Exotic shrub invasion in an undisturbed wetland has little community-level effect over a 15-year period

Biol Invasions (2009) 11:1803–1820
DOI 10.1007/s10530-008-9359-2


Exotic shrub invasion in an undisturbed wetland has little
community-level effect over a 15-year period
Jason E. Mills Æ James A. Reinartz Æ
Gretchen A. Meyer Æ Erica B. Young

Received: 8 July 2008 / Accepted: 24 September 2008 / Published online: 7 October 2008
Ó Springer Science+Business Media B.V. 2008

Abstract In this long-term study, we examined the                 Keywords Invasive shrub  Forested wetland 
invasion by the exotic shrub glossy buckthorn                     Plant community  Long-term study 
(Rhamnus frangula L.) and the response of co-                     Rhamnus frangula L.  Glossy buckthorn
occurring plants in a large, undisturbed wetland. We
first sampled the vegetation in 1991 and repeated the
sample 15 years later using the same, permanently
located sample units (n = 165). Despite dramatic
increases in the abundance of buckthorn, the invasion             Introduction
elicited little apparent response by the resident plant
community. Species richness and cover in the herba-               The increasing number of invasions and the
ceous plant stratum had no apparent relationship with             magnitude of ecological change attributed to plant
change in buckthorn cover. The number of shrub                    invasions have prompted numerous researchers to
species other than buckthorn showed no relationship               regard invasive species as agents of global change
with change in buckthorn cover, but the cover of                  (Vitousek et al. 1997a; Mack et al. 2000; Ricciardi
other shrubs decreased as buckthorn cover increased.              2007). Plant invasions can alter communities and
Species composition changed independently of                      ecosystems through a variety of pathways, and these
changes in buckthorn cover. These results show that               include competing directly with natives for resources
dramatic increases in the abundance of an invasive                (D’Antonio and Mahall 1991) or modifying nutrient
species do not necessarily cause large changes in the             cycles or fire regimes (D’Antonio and Vitousek 1992;
native plant community and suggest disturbance                    Vitousek and Walker 1989; Ashton et al. 2005). Plant
history influences community response to invasion.                invasions clearly change some communities, whereas
                                                                  others accommodate new species while exhibiting
                                                                  little response (Stolhgren 2006). Predicting commu-
                                                                  nity responses to invasion remains a challenge, even
J. E. Mills (&)  E. B. Young
                                                                  for different sites invaded by the same invading
Department of Biological Sciences, University of
Wisconsin-Milwaukee, P.O. Box 413, Milwaukee,                     species (Rejmánek et al. 2005), and our inability to
WI 53201, USA                                                     predict the effects of invasions reflects a lack of a
e-mail: mills@uwm.edu                                             detailed understanding of the conditions that deter-
                                                                  mine how communities react to invasions.
J. A. Reinartz  G. A. Meyer
Field Station, University of Wisconsin-Milwaukee, 3095                Much of what we currently know about plant
Blue Goose Road, Saukville, WI 53080, USA                         invasions comes from studies in ecosystems or

1804                                                                                                  J. E. Mills et al.

communities also affected by anthropogenic distur-          invasions requires longer term studies using a broad
bances. In part, this reflects the difficulty of locating   range of invaders in a wide variety of habitat types.
undisturbed study sites in an increasingly human-              In contrast with the many short-term studies that
dominated landscape (Foley et al. 2005). Since              focus on terrestrial plant invasion in disturbed
invasions are usually studied after the invader has         habitats, this study examines the longer-term spread
established and spread (Parker et al. 1999) and             and effects of an invasive shrub within a large,
anthropogenic disturbance frequently facilitates plant      undisturbed wetland. We carried out an extensive
invasion (Mack et al. 2000), most invasion studies          sample of the vegetation in the early stages of
have involved disturbed systems. Changes caused by          R. frangula (hereafter buckthorn) invasion and
disturbance often cannot be easily separated from the       repeated the sample 15 years later using the same,
effects of an invasion and may confound studies of          permanently located sample units. This allowed us to
plant invasion. Due in part to such factors, Knight         characterize the buckthorn invasion by examining
et al. (2007), for example, could not definitively link     changes in adult shrub cover between sample dates
common buckthorn (Rhamnus cathartica L.) inva-              and comparing the contemporary seedling population
sions to declines among understory plant species,           of buckthorn to those of other woody plant species.
even though the shrub is an aggressive invader.             To assess the community response to invasion, we
Although invasive species are often perceived as            explored: (1) how individual taxa in the herbaceous
causes of community degradation, in some cases they         plant and shrub strata responded to changes in
could simply be passengers of change along with the         buckthorn abundance and (2) how species richness
native species (MacDougall and Turkington 2005). A          and cover in the herbaceous plant and shrub strata
better understanding of the influence of disturbance        responded to changes in buckthorn abundance.
history on the community-level responses to invasion        Although species richness and native cover are
would enhance our ability to predict the conse-             criteria commonly used to assess the effects of plant
quences of invasions (Levine et al. 2003).                  invasions (Parker et al. 1999), they may ignore
   The effects of plant invasions may also frequently       relationships among species in the community. To
defy prediction because studies of relatively few           address this, we also employed multivariate tech-
habitat types and plant functional groups inform our        niques to assess (3) how buckthorn invasion status
understanding of how communities respond to inva-           affected species composition.
sions. Most of the studies used to develop and test
theories of plant invasion have been conducted in
grassland habitats (Pyšek et al. 2006), usually with       Methods
short-term experiments (e.g., Tilman 1997; Davis and
Pelsor 2001; Kennedy et al. 2002; Emery and Gross           The Cedarburg Bog is located in Ozaukee County,
2007; Mwangi et al. 2007). Invasions in wetland             Wisconsin, *40 km north of Milwaukee (43°23.20 N,
habitats remain relatively understudied. Of the few         88°0.630 W). At 1,000 ha, it is one of the largest intact
published plant invasion studies in wetlands, most          wetlands in southeastern Wisconsin and remains
focus on herbaceous plant species that invade emer-         relatively undisturbed because of a long history of
gent aquatic plant communities (e.g., Galatowitsch          protection. Canopy trees were harvested from some
et al. 1999; Maurer and Zedler 2002; Kercher and            parts of the wetland during winters in the early 20th
Zedler 2004). Shrub invasions in wetlands, in               Century, but the wetland has been mostly state-owned
contrast, have received less interest, even though          since the mid-20th C. and currently receives few
the same species that invade wetlands can negatively        public visitors. Forest dominated by Larix laricina
affect plant communities on drier sites. As an              (Du Roi) K.Koch and Thuja occidentalis L. covers the
example, the Eurasian shrub glossy buckthorn                majority of the wetland. Grittinger (1970) surveyed
(Rhamnus frangula L.) invades upland deciduous              the wetland in the late 1960s and established that it
forests (Frappier et al. 2003; Fagan and Peart 2004),       included the southernmost example of string bog in
as well as wetlands (Houlahan and Findlay 2004).            North America. This typically northern, patterned
Improving our ability to predict the effects of             vegetation type includes ‘‘strings’’ of stunted trees

Exotic shrub invasion in an undisturbed wetland                                                                      1805

(L. laricina and T. occidentalis) and ericaceous
shrubs that alternate with swales dominated by low-
growing herbaceous plants, especially Carex spp.
Carnivorous plants (Drosera spp. and Sarracenia
purpurea L.) are common in the wetland, particularly
in the string bog, and their presence indicates low
nutrient availability (Bott et al. 2008). Sphagnum spp.
are widespread, but the wetland lacks the acid
conditions that normally accompany Sphagnum spp.
growth and peat formation. Groundwater flows into
the wetland through glacial till dominated by lime-
stone, resulting in surface water with neutral pH
(Reinartz 1985; Bott et al. 2008). Although most of
Cedarburg Bog is forested, the vegetation also
includes shrub thickets, wet meadow, shallow marsh,
and emergent aquatic plants. Abundant shrub species
include Ilex verticillata (L.) A.Gray, Cornus stolonif-
era Michx. and Toxicodendron vernix (L.) Kuntze. Of
the 407 plant species that we have recorded during this
and other studies, only 21 species in Cedarburg Bog         Fig. 1 Changes in abundance and spatial distribution of glossy
are exotic based on the Wisconsin State Herbarium           buckthorn in the Cedarburg Bog between 1991 and 2006
vascular plant database (WISFLORA 2008). Of these
exotics, only one species, Rhamnus frangula, cur-           circular quadrats, we recorded data on species,
rently exhibits invasive behavior in the Cedarburg          condition (alive or dead standing), and diameter at
Bog. This Eurasian shrub produces bird-dispersed            breast height (DBH) of all tree species stems with at
seed in fleshy fruits, and Pohl (1943) first reported its   least 2.5 cm DBH. A 10 m shrub-intercept sample
presence in Wisconsin. Based on maximum stem ages           line was centered in the 11.3 m diameter, large
estimated from annual growth rings (Reinartz and            circular quadrat and oriented in a cardinal east–west
Kline 1988), it had arrived in the Cedarburg Bog by         direction. We recorded the aerial intercept of each
1955.                                                       species of shrub and woody vine along this 10 m line
   Two quantitative descriptions of the vegetation of       to provide an estimate of plant cover in the shrub
the Cedarburg Bog, completed in 1991 and 2006,              stratum. To record the presence, abundance, and
used identical methods. We established 165 sampling         density of tree and shrub seedlings and to estimate the
units at regular intervals of 100 m (center to center)      cover of plants growing in the herbaceous plant
along 10 east–west transects across the wetland             stratum, we placed square 1 m2 quadrats along the
(Fig. 1). The transects were located 20 m north of          eastern and western boundaries of the 100 m2 circular
each quarter section line that crosses the wetland.         quadrats at each end of the east–west line through
This transect placement enabled the use of surveyed         each sampling unit. Only tree species seedlings were
property boundaries as references for relocation, but       counted in 1991, whereas both shrub and tree species
also avoided the disturbance or changes in distur-          seedlings were counted in 2006. Cover of each
bance history sometimes associated with property            herbaceous plant species was estimated visually using
boundaries along section lines. Transect lines were         the following scale: 0 = absent, 1 = 0–5% cover,
initially established in 1991 using a compass, and          2 = 5–25%, 3 = 26–50%, 4 = 51–75%, and 5 =
sample unit spacing was set using a string distance         76–100% cover. We sampled the herbaceous vege-
measurer. In 2006, a mapping-grade global position-         tation twice in each sample year in order to identify
ing system (GPS) was used to record the UTM                 and record the cover of dominant herbaceous species
coordinates of each sampling unit center.                   in the early and late parts of the growing season.
   A 100 m2 circular quadrat (11.3 m diameter)              Vegetation sampling was conducted between 13 May
defines each sampling unit. Within these 100 m2             and 15 August in 1991, and 24 May and 9 August in

1806                                                                                               J. E. Mills et al.

2006. All plants were identified to species level,         matrix containing pair-wise dissimilarity values
except for Viola spp.                                      (Bray–Curtis index) among all sampling units (both
   Cover of shrubs was estimated once at each sample       years, n = 330) based on the presence/absence of 135
unit during each sampling year, but plant cover in the     of the most abundant herb and shrub taxa, excluding
herbaceous plant stratum at each sampling unit was         buckthorn. Since rare species can account for little
estimated twice each sampling year. To make these          compositional variation among sampling units, herb
datasets equivalently structured, we used the maxi-        and shrub species that occurred in five or fewer
mum cover value recorded for each species in the           sampling units across both sample years were
herbaceous plant stratum, whether early or late in the     excluded from this analysis. The dissimilarity matrix
sampling season, as the single cover value for that        was used for principal coordinates analysis (PCO)
species in the quadrat. The cover classes were             with the R package ‘‘labdsv’’ (Roberts 2006), which
converted to their midpoint percent cover (i.e., 2.5,      follows the method developed by Gower (1966). PCO
15, 38, 66, and 88%). Since different observers            is like principal components analysis (PCA), but PCO
visually estimated herb cover in 1991 and 2006, we         is non-Euclidean and works more effectively with
divided the percent cover values for each species by       data that include many species absences (Legendre
total plant cover in each herb quadrat to reduce           and Legendre 1998). To assess the effects of changes
observer bias. We then calculated the mean percent         in buckthorn abundance on changes in species
cover for each species in the two quadrats in each         composition, we defined three invasion status groups
sampling unit and used this as the single representation   (buckthorn increased, decreased and absent) and
of cover in the herbaceous plant stratum.                  calculated group vector sums using sample unit
   The species list used for all regressions and group     scores from the first two axes of the ordination. In
comparisons included 171 species from the herba-           order to determine if the directions of observed vector
ceous plant stratum and 40 species in the shrub            sums differed significantly among groups, we ran-
stratum (Appendix A). All analyses were performed          domly assigned sampling units to one of the three
in the statistical computing environment R (version        invasion status groups. For each run (n = 1,000), we
2.4.1; R Core Development Team 2006). We                   collected data on the angles between group vector
assessed the effects of buckthorn invasion on species      sums (only those less than 180°). We estimated the
richness and plant cover using linear regression.          probability of obtaining the observed angles between
Change in the percent cover of buckthorn in a sample       vector sums using the null distributions generated
unit (e.g., 80% in 2006 minus 20% in 1991 equaled          through repeated random group assignment.
?60%) was log-transformed prior to use as the
independent variable. The response variables
included changes in sample unit species richness in        Results
the herbaceous plant and shrub strata, excluding
buckthorn, and changes in total percent cover in the       The cover and frequency of buckthorn in the shrub
herb and shrub strata, excluding buckthorn. We also        stratum increased dramatically between 1991 and
used linear regression to examine the relationships        2006. In 1991, adult buckthorn occurred in 45% of
between changes in the percent cover of individual         the sample units, but frequency increased to 73% by
species and change in log-transformed percent cover        2006 (Fig. 1). Many of the 49 sample units that
of buckthorn. Sample units that did not contain            gained buckthorn between sample dates were located
buckthorn in either 1991 or 2006 were excluded from        near the margins or in the northern third of the
regressions. To assess the significance of differences     wetland, and colonization of these areas represented
between those sample units that contained buckthorn        an increase in the spatial distribution of buckthorn
and those that did not, we used t-tests, Mann–             within the Cedarburg Bog. By comparison, the shrub
Whitney tests, or Wilcoxon signed-rank tests,              species with the next highest increases in net
depending on the normality of the data.                    frequency, natives Alnus incana (L.) Moench subsp.
   To assess the effects of buckthorn invasion on          rugosa (Du Roi) R.T.Clausen and Ribes lacustre
changes in species composition, we used the R              (Pers.) Poir., gained only 11 and 4 sample units,
package ‘‘vegan’’ (Oksanen et al. 2007) to generate a      respectively. The native woody vine Parthenocissus

Exotic shrub invasion in an undisturbed wetland                                                                       1807

quinquefolia (L.) Planch. occurred in 21 sample units
more than it did in 1991. The non-native plant with
the second highest net gain in frequency was the
herbaceous plant Rumex crispus L. This species
occurred in 12 more sample units in 2006 than it did
in 1991, but its 2006 frequency remained relatively
low (13% of sample units).
    Between 1991 and 2006, buckthorn cover
decreased in 20 sample units (dropping to zero in 6
sample units) but cover increased in 104 sample
units. Total buckthorn cover increased 127% between
sample dates, and the net gain in cover by buckthorn
is over eight times that of the shrub species with next     Fig. 2 Total seedling counts in 2006 for all 165 sample units
highest net gain in cover, the ericaceous native            for ten tree or shrub species with highest counts (rank order):
Chamaedaphne calyculata (L.) Moench var. angust-            Rhamnus frangula (Rf), Thuja occidentalis (To), Cham-
                                                            aedaphne calyculata (Cc), Ilex verticillata (Iv), Betula
ifolia (Aiton) Rehder. In those sample units                pumila (Bp), Toxicodendron vernix (Tv), Cornus stolonifera
containing buckthorn in 1991, mean cover increased          (Cs), Larix laricina (Ll), Rosa palustrus (Rp), Rhamnus
by 46%. Buckthorn accounted for 11% of total shrub          alnifolia (Ra)
cover in 1991 and 26% of total shrub cover in 2006.
Total shrub cover (all shrub species, all sample units)
decreased 3% between 1991 and 2006, but this                SD = 3.8). There were 51 quadrats that contained
difference was not significant when sample units            more than 20 buckthorn seedlings/m2, and the
were treated as replicates (Wilcoxon V = 7225.5,            maximum number of seedlings found in a 1 m2
P = 0.37).                                                  quadrat was 114.
    Shrub and tree seedlings were counted within two           There was little or no apparent relationship
1 m2 quadrats at each sample unit (total n = 330 per        between change in buckthorn cover and the richness
sample year). In 2006, buckthorn seedlings occurred         or cover of other plant taxa in the herbaceous plant or
in 69% of the 1 m2 quadrats and 79% of the sample           shrub strata between 1991 and 2006. Change in herb
units. Buckthorn seedlings occurred in twice as many        stratum species richness showed no significant linear
sample units as the second most frequent species            relationship with change in adult buckthorn cover,
(Thuja occidentalis), and we counted 3183 buckthorn         and cover in the herb stratum also did not change
seedlings in total—this number exceeded by an order         linearly with buckthorn cover (Fig. 3). Change in the
of magnitude the number of seedlings recorded for           number of shrub species other than buckthorn showed
all other species combined (Fig. 2). Seedlings of           no linear relationship with change in adult buckthorn
T. occidentalis were second most numerous (236              cover, but there was a weak negative relationship
seedlings), and seedlings of Ilex verticillata were third   between change in shrub cover and change in adult
most abundant (132 seedlings). Both T. occidentalis         buckthorn cover (Fig. 3d; P \ 0.01, R2 = 0.06). This
and I. verticillata were widespread at Cedarburg Bog,       relationship implies that cover of all shrub species,
and in 2006, adults grew in 108 and 109 sample              excluding buckthorn, decreased as buckthorn cover
units (65 and 66% frequency), respectively. The             increased.
seedling abundance of these native species was only a          We examined relationships between change in
fraction of the buckthorn seedling abundance,               buckthorn cover and the change in cover of each of
despite having adult frequencies similar to buckthorn       the 50 herbaceous plant and shrub species that
adult frequency. Similarly, buckthorn seedling den-         showed the greatest total gains or losses in cover in
sities exceeded those of native woody species.              the 15 years between sample dates. Only the native
Mean buckthorn seedling density in 2006 was 9.6             shrub Cornus stolonifera showed a weak negative
seedlings/m2 (SD = 14.7), which was more than               relationship with change in buckthorn cover
twice the mean seedling density of all other tree and       (P \ 0.01, R2 = 0.07), and only among those sample
shrub taxa combined (mean = 3.7 seedlings/m2,               units in which buckthorn cover increased (n = 104).

1808                                                                                           J. E. Mills et al.

Fig. 3 Wetland plant
community changes
between 1991 and 2006 in
relation to change in
R. frangula cover. Changes
in herb stratum species
richness (a), herb stratum
percent plant cover (b),
shrub species richness
excluding buckthorn (c),
and percent shrub cover
excluding buckthorn (d) in
relation to change in log-
transformed percent cover
of buckthorn (n = 124
sample units). Horizontal
dashed line indicates zero

The relationship between change in total shrub cover    the negative end of the primary axis (Fig. 4). The
and change in buckthorn cover (Fig. 3d) was not         angle between the vector sum for sampling units in
solely due to the change in C. stolonifera cover; the   which buckthorn cover increased and the vector sum
relationship remained significant when the contribu-    for units in which buckthorn never occurred (Fig. 4b)
tion of C. stolonifera to total shrub cover was         did not vary significantly based on a distribution
excluded from the regression. Although C. stolonif-     derived from 1,000 randomizations of invasion status
era cover decreased as buckthorn cover increased,       group membership (P = 0.18). In other words, these
there was no significant difference in mean change of   groups of sample units moved in statistically indis-
C. stolonifera cover between sample units lacking       tinguishable directions through species space.
buckthorn at both sample dates and those sample         Similarly, the angle between the 1991-to-2006 vector
units in which buckthorn cover increased (t =           sum of sample units in which buckthorn never
- 1.06, P = 0.29, df = 143). Cover of C. stolonifera    occurred and the vector sum of sample units in
decreased in both groups of plots between 1991 and      which buckthorn cover decreased did not signifi-
2006.                                                   cantly vary from randomly generated angles
   Ordination by principal coordinates analysis         (P = 0.08), nor did the angle between vector sums
(PCO) indicated that species composition in the herb    of sample units in which buckthorn cover increased
and shrub strata in the majority of sample units        and in which cover decreased (P = 0.024; Bonfer-
changed similarly in the 15 years between samples.      roni-corrected a = 0.017). Sample units that gained
Independent of buckthorn invasion status, most          or lost buckthorn cover occupied the same general
sample units moved through species space towards        region of species space in both years.

Exotic shrub invasion in an undisturbed wetland                                                                             1809

Fig. 4 a Diagram of ordination by principal coordinates            sample unit vector directions, and black arrow indicates mean
analysis of presence/absence data for 135 herb or shrub species    direction of all sample unit vectors. b Vector sums for three
in 165 sample units. R. frangula was excluded from the species     sets of sample units grouped by invasion status indicated with
list prior to analysis. Symbol type indicates invasion status of   black arrows: buckthorn cover increased between sample dates
sample units: buckthorn cover increased between sample dates       (Inc), buckthorn cover decreased between sample dates (Dec),
(circles, n = 104), buckthorn cover decreased between sample       and buckthorn absent in both sample dates (Abs). The origins
dates (triangles, n = 20), buckthorn absent in both sample         of the vector sum arrows indicate the position of the 1991
dates (squares, n = 41). Symbols indicate position of 1991         group centroids, and the arrowheads indicate the position of
sample units and arrowheads indicate position of 2006 sample       2006 group centroids
units in species space. Inset shows relative frequencies of

Discussion                                                         Much as it does for other invasive woody plant
                                                                   species (Rejmánek and Richardson 1996; Richardson
The abundance of buckthorn in Cedarburg Bog                        et al. 2000), seed dispersal by birds facilitates rapid
increased dramatically between 1991 and 2006. Our                  spread of buckthorn. As an example, buckthorn was
results support the inclusion of buckthorn among the               introduced in Ontario in the early 1900s and was
most invasive woody plants in temperate eastern                    initially largely restricted to urban centers, but by the
forests (Webster et al. 2006). Buckthorn has spread                mid-1990s, it grew throughout the province (Catling
throughout much of the wetland, and the rate of                    and Porebski 1994). Even if over 90% of the fruit
spread appears to be increasing. The frequency of                  crop drops beneath the parent trees in our study
occurrence increased from zero when buckthorn first                system, as it does with the similarly invasive
arrived in the wetland around 1955 (Reinartz and                   Rhamnus cathartica (Archibold et al. 1997; Knight
Kline 1988) to 33% in less than 40 years (1955–                    and Reich 2005), the number of seeds that are
1991). In the 15 years between sample dates of this                dispersed larger distances by birds must be increas-
study (1991–2006), its frequency increased to 72%.                 ing. The long distance dispersal rate may not change,
This increasing rate of spread is consistent with other            but more seeds will travel long distances as the seed
studies indicating lag phases in the spread of invasive            availability continues to grow. Propagule pressure, a
plants. Frappier et al. (2003) inferred an increasing              critical driver in successful plant invasions (Lonsdale
rate of buckthorn spread in a New England upland                   1999), has increased in the Cedarburg Bog and could
forest using stem ages estimated from annual growth                promote spread to adjacent wetlands.
rings, and Wangen and Webster (2006) identified                       Given the negative effects so often documented
similar behavior in the spread of the non-native tree              following exotic shrub invasions and the magnitude
Acer platanoides L.                                                of the increase in buckthorn abundance over
   The high rate of spread and invasiveness of                     15 years, the lack of any major changes in the plant
buckthorn can be partially attributed to the produc-               community composition or structure attributable to
tion of large numbers of fleshy fruits that attract birds.         buckthorn invasion was surprising. The vast majority

1810                                                                                             J. E. Mills et al.

of published studies suggest that exotic shrub inva-      a relationship between change in buckthorn cover and
sions negatively affect plant communities. Fagan and      changes in shrub cover or richness. Competition
Peart (2004) found that glossy buckthorn decreased        among species within a functional group offers
growth rates of native tree saplings, increased sapling   intuitive appeal for assessing community responses
mortality rates, and reduced seedling performance for     to invasion, but the degree to which plants of the
all but the most shade tolerant species in upland         same functional type interact seems to vary. As
deciduous forests. Following invasion of upland           examples, Fargione et al. (2003) showed that resident
forests by Lonicera maackii (Rupr.) Maxim., Gould         plants in an experimental grassland limited invasion
and Gorchov (2000) observed reduced survival and          by plants of the same functional type, whereas Von
fecundity of several annual plant species, and a          Holle and Simberloff (2004) did not observe this type
similar study comparing invaded and uninvaded plots       of inhibition in a similar experiment conducted in
showed that tree seedling density and species rich-       riparian forest. In our study, although the negative
ness, as well as herb cover, were inversely related to    relationship between change in shrub cover and
L. maackii cover (Hutchinson and Vankat 1997).            change in buckthorn cover was statistically signifi-
Plant species richness and cover, seed and bud bank       cant, it was weak. Cornus stolonifera was the only
richness and density, and tree seedling richness and      species that appeared to significantly respond to
density were all lower under L. maackii canopies and      increased buckthorn cover, but the relationship
the magnitude of many of these effects increased with     between changes in total cover of shrubs (excluding
L. maackii residence time (Collier et al. 2002).          buckthorn) and buckthorn cover (Fig. 3d) likely
Lonicera tatarica L., another exotic invasive shrub,      reflects subtle decreases in cover among several
similarly reduced tree seedling densities and plant       shrub species. Although buckthorn may negatively
species richness and cover in the herbaceous plant        affect other shrubs, shrub cover and richness declined
stratum in New England forests, most likely by            throughout the wetland, even in the absence of
reducing light availability within and below the shrub    buckthorn. The effect of this invasive exotic shrub on
stratum (Woods 1993).                                     species in the same functional group appeared
   In contrast to the many studies suggesting exotic      minimal.
shrub invasions reduce the growth and abundance of           The buckthorn invasion had no detectable influ-
other plants, we found that plant cover in the            ence on the compositional changes we observed in
herbaceous plant stratum and species richness in          the 15 years between sample dates (Fig. 4), but our
both the herb and shrub strata showed no response to      results do indicate habitat preferences of this exotic
change in buckthorn cover. The buckthorn invasion         shrub. Obligate wetland plant species dominated the
also had no detectable influence on changes in            majority of sample units that lacked adult buckthorn
species composition. Although unexpected, our             in both 1991 and 2006, whereas sample units that
results are consistent with those reported by Houla-      contained buckthorn often included species that
han and Findlay (2004). They found that buckthorn         frequently grow in slightly drier microhabitats. This
and other invasive exotic plants did not exclude          suggests that adult buckthorn shrubs prefer drier
native plant species in temperate wetlands and that       sites within the wetland. Buckthorn seedlings
exotics were no more likely than native species to act    occurred more widely throughout the wetland, but
as community dominants. Likewise, high buckthorn          inundation events that occur during long-term
cover did not affect herb cover and the presence of       hydrologic fluctuation will likely prevent many of
buckthorn had no effect on species richness in the        these from reaching maturity. Incidentally, changes
upland deciduous forests studied by Frappier et al.       in the composition of vegetation in Cedarburg Bog
(2004). Our results and these few other published         between 1991 and 2006 involved decreases in the
studies support the conclusions of Ricciardi and          frequency of wetland obligate species and increases
Cohen (2007)—the conditions that favor invasiveness       in the frequency of species that less often occur in
need not lead to negative effects.                        wetland habitat (Appendix B). These changes in
   Since the species growing in the shrub stratum         species composition imply that water levels
share physical space and may compete for resources        declined over time. Christensen et al. (2007) pre-
such as light and seed dispersers, we expected to find    dicted that central North America will likely face

Exotic shrub invasion in an undisturbed wetland                                                               1811

increased drying over the next century, since the          invasions by altering the selection regime to favor the
predicted increases in temperature will offset             invader. In the absence of disturbance, the compet-
increased precipitation. Continued drying would            itive ability of native plants remains unaltered and
likely increase the amount of habitat that could           they can better accommodate the presence of new
support buckthorn.                                         species. The relationship between disturbance and the
    In seeking to develop statistical generalizations of   effects of plant invasion remains understudied
biotic invasions, Williamson and Fitter (1996) argued      (Levine et al. 2003), but our findings suggest that
that plant invasions often have little or no effect on     disturbance mediates the community-level response
invaded communities or ecosystems and, despite its         to invaders.
magnitude, the buckthorn invasion described in this            While minimal disturbance may have promoted
study may be another example. Accommodation                the biotic acceptance of buckthorn, it is also possible
among species may occur more often than compet-            that the response of the plant community to buck-
itive exclusion, and our results support the theory of     thorn invasion lags well behind invasion and has yet
biotic acceptance proposed by Stohlgren et al.             to become apparent. In a 50-year retrospective study
(2006). The theory, developed from data collected          using re-sampled Wisconsin upland forest stands,
over a range of spatial scales and vegetation types,       Rogers et al. (2008) found that declines in native
posits that invaders tend to coexist with resident         species richness showed little relationship with
species, rather than displace them. In their meta-         invasive species richness. They concluded that weedy
analysis, Levine et al. (2004) similarly concluded that    natives reduced overall species richness as much as
species interactions did not repel invaders, but could     non-native species, but also proposed that a time lag
act to limit the abundance of exotic species. If the       could explain the generally weak relationship
lack of any major effect indicates the biotic accep-       between non-native and native richness. At present,
tance of buckthorn in Cedarburg Bog, this might            predicting how long it takes for an invasion to elicit a
suggest buckthorn acquires resources in a manner           response remains a challenge, and lag times likely
distinct from the resident species. The absence of         vary widely among communities. It is possible that
species that utilize resources in a manner similar to      the weak responses to invasion that we observed will
buckthorn could create what Shea and Chesson               increase with buckthorn residence time, but this can
(2002) termed a niche opportunity. Resource use            only be assessed through continued long-term
efficiency of invasive species in low-nutrient systems     monitoring.
can exceed that of natives (Funk and Vitousek 2007),           In this study, we examined an exotic shrub
and buckthorn may use nutrient resources more              invasion in an undisturbed wetland and saw little
efficiently than native species in this nitrogen-limited   response in the plant community after a 15-year
wetland system.                                            period. Plant invasions do adversely affect some
    Although disturbance can facilitate plant invasion     invaded communities, but studying communities that
(Davis et al. 2000; Davis and Pelsor 2001; Thompson        exhibit little change in response to invasion is
et al. 2001; Vilà et al. 2007; but see Walker et al.      important for shaping a more complete understanding
2005), the buckthorn invasion we have described            of the community and ecosystem responses to
occurred in the absence of eutrophication, recent          invasion (Levine et al. 2003). Focusing only on those
vegetation removal, or hydrological alteration—all         invasions that produce strong negative effects will
common anthropogenic disturbances in freshwater            limit the development of theories to explain the
wetlands (Galatowitsch et al. 1999). It is possible that   effects of invasion. Additionally, an improved under-
atmospheric nitrogen deposition, which has increased       standing of the relationships among species during
globally from pre-industrial levels (Vitousek et al.       and following invasion would increase the utility of
1997b), has favored this buckthorn invasion.               invasion response theories (Parker et al. 1999; Shea
Although natural disturbances occur in the Cedarburg       and Chesson 2002). While disturbance can facilitate
Bog, the low levels of anthropogenic disturbance may       biological invasions, our findings suggest that distur-
help explain the apparent acceptance of buckthorn by       bance can also influence the interactions between
the plant community. Byers (2002) argued that              resident native and invasive species following
anthropogenic disturbance magnifies the effect of          invasion.

1812                                                                                                                  J. E. Mills et al.

Acknowledgments We appreciate the data collection efforts              funded through the Research Growth Initiative of the
of Ron Londré, Kristin Westad and Joanne Kline. We wish to            University of Wisconsin-Milwaukee, and a grant from the
thank Dave Roberts and Dave Rogers for their advice and                Wisconsin Department of Natural Resources.
assistance in preparing this manuscript. This research was


Appendix A List of taxa present in shrub and herbaceous plant          Bog contains only the native genotypes of these species.
strata. Non-native species indicated with asterisk (WISFLORA           Frequency indicates percent fraction of 165 sample units that
2008). Although Phalaris arundinacea and Phragmites aus-               contain the taxon. Mean cover calculated using only those
tralis are often treated as non-native, we believe Cedarburg           sample units containing the taxon
Taxon                                                           1991 Freq.     2006 Freq.    1991 Mean cover      2006 Mean cover
                                                                (%)            (%)           (%)                  (%)

Shrub stratum
Alnus incana (L.) Moench subsp. rugosa (Du Roi)                 13.9           20.6          30.9                 18.8
Amelanchier interior Nielsen                                    0.6            0             21                   0
Aronia 9 prunifolia (Marshall) Rehder (pro sp.)                 17.6           12.7          5.8                  13.8
Betula pumila L.                                                50.3           41.8          26                   21.7
Chamaedaphne calyculata (L.) Moench var. angustifolia           20             16.4          11.5                 24.4
  (Aiton) Rehder
Cornus racemosa Lam.                                            1.2            0             2.5                  0
Cornus stolonifera Michx.                                       66.1           44.2          26.7                 22.2
Gaylussacia baccata (Wangenh.) K.Koch                           4.8            7.3           11                   6.7
Ilex mucronata (L.) M.Powell, V.Savolainen & S.Andrews          9.1            1.2           6.9                  13
Ilex verticillata (L.) A. Gray                                  64.2           66.1          38.2                 39.2
Juniperus communis L. var. depressa Pursh                       9.1            11.5          6.4                  9.1
Lonicera dioica L.                                              5.5            1.8           2                    3.3
Lonicera oblongifolia (Goldie) Hook.                            1.8            1.8           1.3                  5.3
Lonicera villosa (Michx.) Schult.                               11.5           6.1           6.1                  7
Parthenocissus quinquefolia (L.) Planch.                        15.8           28.5          2.7                  4.2
Prunus virginiana L. var. virginiana                            0.6            0             1                    0
Rhamnus alnifolia L’Hér.                                       19.4           18.8          8.2                  11.1
Rhamnus cathartica L.*                                          2.4            1.8           8.8                  8
Rhamnus frangula L.*                                            46.7           72.7          24.6                 35.8
Ribes americanum Mill.                                          12.1           6.7           8.5                  7.5
Ribes cynosbati L.                                              1.8            0             6                    0
Ribes hirtellum Michx.                                          12.7           1.8           3.8                  2
Ribes lacustre (Pers.) Poir.                                    0              2.4           0                    4.8
Ribes missouriense Nutt.                                        1.2            0             6                    0
Ribes triste Pall.                                              1.2            0             9.5                  0
Rosa palustris Marshall                                         20             17            10.7                 7.7
Rubus idaeus L. var. strigosus (Michx.) Maxim.                  2.4            0.6           3.8                  20
Salix bebbiana Sarg.                                            6.1            1.8           7                    20.7
Salix candida Fluggé ex Willd.                                 8.5            6.7           9.1                  9.1
Salix discolor Muhl.                                            23             5.5           21.9                 13.9

Exotic shrub invasion in an undisturbed wetland                                                                  1813

Appendix A continued
Taxon                                                      1991 Freq.   2006 Freq.   1991 Mean cover   2006 Mean cover
                                                           (%)          (%)          (%)               (%)

Salix pedicellaris Pursh                                   10.3         4.2          3.9               8.3
Salix petiolaris Sm.                                       8.5          4.8          18.1              27
Salix sericea Marshall                                     4.8          4.8          14                18.8
Spiraea alba Du Roi var. alba                              2.4          0            8                 0
Toxicodendron radicans (L.) Kuntze subsp. negundo          1.2          1.8          1.1               0.5
  (Greene) Gillis
Toxicodendron vernix (L.) Kuntze                           46.7         46.1         15                10.3
Viburnum lentago L.                                        12.1         6.7          15.2              14.5
Viburnum opulus L.                                         4.8          3.6          4.6               9.2
Viburnum prunifolium L.                                    1.2          0            5                 0
Vitis riparia Michx.                                       7.3          12.7         1.1               2
Herbaceous plant stratum
Actaea rubra (Aiton) Willd.                                0            0.6          0                 2.8
Agalinis paupercula (A.Gray) Britton                       1.8          0            1.2               0
Amphicarpaea bracteata (L.) Fernald                        6.7          5.5          2.9               2.1
Andromeda glaucophylla Link                                7.3          4.8          1.1               1.7
Anemone quinquefolia L. var. quinquefolia                  0.6          0.6          1                 4.5
Apios americana Medik.                                     0            0.6          0                 0.7
Aralia nudicaulis L.                                       6.7          16.4         8.2               6.8
Arisaema triphyllum (L.) Schott subsp. Triphyllum          6.1          13.3         1                 1.4
Asclepias incarnata L. subsp. Incarnata                    3.6          3            1.4               1.9
Aster borealis (Torr. & A.Gray) Prov.                      7.3          15.8         1.8               2.6
Aster laevis L. var. laevis                                0            0.6          0                 3.3
Aster lateriflorus (L.) Britton                            3            7.3          1.5               2.9
Aster puniceus L.                                          41.2         44.2         2.3               3.8
Athyrium filix-femina (L.) Roth ex Mert.                   0            1.8          0                 1
  var. angustum (Willd.) G.Lawson
Bidens comosus (A.Gray) Wiegand                            20.6         21.8         3.2               3
Bidens connatus Muhl. ex Willd.                            0            3.6          0                 2.2
Bidens coronatus (L.) Britton                              29.7         37.6         2.8               2.6
Boehmeria cylindrica (L.) Sw.                              4.2          6.1          2.2               2.8
Bromus ciliatus L.                                         3            0            2.3               0
Calamagrostis canadensis (Michx.) P.Beauv.                 12.7         7.9          6.8               6.8
Calla palustris L.                                         23           19.4         7.3               2.2
Calopogon tuberosus (L.) Britton; Sterns & Poggenb. var.   1.8          1.2          0.9               0.3
Caltha palustris L.                                        28.5         18.8         4.9               3.8
Campanula aparinoides Pursh                                15.2         18.2         1.3               2.4
Cardamine pratensis L. var. palustris Wimm. & Grab.        30.9         16.4         1.7               1.2
Carex aquatilis Wahlenb. var. aquatilis                    11.5         6.7          10.6              5.8
Carex aurea Nutt.                                          0.6          1.8          1.2               0.5
Carex bebbii (L.H.Bailey) Olney ex Fernald                 2.4          0            1                 0
Carex bromoides Schkuhr ex Willd. subsp. Bromoides         0            0.6          0                 21.2

1814                                                                                         J. E. Mills et al.

Appendix A continued
Taxon                                        1991 Freq.   2006 Freq.   1991 Mean cover   2006 Mean cover
                                             (%)          (%)          (%)               (%)

Carex chordorrhiza Ehrh. ex L.f.             7.3          1.2          5.1               3.3
Carex communis L.H.Bailey var. communis      3            0            2.3               0
Carex cristatella Britton                    0            0.6          0                 0.8
Carex deweyana Schwein. subsp. Deweyana      5.5          12.1         2                 4
Carex diandra Schrank                        4.8          1.2          4.9               1.3
Carex disperma Dewey                         15.8         4.2          3.4               3
Carex gracillima Schwein.                    0.6          0.6          1                 9.7
Carex gynocrates Wormsk. ex Drejer           0            0.6          0                 0.6
Carex hystericina Muhl. ex Willd.            0            4.2          0                 3.2
Carex interior L.H.Bailey                    21.8         36.4         3                 5.4
Carex lacustris Willd.                       18.2         18.2         11.1              9.4
Carex lasiocarpa Ehrh. subsp. americana      27.9         26.7         6.8               6.8
  (Fernald) D.Löve & Bernard
Carex leptalea Wahlenb. subsp. Leptalea      37.6         43.6         2.9               3.6
Carex leptonervia (Fernald) Fernald          0            0.6          0                 0.5
Carex limosa L.                              7.3          14.5         3                 2.9
Carex livida (Wahlenb.) Willd.               0            6.1          0                 4.2
  var. radicaulis Paine
Carex magellanica Lam.                       1.2          1.2          1.4               2.9
Carex oligosperma Michx.                     0            0.6          0                 6.8
Carex pedunculata Muhl. Ex Willd.            0            3            0                 2.1
Carex prairea Dewey ex A.W.Wood              0            0.6          0                 0.4
Carex pseudocyperus L.                       20           16.4         3.1               3.6
Carex stipata Muhl. ex Willd. var. stipata   3.6          5.5          1.2               3.3
Carex stricta Lam.                           4.2          6.7          20.4              6.4
Carex tenera Dewey                           0            0.6          0                 0.8
Carex tenuiflora Wahlenb.                    5.5          1.8          1.4               3.5
Carex trisperma Dewey var. trisperma         3.6          13.3         2.6               3.5
Carex utriculata Boott                       0            0.6          0                 2.4
Carex vesicaria L.                           0.6          0            14.6              0
Chelone glabra L.                            6.1          3            1.1               1.1
Cicuta bulbifera L.                          27.9         8.5          2.2               2.5
Cicuta maculata L.                           10.9         13.9         4.4               2.2
Cinna arundinacea L.                         0.6          6.1          0.7               4.8
Circaea alpina L. subsp. alpina              0            1.8          0                 2
Clematis virginiana L.                       0            0.6          0                 0.6
Clintonia borealis (Aiton) Raf.              1.2          8.5          8.5               3.1
Comarum palustre L.                          26.1         21.8         2.5               3.8
Coptis trifolia (L.) Salisb.                 5.5          6.1          2.4               2.2
Cornus canadensis L.                         1.8          4.8          1.4               4.8
Cuscuta gronovii Willd. ex Roem. & Schult.   0.6          1.2          0.4               2.6
  var. gronovii
Cypripedium parviflorum Salisb.              0.6          4.8          1                 2.2

Exotic shrub invasion in an undisturbed wetland                                                                  1815

Appendix A continued
Taxon                                                      1991 Freq.   2006 Freq.   1991 Mean cover   2006 Mean cover
                                                           (%)          (%)          (%)               (%)

Decodon verticillatus (L.) Elliott                         3            0.6          6.2               8.7
Drosera linearis Goldie                                    1.2          1.8          0.8               1.8
Drosera rotundifolia L.                                    6.7          9.1          2.7               1.4
Dryopteris carthusiana (Vill.) HP.Fuchs                   10.3         13.9         1.3               1.7
Dryopteris cristata (L.) A.Gray                            3.6          12.7         1.4               1.5
Dulichium arundinaceum (L.) Britton                        1.2          0.6          11                2.7
Eleocharis elliptica Kunth                                 6.1          2.4          1.2               0.8
Eleocharis erythropoda Steud.                              0.6          0.6          1.3               2
Eleocharis quinqueflora (Hartmann) Schwarz                 1.2          0            1.9               0
Elymus virginicus L. var. virginicus                       0            0.6          0                 0.5
Epilobium coloratum Biehler                                5.5          1.8          1.2               1.2
Epilobium leptophyllum Raf.                                11.5         12.1         1.9               1.2
Equisetum arvense L.                                       4.2          1.8          9                 1.2
Equisetum fluviatile L.                                    37.6         27.3         5.1               3.5
Erigeron annuus (L.) Pers.                                 0            0.6          0                 2.2
Eriophorum vaginatum L. subsp. spissum (Fernald) Hultén   1.2          0            0.8               0
Eriophorum viridi-carinatum (Engelm.) Fernald              4.2          0.6          1.7               2.5
Eupatorium maculatum L.                                    21.2         23           1.8               3.7
Eupatorium perfoliatum L. var. perfoliatum                 1.8          1.2          1                 2.5
Eupatorium rugosum Houtt. var. rugosum                     0            1.2          0                 7.3
Fragaria vesca L. subsp. americana (Porter) Staudt         0            0.6          0                 6.5
Fragaria virginiana Duchesne                               0            5.5          0                 2.3
Galium labradoricum (Wiegand) Wiegand                      13.9         17           1.3               0.9
Galium tinctorium L.                                       0            1.8          0                 3.3
Galium trifidum L. subsp. trifidum                         17           11.5         1.3               1.9
Galium triflorum Michx.                                    3            6.7          1.3               1.6
Gaultheria hispidula (L.) Muhl. ex Bigelow                 4.2          0.6          2.3               0.7
Gaultheria procumbens L.                                   0.6          1.8          1                 15
Geranium maculatum L.                                      0            1.2          0                 4.2
Geum canadense Jacq.                                       0            0.6          0                 2.8
Glyceria grandis S.Watson                                  0            0.6          0                 0.8
Glyceria striata (Lam.) Hitchc.                            41.2         43.6         2.2               3.7
Gnaphalium helleri Britton var. micradenium (Weath.)       0            0.6          0                 0.3
Impatiens capensis Meerb.                                  30.9         37           7.2               6.5
Iris versicolor L.                                         0            0.6          0                 0.5
Laportea canadensis (L.) Wedd.                             0.6          0            0.7               0
Leersia oryzoides (L.) Sw.                                 22.4         34.5         4.4               3.7
Lemna minor L.                                             2.4          0            13.8              0
Linnaea borealis L. subsp. americana (Forbes) Hultén ex   2.4          2.4          1                 4.2
Liparis loeselii (L.) Rich.                                0.6          0            1.2               0
Lobelia kalmii L.                                          3.6          2.4          1.4               1.3

1816                                                                                                  J. E. Mills et al.

Appendix A continued
Taxon                                                 1991 Freq.   2006 Freq.   1991 Mean cover   2006 Mean cover
                                                      (%)          (%)          (%)               (%)

Lycopus americanus Muhl. ex WP.C.Barton              0            0.6          0                 1.9
Lycopus uniflorus Michx.                              69.7         81.2         2.6               4
Lysimachia ciliata L.                                 1.2          1.2          0.8               2.2
Lysimachia thyrsiflora L.                             67.9         66.1         1.8               1.9
Maianthemum canadense Desf.                           52.1         57.6         2.4               3.7
Maianthemum trifolium (L.) Sloboda                    32.7         19.4         4.7               3.2
Mentha arvensis L. var. canadensis (L.) Kuntze        0.6          0.6          1                 0.7
Menyanthes trifoliata L.                              18.8         15.8         5                 6.8
Mitchella repens L.                                   3            4.2          1.3               3.9
Mitella diphylla L.                                   0.6          0.6          2                 0.8
Mitella nuda L.                                       4.8          7.9          2.8               3.6
Muhlenbergia glomerata (Willd.) Trin.                 1.2          4.2          2.3               4.9
Muhlenbergia mexicana (L.) Trin.                      0            1.2          0                 2.7
Nuphar variegata Durand                               0.6          0.6          6.1               2.6
Onoclea sensibilis L.                                 1.8          2.4          7.3               7.4
Osmunda regalis L. var. spectabilis (Willd.) A.Gray   3            4.8          3.6               10.6
Packera paupercula (Michx.) A.Löve & D.Löve         0            0.6          0                 0.3
Parnassia glauca Raf.                                 3.6          4.2          3.2               4.1
Pedicularis lanceolata Michx.                         3            3            1                 3
Phalaris arundinacea L.                               6.1          9.1          9.7               10.5
Phragmites australis (Cav.) Trin. ex Steud.           9.1          12.1         3.7               6.1
Pilea pumila (L.) A.Gray                              0            4.2          0                 1.2
Pogonia ophioglossoides (L.) Ker Gawl.                1.8          2.4          1                 0.5
Polygonum amphibium L.                                2.4          5.5          4.4               1.5
Polygonum sagittatum L.                               0            0.6          0                 0.6
Potamogeton gramineus L.                              1.8          0            2.5               0
Potamogeton pusillus L.                               0.6          0            1                 0
Prenanthes alba L.                                    0.6          0            1.2               0
Pyrola asarifolia Michx. subsp. asarifolia            3.6          1.2          1.2               4.2
Ranunculus hispidus Michx.                            0            0.6          0                 10.3
Rhynchospora alba (L.) Vahl                           4.8          4.2          11.4              8.2
Rhynchospora capillacea Torr.                         1.8          1.8          2.2               7.9
Rubus pubescens Raf.                                  65.5         72.7         6.2               5.4
Rumex crispus L.*                                     5.5          12.7         1.1               1.3
Rumex orbiculatus A.Gray                              0            0.6          0                 0.6
Sagittaria latifolia Willd. var. latifolia            10.3         10.3         3.6               4.1
Sarracenia purpurea L. subsp. purpurea                14.5         17.6         4.5               5.3
Schoenoplectus acutus (Muhl. ex Bigelow)              3            1.2          12.4              7.1
  A.Löve & D.Löve var. acutus
Scutellaria galericulata L.                           10.3         10.9         1.3               4.1
Scutellaria lateriflora L.                            30.9         40.6         1.9               2.2
Sium suave Walter                                     5.5          12.7         2.3               2.4
Solanum dulcamara L.*                                 33.3         38.8         2.9               4.2
Solidago gigantea Aiton                               23.6         13.9         1.3               3.5

Exotic shrub invasion in an undisturbed wetland                                                                                   1817
Appendix A continued
Taxon                                                             1991 Freq.     2006 Freq.      1991 Mean cover    2006 Mean cover
                                                                  (%)            (%)             (%)                (%)

Solidago patula Muhl. ex Willd. var. patula                       5.5            13.9            1                  3
Solidago uliginosa Nutt.                                          8.5            6.7             1.4                3
Sparganium americanum Nutt.                                       0.6            0               1.1                0
Sparganium emersum Rehmann                                        0              0.6             0                  9.6
Stellaria longifolia Muhl. Ex Willd.                              0.6            1.2             1                  0.3
Symplocarpus foetidus (L.) Salisb. ex WP.C.Barton                10.9           17.6            5.1                6.2
Taraxacum officinale Weber*                                       4.8            8.5             1                  0.5
Thelypteris palustris Schott var. pubescens (Lawson) Fernald      64.8           67.9            5.5                6.6
Tofieldia glutinosa (Michx.) Pers. var. glutinosa                 1.8            1.2             0.9                1.7
Triadenum fraseri (Spach) Gleason                                 5.5            12.1            1.9                3.6
Trientalis borealis Raf. subsp. borealis                          38.2           50.3            2.4                2.8
Triglochin maritima L.                                            3              2.4             1.3                1.5
Typha latifolia L.                                                1.2            9.7             11                 5
Typha 9 glauca Godr.*                                             22.4           20.6            16.8               17.1
Vaccinium angustifolium Aiton                                     0              0.6             0                  3.6
Vaccinium myrtilloides Michx.                                     27.9           21.8            9.6                8.4
Vaccinium oxycoccos L.                                            27.3           23              2.7                3.4
Viola spp.                                                        38.2           60.6            1.7                2.1

Appendix B Species scores for the 10 species present in                 to occur on upland or wetland sites, FACW = facultative
more than 10% of sample units between sample dates and                  wetland species that usually occur in wetlands, and
with the largest positive and negative loadings on PCO axis 1           OBL = obligate wetland species that grow only in wetland
(Fig. 4). Species are sorted in ascending order by axis 1               habitat. Note that half of species with negative axis 1 scores
score. Wetland indicator categories indicate the likelihood             are not wetland obligates, and all but one of the species with
of occurrence in wetland habitat (WISFLORA 2008):                       positive axis 1 scores are wetland obligates. The overall
FACU = facultative upland species that usually occur on                 movement (1991–2006) of sample units in this ordination
upland sites, FAC = facultative species that are equally likely         (Fig. 4) is towards the negative end of axis 1
Species                                Axis 1 score        Axis 2 score              Wetland            Frequency          Frequency
                                                                                     indicator          1991 (%)           2006 (%)

Aralia nudicaulis                      -0.219              -0.033                    FACU                6.7               16.4
Dryopteris carthusiana                 -0.215              -0.051                    FACW               10.3               13.9
Symplocarpus foetidus                  -0.182              -0.054                    OBL                10.9               17.6
Cicuta maculata                        -0.178              -0.117                    OBL                10.9               13.9
Caltha palustris                       -0.172              -0.053                    OBL                28.5               18.8
Parthenocissus                         -0.169              -0.067                    FAC                15.8               28.5
Vitis riparia                          -0.167              -0.040                    FACW                7.3               12.7
Maianthemum canadense                  -0.142                0.049                   FAC                52.1               57.6
Gylceria striata                       -0.123                0.039                   OBL                41.2               43.6
Aster puniceus                         -0.123              -0.019                    OBL                41.2               44.2
Campanula aparinoides                   0.157              -0.042                    OBL                15.2               18.2
Carex limosa                            0.167                0.192                   OBL                 7.3               14.5
Aster borealis                          0.180                0.063                   OBL                 7.3               15.8

1818                                                                                                                J. E. Mills et al.

Appendix B continued
Species                              Axis 1 score           Axis 2 score         Wetland            Frequency            Frequency
                                                                                 indicator          1991 (%)             2006 (%)

Sarracenia purpurea                    0.192                  0.251              OBL                14.5                 17.6
Chamaedaphne calyculata                0.200                  0.198              OBL                20                   16.4
Carex lasiocarpa                       0.222                  0.112              OBL                27.9                 26.7
Comarum palustre                       0.242                -0.002               OBL                26.1                 21.8
Phragmites australis                   0.265                  0.175              FACW                9.1                 12.1
Typha 9 glauca                         0.267                -0.107               OBL                22.4                 20.6
Sagittaria latifolia                   0.280                -0.092               OBL                10.3                 10.3

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