study demonstrated that nonnative Phragmites had the
potentialto oxidize the substrate more than native Phragmites.
While not measured in the field, one consequence of the
higher ventilation rates would be more efficient oxidation of
the substrate and a less reduced substrate in stands of
nonnative Phragmites, which in the long run would improve
The convective flow-through pressurized ventilation
mechanism has been described for several wetland species
(Armstrong and Armstrong 1991), and Phragmites was
shown to have the highest flow rate when compared to 13
other wetland plants (Brix et al. 1992). This mechanism may
offer a competitive advantage over species relying exclusively
on diffusive gas transport (Brix et al. 1992). Higher
Table 1 Characteristics of
nonnative and native Phragmites
stands at King's Creek (MD)
measured in August 2006
(mean ± SE)
Nonnative Native F statistic df p-value Sample
Shoot length (cm) 300.58 ± 15.13 260.12 ± 14.52 3.72 1 0.12 18
Shoot circumference (cm) 2.71±0.11 2.30±0.11 6.31 1 0.06 18
Number of green leaves
13.50± 1.43 8.48± 1.42 6.19 1 0.06 18
Diameter (m) of native
and nonnative stands
32.67± 8.83 23.13± 4.23 0.95 1 0.38 3
Estuaries and Coasts
ventilation efficiency can also benefit the nonnative
Phragmites by oxidizing potentially toxic compounds
in the rhizosphere (Armstrong and Armstrong 1991). Efficient
ventilation would oxidize sulfides, allowing Phragmites to
grow in brackish wetlands with higher sulfide concentrations
(Cronk and Fennessy 2001). Although nonnative Phragmites
can tolerate higher salinity levels than native Phragmites
(Vasquez et al. 2005), it cannot tolerate high sulfide
concentrations (Bart and Hartman 2003; Chambers et al.
1998; Wijte and Gallagher 1996). By supplying oxygen to
nitrifying bacteria, the nitrification of ammonium is
increased (Armstrong and Armstrong 1991), which could
benefit the plant, nitrate being mentioned as a primary cause
for increased introduced Phragmites abundance (Marks et al.
1994). Future studies should collect soil redox data and relate
them with ventilation efficiency and stand characteristics.
Our survey of Chesapeake Bay Phragmites stands revealed
that surprisingly few stands, all located on the eastern shore,
were of the native lineage (Fig. 1). Meadows and Saltonstall
(2007) reported that native Phragmites was much more
common on the Maryland eastern shore than in Delaware or
southern New Jersey, but they did not search for stands along
the western shore of Chesapeake Bay. Although subsequent
work by co-author Whigham and colleagues had identified a
stand of native Phragmites along Parker’s Creek on the
western shore of Chesapeake Bay, it was in an area with very
little shoreline or upland development, atypical of the western
shore. Upland development and disturbance in wetlands have
been reported as factors contributing to the spread of nonnative
Phragmites (Bertness et al. 2002; King et al. 2007; Meadows
and Saltonstall 2007; Minchinton and Bertness 2003), often at
the expense of the native subspecies (Saltonstall 2003). We
cannot attribute causality to the low proportion of native
stands, but it is clear that the introduced lineage is far more
prevalent than the native lineage around Chesapeake Bay. The
rapid expansion of the nonnative Phragmites (McCormick et
al. 2010) potentially could result in the complete elimination
of the native haplotype when they co-occur.
Table 2 Differences in above ground biomass and stem density within the three zones of a stand (center, intermediary, and edge) for nonnative and
Center Intermediary Edge Per stand Center Intermediary Edge Per stand
Biomass (mean ± SE)
as dry weight (g m
2,410.4± 69.7 2,868.8 ± 106.0 2,667.5 ±72.6 2,649±80.0 974.6 ± 45.0 708.0 ± 38.4 545.5± 26.1 742.7 ± 35.4
Density of new culms
(# stems m
96.9± 21.2 72.4 ± 10.2 83.6±10.7 84.3± 8.5 48.4 ± 6.5 37.3± 6 49.3± 12.5 45 ± 5
Density of old culms
(# stems m
31.6± 4.9 56.0± 14.7 37.3± 10.0 41.6 ± 6.3 9.3± 3.0 10.7± 2.2 8.0± 3.0 9.3± 1.6
Total stem density
(# stems m
128.4± 14.8 128.0±15.3 120.9± 16.3 126.0±31.3 57.8± 11.6 48.0±11.2 57.3± 9.0 54.4 ±20.2
Table 3 AICc-based model
selection for (1) total stem
density, (2) new culm density, (3)
old culm density, (4) biomass, and
(5) ventilation efficiency.
Generalized Linear Mixed-Effect
Models used site as a random
factor and included Lineage (Lin)
and Location within stand (L) as
fixed factors. We show the
number of predictor variables (K),
AICc differences (Δ) and Akaike
Model rank Model KAICc ∆ώ
Total stem density (# stems m
) Lin + L 3 624.1 32.0 0.001
Lin 2 592.1 0.0 0.999
L 2 606.1 14.0 0.009
New culms (# new stems m
) Lin + L 3 624.1 32.0 0.001
Lin 2 592.1 0.0 0.999
L 2 606.1 14.0 0.009
Old culms (# old stems m
) Lin + L 3 575.2 29.3 0.004
N 2 545.9 0.0 0.996
L 2 557.2 11.3 0.003
Biomass Lin + L 3 962.8 32.6 0.008
Lin 2 930.2 0.0 0.999
L 2 944.8 14.6 0.006
Ventilation Efficiency (per m
) Lin + L 3 823.5 27.9 0.008
Lin 2 795.6 0.0 0.992
L 2 805.5 9.9 0.007
Estuaries and Coasts
The growth of the native and introduced stands within
meters of one another at King’s Creek made this site the ideal
setting for our study because edaphic conditions were similar,
therefore any differences observed could be attributed to
differences in lineage. Even though sampling nonnative and
native Phragmites pairs at different locations would have been
desirable, we could not locate other native and nonnative
Phragmites growing side by side at other sites besides King’s
Creek. As expected, nonnative Phragmites had greater
biomass and stem density per unit area than the native
Phragmites, similar to the findings of previous studies
(League et al. 2006; Meadows and Saltonstall 2007; Mozdzer
and Zieman 2010; Vasquez et al. 2005), which increase the
competitiveness and the ability of the nonnative Phragmites to
compete for resources such as light and space.
Rapid vegetative growth is one of the qualities of successful
weeds (Baker 1974; Sakai et al. 2001), allowing them to
maintain vigorous growth in their current habitat (Eriksson
1994). A greater growth rate towards the periphery of patches
has been shown to be inversely related to the time of stand
recruitment and clone density (Hartnett and Bazzaz 1985;
Parker 2000). We predicted that the stands of nonnative
Phragmites would exhibit greater clonal vigor (number of
stems and biomass) towards the edge of the clones. We
observed that biomass decreased toward the periphery of
native stands but not stands of the nonnative lineage, nor did
stem density per unit area change with increasing distance
from the center of stands (Table 2). However, Phragmites
stands sampled here have been established at King’s Creek
for several decades, very likely during the 1980s (Rice et
al. 2000), and lack of vigor could be related to patch age. To
further test our prediction that introduced stands would have
greater clonal vigor with increasing distance from the center of
the stand, future studies would either have to compare the
clonal growth in stands of Phragmites of different ages or use
newly established stands and measure parameters of clonal
vigor during several years immediately after establishment.
Studies documenting differences between native and
nonnative Phragmites are essential for a sound management
of Phragmites. This study explored one aspect of Phragmites
invasion, namely mechanisms employed by Phragmites to
sustain its invasion.
Once established, Phragmites is difficult to control as it
displaces native vegetation and changes wetland properties.
This study is the first one to show that nonnative Phragmites
has a higher ability to send oxygen to the rhizosphere than
native Phragmites, a physiological attribute that clearly bene-
fits nonnative Phragmites and provides a partial explanation
for its success. While testing with an experimental approach
should be conducted, our results suggest that once established,
along with other management practices (e.g., herbicide treat-
ment), measures targeted at inhibiting the pressurized ventila-
tion mechanism, such as completely removing the culms
which act as influx/efflux culms, followed by flooding for a
long period of time can reduce Phragmites success.
Acknowledgments We thank Dr. Doug Samson from The Nature Con-
servancy for providing information about the King’s Creek Preserve, Drs.
Joydeep Bhattacharjee and Neil Reese for help with choosing the instru-
ments, Jay O’Neill for lab assistance, Dr. Kristin Saltonstall and Robert
Meadows for suggestions regarding native stand locations in Maryland,
Elaine Friebele for permission to sample Jug Bay wetlands, and Ned Gerber
for allowing us to use his farm during the field season. Funding came
through the Joseph F. Nelson scholarship to MGT. We thank the editors and
two anonymous reviewers for helpful comments on an earlier draft.
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Estuaries and Coasts