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Cryptic intercontinental dispersal, commercial retailers, and the genetic diversity of native and non-native cattails (Typha spp.) in North America


Abstract and Figures

Although cattails (Typha spp.) are important components of wetlands around the world, the three most widespread species (T. angustifolia, T. domingensis, T. latifolia) are becoming increasingly dominant. We used global phylogenetic and phylogeographic assessments to test the hypotheses that each species has experienced multiple introductions of divergent lineages into North America and that commercial retailers are aiding long-distance dispersal. Our analyses identified T. angustifolia as a paraphyletic species with a highly divergent lineage. We found evidence for at least one introduced T. angustifolia lineage in wild populations and garden centres of North America. Although potentially complicated by incomplete lineage sorting, our data suggest dispersal of T. domingensis between Europe and Australia, and further investigation should assess a possible introduction of a non-native T. domingensis lineage into North America. T. latifolia has experienced bidirectional dispersal between North America and Europe, and a sample of T. latifolia purchased in a Canadian garden centre was an Asian lineage. Interspecific hybridization and novel intraspecific admixture have been repeatedly implicated in biological invasions, including invasions by the hybrid cattail Typha × glauca, and future work should focus on the potential contributions of non-native lineages to regional patterns of invasion by Typha spp. in North America.
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Cryptic intercontinental dispersal, commercial retailers,
and the genetic diversity of native and non-native cattails
(Typha spp.) in North America
Claudia Ciotir .Joanna Freeland
Received: 2 June 2015 / Revised: 7 October 2015 / Accepted: 8 October 2015 / Published online: 23 October 2015
ÓSpringer International Publishing Switzerland 2015
Abstract Although cattails (Typha spp.) are impor-
tant components of wetlands around the world, the
three most widespread species (T. angustifolia, T.
domingensis, T. latifolia) are becoming increasingly
dominant. We used global phylogenetic and phylo-
geographic assessments to test the hypotheses that
each species has experienced multiple introductions of
divergent lineages into North America and that
commercial retailers are aiding long-distance dispersal.
Our analyses identified T. angustifolia as a paraphyletic
species with a highly divergent lineage. We found
evidence for at least one introduced T. angustifolia
lineage in wild populations and garden centres of North
America. Although potentially complicated by incom-
plete lineage sorting, our data suggest dispersal of T.
domingensis between Europe and Australia, and further
investigation should assess a possible introduction of a
non-native T. domingensis lineage into North America.
T. latifolia has experienced bidirectional dispersal
between North America and Europe, and a sample of
T. latifolia purchased in a Canadian garden centre was
an Asian lineage. Interspecific hybridization and novel
intraspecific admixture have been repeatedly impli-
cated in biological invasions, includinginvasions by the
hybrid cattail Typha 9glauca, and future work should
focus on the potential contributions of non-native
lineages to regional patterns of invasion by Typha spp.
in North America.
Keywords Typha spp. Intercontinental dispersal
Cryptic introductions Biological invasions
Wetlands Garden centres
Propagule pressure is recognized as a potentially
important determinant of the invasive success of
introduced species, partly because strong propagule
pressure should increase the likelihood of a suit-
able match between genotype and environment in the
introduced range (Simberloff, 2009). In addition, when
multiple provenances are involved, strong propagule
pressure can increase the likelihood of admixture
between formerly allopatric conspecific lineages that
have become sympatric in their introduced range, and
the resulting evolutionary novelty may facilitate bio-
logical invasions (Kolbe et al., 2004; Lavergne &
Molofsky, 2007). Although multiple founders and high
Handling editor: John Havel
Electronic supplementary material The online version of
this article (doi:10.1007/s10750-015-2538-0) contains supple-
mentary material, which is available to authorized users.
C. Ciotir
Environmental and Life Sciences Graduate Program,
Trent University, Peterborough, ON K9J 7B8, Canada
J. Freeland (&)
Department of Biology, Trent University, 2140 East Bank
Drive, Peterborough, ON K9J 7B8, Canada
Hydrobiologia (2016) 768:137–150
DOI 10.1007/s10750-015-2538-0
genetic diversity provide only one explanation for
successful biological invasions (Dlugosch & Parker,
2008), genetic diversity can be an important contribut-
ing factor (Roman & Darling, 2007) and may be
particularly likely to play a role in invasions by species
that have been repeatedly—and sometimes deliber-
ately—introduced to sites around the world.
Plant nurseries provide one important route for
introducing non-native species, including aquatic
macrophytes (Martin & Coetzee, 2011; Hussner,
2012). These macrophytes may include cattails
(species in the genus Typha) which are perennial
semi-aquatic plants important in temperate and tropical
wetlands of the northern and southern hemispheres.
There are approximately 10–15 species of Typha
worldwide (Smith, 2000; Kim & Choi, 2011), occur-
ring in all major land masses except Greenland and
Antarctica (Geze, 1912; Smith, 2000). The three most
widely distributed cattail species, which are also the
only three species growing in the wild in North
America, are Typha angustifolia L. (narrow-leaf cat-
tail), Typha domingensis Pers. (southern cattail), and
Typha latifolia L. (broad-leaf cattail); each of these,
plus their interspecific hybrids, has in recent decades
become increasingly dominant in multiple geographic
regions (Grace & Harrison, 1986; Beare & Zedler,
1987; Galatowitsch et al., 1999; Parsons & Cuthbert-
son, 2001; Miao, 2004; Freeland et al., 2013; Zapfe &
Freeland, 2015).
Although the three species are partially sympatric
(see Figs. 1,2,3for geographic ranges), their latitu-
dinal and altitudinal limits vary. Typha angustifolia
reaches its northern limit around 51°N and grows
throughout temperate North America and Eurasia
(Grace & Harrison, 1986; Smith, 2000; Stevens &
Hoag, 2000) at elevations up to 2000 m (Hickman,
1993). This species was introduced into Australia and
North America (AVH, 2013; Ciotir et al., 2013) and is
considered invasive in parts of North America (Gala-
towitsch et al., 1999). Typha domingensis is limited to
the pantropical latitudes of Eurasia, North, Central, and
South America, southern Pacific Islands, New Zealand,
and Australia (Briggs, 1987; Paczkowska, 1994;
Smith, 2000; Gupta, 2013), reaching its limits at
around 40°N (Smith, 2000) and 1500 m in altitude
(Hickman, 1993; Vibrans, 2004; Stevens & Hoag,
2006). This species is considered introduced and
invasive in Hawaii (USDA-NRCS, 2014) and,
although native to central and southern North America,
is considered invasive in the Florida Everglades
(Newman et al., 1998; Miao, 2004), parts of California
(Beare & Zedler, 1987), and Costa Rica (Osland et al.,
2011). Typha latifolia is more widely distributed and
tolerates more northerly latitudes and higher altitudes
(up to 2300 m) than the other two species (Grace &
Harrison, 1986; Smith, 2000). Typha latifolia has a
native range in temperate latitudes of Europe (USDA-
ARS, 2005), North America (Smith, 2000; Sawada
et al., 2003), Africa (Geze, 1912), and Asia (Kun &
Simpson, 2010) and has been introduced to Australia
(Briggs, 1987; Parsons & Cuthbertson, 2001), New
Zealand (ISSG, 2006), Tasmania (Barnard, 1882), and
the Caribbean (USDA-ARS, 2005). Australia (Parsons
& Cuthbertson, 2001; Zedler & Kercher, 2004), New
Zealand (Champion & Clayton, 2001), Tasmania
(Parsons & Cuthbertson, 2001), and Hawaii (HISC,
2013) consider T. latifolia an invasive species.
A quick search on the internet using the search terms
‘‘Typha’ and ‘‘nurseries’’ identified nearly 70,000
websites from around the world, many of which
advertised one or more of T. latifolia, T. angustifolia,
and T. domingensis (along with additional congeneric
species) for sale. This high level of Typha trafficking
suggests that cryptic intercontinental dispersal of Typha
lineages may be more common than realized, which in
turn may have implications for the growing invasive-
ness of Typha spp. In addition, if multiple non-native
lineages of Typha spp. have been introduced into North
America, they could help guide potential avenues of
investigation into phenomena such as regional varia-
tions in the success of non-native Typha (Freeland et al.,
2013), or the transition to invasiveness by native Typha
species (Newman et al., 1998; Miao, 2004).
The primary goal of this study was therefore to test
the hypothesis that multiple non-native lineages of T.
angustifolia, T. domingensis, and T. latifolia have been
introduced into North America. We also tested the
hypothesis that plant nurseries are facilitating long-
distance dispersal of Typha lineages.
Materials and methods
Sampling, DNA extraction, and DNA sequencing
This study was primarily based on T. angustifolia, T.
latifolia, and T. domingensis sequences from three
sources. The first source was 82 samples collected
138 Hydrobiologia (2016) 768:137–150
from North America, Europe, and Africa between
2007 and 2013, from which we identified 42 novel
haplotypes (see below). Throughout this study, hap-
lotype refers to a specific cpDNA sequence. The
second source was eight plant nurseries in Canada
(Ontario and British Columbia) from which we
purchased 25 plants. Nineteen of these purchases
were identified by the nurseries as T. angustifolia, one
as T. latifolia, four as Typha laxmannii Lepech., and
one as Typha minima Funck; these are the only four
Typha species that we found for sale in Canada, and
border restrictions meant that we were unable to order
plants from nurseries in the USA or other countries.
The third source was 38 sequences previously pub-
lished by Kim & Choi (2011) which comprise 21
unique haplotypes. In addition, we obtained from Kim
& Choi (2011), and from some additional samples that
we collected, a total of 16 haplotypes from six
additional species in the genus Typha, and five
haplotypes from five Sparganium spp., for use as
outgroups in our phylogenetic analyses (see below).
The genus Sparganium was chosen as an outgroup
because it is the closest sister group to the genus Typha
(Bremer, 2000). Sample locations are provided in
Figs. 1,2, and 3, and Table S1. For the newly acquired
sequences, a leaf tip of approximately 2 cm from each
sampled plant was dried in a bag of silica beads (Fisher
Scientific) and stored at -20°C on return to the lab.
Dried plant material was ground in a mixer mill
(Retsch MM300; Retsch, Newtown, Pennsylvania,
USA), and genomic DNA was extracted from 10 to
30 mg dried tissue per plant using the E.Z.N.A spin
Fig. 1 Map of T. angustifolia indicating the sampling sites
represented by black circles and the contemporary distribution
areas represented in dark grey. Distribution information from
WCSP (2012), Kim & Choi (2011), and Ciotir et al. (2013).
Solid lines with arrows identify approximate pathway of
intercontinental movement of naturalized plants, and small
dashes indicate the approximate provenance of samples
obtained from garden centres in Canada (see text and
Table S1 for details)
Hydrobiologia (2016) 768:137–150 139
column DNA plant mini kits (Omega Bio-Tek,
Georgia, USA), eluted into a final volume of 100 ll.
From each collected or purchased sample, three
chloroplast DNA (cpDNA) regions were amplified:
trnL–trnF(trnL gene, trnL intron, and trnLFinter-
genic spacer), trnC–petN (intergenic spacer), and
psbMtrnD (intergenic spacer). The trnL–trnF region
was amplified using the primers ‘c’ and ‘f’ described in
Taberlet et al. (1991). The trnC–petN and psbMtrnD
regions were amplified using primers developed by
Kim & Choi (2011). Each PCR reaction included 19
Taq reaction buffer (UBI Life Sciences), 2 mM
, 0.2 mM dNTPs, 20 lM of each primer, 2.5U
HP Taq (UBI Life Sciences), 1.2 ll (100%) of BSA, and
approximately 10 ng DNA in a total volume of 25 ll.
PCR amplifications were performed in a Mastercycler
epgradient thermal cycler (Eppendorf) (Table 1), and
PCR products were purified by incubating with 10U
exonuclease I and 2U shrimp alkaline phosphatase
(Fermentas International, Inc.) for 15 min at 15°C
followed by 15 min at 80°C. Purified products were
sequenced in both directions using a BigDye Termina-
tor v3.1 Cycle Sequencing Kit (Applied Biosystems,
Foster City, California, USA). Sequences were run on a
DNA Analyser 3730xl ABI (Applied Biosystems).
The plants acquired from nurseries that were
identified as either T. angustifolia or T. latifolia were
additionally genotyped at microsatellite loci TA3,
TA5, TA8, and TA20 (Tsyusko-Omeltchenko et al.,
2003), which have alleles that are specific to either T.
latifolia or T. angustifolia (Snow et al., 2010; Kirk
et al., 2011) and can therefore be used to discriminate
T. angustifolia, T. latifolia, and T. 9glauca; the latter
is the invasive hybrid of T. angustifolia and T. latifolia
that dominates the Great Lakes and St. Lawrence
Seaway regions of North America (Olson et al., 2009;
Travis et al., 2010; Freeland et al., 2013).
Sequence alignments and data analysis
De novo sequences were assembled and edited in
Seqman (DNASTAR LaserGene 5, Madison, WI,
Fig. 2 Map of T. domingensis indicating the sampling sites
represented by black circles and the contemporary distribution
areas represented in dark grey.Dotted lines show potential
pathways of long-distance dispersal, although direction of
movements could not be determined (see text and Table S1
for details). Distribution information from WCSP (2012) and
Kim & Choi (2011)
140 Hydrobiologia (2016) 768:137–150
USA) and aligned with the previously published Typha
and Sparganium sequences (Table S1). All sequences
were imported into BioEdit Software (Hall, 1999).
Each region was aligned using CLUSTALW (Thomp-
son et al., 1994) with subsequent manual adjustments,
based on 55 sequences of each chloroplast region from
T. angustifolia,22fromT. domingensis, and 63 from T.
latifolia (Table S1). The three cpDNA regions were
then appended in a single 3147 bp alignment.
Duplicate sequences were removed, leaving 10 haplo-
types from T. angustifolia (three novel, and seven from
Kim & Choi, 2011), 15 haplotypes from T. domingen-
sis (11 novel, and four from Kim& Choi, 2011), and 38
haplotypes from T. latifolia (28 novel, and 10 from
Kim & Choi, 2011). Phylogenetic analyses were
performed on these haplotypes plus an additional 35
haplotypes from T. capensis Rohrb., T. elephantine
Roxb., T. laxmannii Lepech., T. minima Lepech.,T.
Fig. 3 Map of T. latifolia indicating the sampling sites
represented by black circles and the contemporary distribution
areas represented in dark grey.Solid lines with arrows identify
approximate pathway of intercontinental movements of
naturalized plants, and small dashes indicate the approximate
provenance of samples obtained from garden centres in Canada
(see text and Table S1 for details). Distribution information
from WCSP (2012), Kim & Choi (2011), and Ciotir et al. (2013)
Table 1 PCR conditions used for amplifying the three cpDNA regions
Region PCR conditions
Initial denaturation
Final extension
No. of
trnL–trnF94°C/120 s 94°C/60 s 55°C/60 s 72°C/120 s 72°C/420 s 32
trnC–petN95°C/240 s 95°C/60 s 59.5°C/60 s 72°C/90 s 72°C/420 s 40
psbM–trnD94°C/240 s 94°C/60 s 58°C/60 s 72°C/90 s 72°C/600 s 40
Hydrobiologia (2016) 768:137–150 141
shuttleworthii Koch & Sond., T. orientalis C.Presl.,
and the outgroup Sparganium (Table S1).
Bayesian inference was used to reconstruct the
phylogeny of Typha spp. in MRBAYES ver. 3.2
(Huelsenbeck & Ronquist, 2001). Three Bayesian runs
were generated with independent partitions for trnL–
trnF, trnC–petN, and psbM–trnD according to their
alignment lengths and models. The default prior and
likelihood settings were used for all parameters except
for the nucleotide substitution models which were set to
GTR ?I for the trnL–trnF and psbM–trnD regions
(with alignment lengths of 1006 bp and 1129 bp,
respectively), and GTR ?G for the trnC–petN region
(alignment length of 1012 bp). Each analysis included
77 sequences, of which five represented outgroups.
Models of nucleotide sequence substitution were
generated by MrModeltest ver. 2.3 based on all variable
sites and the good fit of Akaike Information Criterion
(AIC) (Nylander, 2004). Substitution model parameters
and rates of substitution were allowed to vary across
partitions using ratepr =variable and the ‘unlink’
command. MCMC chain analyses were run for up to
50,000,000 iterations, sampling trees once every 1,000
iterations. Convergence of the four Markov chains and
assessment of ‘burn-in’ values were determined by
examining the average standard deviation of split
frequencies and by plotting the likelihood values
against the number of generations on a linear regression
graph. Using a burn-in value of 10% of the total number
of trees, we generated the consensus tree and posterior
probability values. Multiple output files were examined
to assess the convergence between samples in Tracer
ver.1.5. (Rambaut & Drummond, 2008). The consensus
trees were visualized in FigTree ver.1.3.1. (Drummond
& Rambaut, 2007).
Concatenated alignments of all sequences (i.e.
duplicates were returned to the dataset) of each of T.
angustifolia,T. domingensis, and T. latifolia were used
to generate parsimony networks in TCS ver. 1.21
(Clement et al., 2000). The analyses were set with 95%
statistical parsimony and gaps as the fifth state
(Templeton & Singh, 1993).
The Bayesian 50% majority rule consensus tree
reconstructed T. angustifolia and T. domingensis as
paraphyletic or polyphyletic species, and T. latifolia as
a monophyletic species (Fig. 4). Typha angustifolia is
divided into one clade that comprises multiple lin-
eages, plus one divergent haplotype (E4/N1/P3) that
was found in both Europe and North America. The
former has two clusters, the first of which includes
three Asian, one North American, and two purchased
(from Canadian nurseries) haplotypes, plus one haplo-
type that is dispersed across multiple continents (Asia,
Europe, North America, and Australia). The second
cluster comprises two European haplotypes and one
Asian haplotype. The divergent haplotype of T.
angustifolia (E4/N1/P3) groups with T. capensis,T.
elephantina, and T. domingensis, with T. capensis as its
nearest neighbour. These relationships are supported in
all analyses by high posterior probability values (pp:
0.71–1). In T. domingensis, five basal lineages repre-
sented by two North American haplotypes (N2, N3),
one African (Af2), and two Asian (A2, A3) haplotypes
are intermediate to T. elephantina and the remaining T.
domingensis sequences, which form a single clade
comprising haplotypes from Asia, Africa, Europe, and
North America. The T. domingensis topology is
supported by high posterior probability values (pp:
0.93–0.99). One haplotype is shared between Europe
and Australia (E4/Au). For T. latifolia, the phylogeny
recovered three broad clusters: one from North Amer-
ica, one from Asia and eastern Europe, and the third
primarily from western Europe (Fig. 4). All relation-
ships within T. latifolia were supported by high
posterior probability values (pp: 0.99–1). The relative
extent of divergence among haplotypes inferred from
the phylogenetic tree was largely reflected in each of
the haplotype networks (Figs. 5,6,7).
In both the phylogenetic tree and the haplotype
networks, samples purchased from nurseries in
Canada have the haplotype prefix ‘P’ (Figs. 4,5,6,
7). With the exception of three plants identified as T.
angustifolia that turned out to be T. latifolia, each
purchased plant had a haplotype sequence that agreed
with the retailer’s taxonomic identification; however,
the microsatellite data identified ten of the plants
labelled as T. angustifolia as the hybrid T. 9glauca.
Purchased samples of T. angustifolia comprised
haplotypes from the two divergent genetic lineages,
and the purchased T. latifolia plant represented an
Asian lineage. The purchased T. minima matched a
haplotype previously identified from Europe, and the
purchased T. laxmannii matched a haplotype previ-
ously identified in both Europe and Asia (Table S1).
142 Hydrobiologia (2016) 768:137–150
T. angustifolia
T. latifolia
T. minima
T. domingensis
T. latifolia
T. angustifolia
T. latifolia
T. latifolia
T. latifolia
T. angustifolia
T. latifolia
T. elephantina
T. shuttleworthii
T. capensis
T. latifolia
T. latifolia
T. latifolia
T. latifolia
S. fallax
S. eurycarpum
T. latifolia
T. latifolia
T. latifolia
T. angustifolia
T. domingensis
T. latifolia
T. latifolia
T. latifolia
T. latifolia
T. latifolia
T. domingensis
T. latifolia
T. domingensis
T. latifolia
T. domingensis
T. angustifolia
T. latifolia
T. orientalis
T. latifolia
T. domingensis
T. latifolia
T. minima
T. domingensis
T. latifolia
T. minima
T. latifolia
T. latifolia
T. angustifolia
T. latifolia
S. emersum
T. laxmannii
T. domingensis
T. latifolia
T. laxmannii
T. domingensis
T. latifolia
T. orientalis
T. angustifolia
T. domingensis
T. domingensis
T. latifolia
T. latifolia
T. orientalis
T. angustifolia
T. angustifolia
T. latifolia
T. angustifolia
T. domingensis
T. latifolia
T. orientalis
T. latifolia
T. domingensis
S. erectum
T. latifolia
T. domingensis
T. latifolia
T. laxmannii
T. latifolia
T. domingensis
T. latifolia
S. hyperboreum
T. elephantina
T. shuttleworthii
Fig. 4 The 50% majority rule consensus tree from Bayesian
analyses based on combined cpDNA sequences of Typha and
Sparganium species. Numbers on nodes represent the posterior
probability support values. Haplotypes are labelled with letters
that indicate provenance: AAsia, EEurope, Af Africa, Au
Australia, NNorth America, Ppurchased samples (purchased
from plant nurseries in Canada). Numbers in brackets represent
the numbers of individuals from each location. T. latifolia
haplotypes E4, E5, and E6 are from eastern Europe, and E1, E2,
E3, E7, E8, and E9 are from western Europe. See Table S1 for
more detailed information on locations
Hydrobiologia (2016) 768:137–150 143
Although globally distributed species are among those
most likely to become invasive due to their high
dispersal and colonizing capacity (Nikulina et al.,
2007), global movements are often underestimated
due to cryptic introductions (Lavoie et al., 1999;
Geller et al., 2010). In this study, we found evidence
that the designation of native and non-native Typha
taxa in North America is complicated by cryptic
introductions of non-native lineages and, in the case of
T. angustifolia, by taxonomic uncertainty. Below, we
will discuss our findings and the associated implica-
tions for each species.
Typha angustifolia
Our results clearly show that T. angustifolia is
polyphyletic, with one divergent haplotype (E4/N1/
P3) more closely related to T. domingensis,T. capensis,
and T. elephantina than to its conspecific lineages. This
polyphyly could potentially be explained by inter-
specific hybridization (either ancient or recent) with T.
capensis and subsequent introgression of the chloro-
plast genome; previous examples of introgression
following ancient hybridization have been found in
diverse taxa (e.g. Gross & Rieseberg, 2005; Klymus
et al., 2010). Alternatively, haplotype E4/N1/P3 may
belong to a cryptic species that closely resembles T.
A2 A5
Fig. 5 TCS network for T. angustifolia. Haplotype labels:
AAsia, EEurope, Af Africa, Au Australia, NNorth America,
Ppurchased samples (purchased from plant nurseries in Canada).
Haplotypes are coloured according to their actual or inferred
origin: white North America, light grey Asia, dark grey Europe.
Haplotypes present in multiple continents are marked with a thick
line.Sizesofcircles are proportional to haplotype frequencies.
See Table S1 for more detailed information on locations
E2 E3
Fig. 6 TCS network for T.
domingensis. Haplotype
labels: AAsia, EEurope, Af
Africa, Au Australia,
NNorth America,
Ppurchased samples
(purchased from plant
nurseries in Canada).
Haplotypes are coloured
according to their actual or
inferred origin: white North
America, light grey Asia,
dark grey Europe.
Haplotypes present in
multiple continents are
marked with a thick line.
Sizes of circles are
proportional to haplotype
frequencies. See Table S1
for more detailed
information on locations
144 Hydrobiologia (2016) 768:137–150
angustifolia. Polyphyly and cryptic species have often
been identified from molecular data in taxa with
cosmopolitan distributions (e.g. Bickford et al., 2007;
Lemmon et al., 2007; Nikulina et al., 2007). Further
investigation is necessary before we can explain this
highly divergent haplotype.
The remaining T. angustifolia haplotypes comprise
Asian, European, and North American haplotypes. A
previous study based on microsatellite genotypes
suggested that Typha angustifolia was introduced to
North America from Europe (Ciotir et al., 2013), and
the current study agrees with this conclusion because
we found three haplotypes in North America (N2, E4/
N1/P3, A1/E1/N3/Au) that are sufficiently divergent
to represent at least one introduction of a non-native
haplotype (Fig. 5), and possibly multiple introduc-
tions. Because it is embedded within the predomi-
nantly Asian cluster (Fig. 5), one of the T. angustifolia
haplotypes introduced into North America (A1/E1/
N3/Au) seems also to have cryptically moved from
Asia to Europe, where T. angustifolia is considered
native (Geze, 1912; Cirujano, 2002). That same
N3 N13
N16 N5
Fig. 7 TCS network for T. latifolia. Haplotype labels: AAsia,
EEurope, Af Africa, Au Australia, NNorth America,
Ppurchased samples (purchased from plant nurseries in
Canada). Haplotypes E4, E5, and E6 were from eastern Europe
(east of longitude 13°, while haplotypes E1, E2, E3,
E7, E8, and E9 were from western Europe (west of longitude
13°01.39.1500). Haplotypes are coloured according to their
actual or inferred origin: white North America, light grey Asia,
dark grey Europe. Haplotypes present in multiple continents are
marked with a thick line. Sizes of circles are proportional to
haplotype frequencies. See Table S1 for more detailed
information on locations
Hydrobiologia (2016) 768:137–150 145
haplotype (A1/E1/N3/Au) was also blatantly intro-
duced into Australia, where T. angustifolia was first
recorded in 1943 (AVH, 2013).
Formally differentiating between the contributions
of processes such as dispersal, vicariance, and lineage
sorting to the current distributions of haplotypes is
challenging in species with complex evolutionary
histories (e.g. Kodandaramaiah, 2010). Typha angus-
tifolia should be considered one example of such a
species because it has repeatedly experienced both
vicariance and dispersal throughout its history and
also hybridizes with multiple congeneric species (see
Kim & Choi, 2011, and references therein). In
addition, samples for widespread species such as T.
angustifolia are unlikely to represent the entire
species’ distribution. Despite these complications,
incomplete lineage sorting must be considered as a
possible explanation for haplotypes sharing between
continents. Nevertheless, we do not believe that
incomplete lineage sorting can explain the patterns
that we found in T. angustifolia, partly because this
study is based on haplotypes that reflect [3000 bp of
the chloroplast genome, which evolves relatively
rapidly in Typha (Guisinger et al., 2010); this high
resolution, combined with the relatively rapid lineage
sorting that occurs in plastid versus nuclear DNA
markers, means that identical cpDNA haplotypes
shared a relatively recent common ancestor. Further-
more, intercontinental dispersal of T. angustifolia is
unequivocal in locations from which it was previously
absent, including Australia (AVH, 2013). Finally, as
noted above, a previous study used microsatellite
genotypes to conclude that T. angustifolia had dis-
persed from Europe to North America (Ciotir et al.,
2013). Therefore, although constraints imposed by our
study species leave us unable to unequivocally
demonstrate that lineage sorting was complete prior
to more recent episodes of intercontinental dispersal,
several lines of evidence collectively suggest that
incomplete lineage sorting cannot be the sole expla-
nation for our conclusion of long-distance dispersal in
T. angustifolia.
Our data therefore reflect at least one introduction of
a non-native T. angustifolia lineage into North Amer-
ica. In addition, we found three non-native T. angus-
tifolia haplotypes in plants obtained from garden
centres, and one of these haplotypes is found in natural
populations. The remaining two nursery haplotypes,
which are of Asian provenance, have not been found in
the wild, but are very closely related to the widespread
non-native A1/E1/N3/Au haplotype that is also found
in North America, and more exhaustive sampling in
North America is required before we can conclude that
these lineages have not been naturalized at any
location. We cannot exclude the possibility that garden
centres obtained their plants from natural populations,
although this seems much less likely for haplotypes
that have not been found in the wild. Regardless, it is
notable that we had a T. angustifolia plant delivered to
us in Ontario through an online order from a supplier in
British Columbia, a transaction that led to a dispersal of
a non-native T. angustifolia haplotype across a distance
of approximately 4500 km. Less dramatically, a recent
survey of garden owners in Ontario identified a mean
Euclidean distance of *40 km between sites of
purchased plants (including invasive species) and their
destinations, but there were also rare long-distance
dispersal events of up to 500 km between purchase
location and destination (Marson et al., 2009). Com-
mercial suppliers are therefore facilitating the dispersal
of non-native lineages regardless of whether they were
the initial source of the introductions. Finally, the sale
by nurseries of the hybrid T. 9glauca, labelled as T.
angustifolia, could also help with the spread of the
hybrid which is dominant in the Great Lakes region
(Travis et al., 2010; Kirk et al., 2011; Freeland et al.,
Typha domingensis
Typha domingensis is paraphyletic, with several North
American, Asian, and African haplotypes (Af2, A2,
A3, N2, N3) marginally more closely related to T.
elephantina than to the remaining T. domingensis
haplotypes, which form a monophyletic group
(Fig. 4). The proximity of the paraphyletic clades to
one another suggests that paraphyly in this case may
be explained by incomplete lineage sorting following
speciation. The parsimony network reveals three
lineages in North America that have a fairly high
degree of relatedness (N2, N3, N4), and which
therefore likely shared a recent common provenance,
although it is unclear whether these three haplotypes
were more likely to have dispersed from Africa (their
nearest neighbour) to North America or vice versa. A
third lineage that is also present in North America (N1)
shows substantial divergence from the other two North
American lineages, which suggests that at least one
146 Hydrobiologia (2016) 768:137–150
non-native lineage of T. domingensis may have been
introduced into North America. There also seems to
have been at least one dispersal event of T. domingensis
between Europe and Australia (E4/Au) (Fig. 2). Typha
domingensis is introduced and invasive in Hawaii
(HISC, 2013), and invasive in Florida (Zedler &
Kercher, 2004), southern California (Beare & Zedler,
1987), and Costa Rica (Osland et al., 2011). Cryptic
intercontinental dispersal of T. domingensis lineages to
North America could help explain the invasiveness of
putatively native populations, although the lack of
continental clustering for this species, combined with
paraphyly at the species level (Fig. 4), means that we
cannot rule out a potential influence of incomplete
lineage sorting on the patterns that we found. We are
therefore more cautious about inferring intercontinen-
tal dispersal in T. domingensis, and conclude that
although dispersal has likely occurred to some extent
(e.g. between Europe and Australia, based on an
identical haplotype found at geographically distant
sites), additional markers should be employed in future
studies to further investigate the phylogeographic
history of this species.
Typha latifolia
The T. latifolia haplotypes identified a single mono-
phyletic group with continental phylogeographic struc-
turing: the three subclades represent North America,
western Europe, and a combination of eastern Europe
and Asia (Fig. 4). The continental phylogeographic
structuring is also evident in the network, which shows
a distinct separation between two clusters: Asia and
eastern Europe versus North America and western
Europe (Fig. 7). The phylogenetic tree suggests that
haplotype E9/N1 was introduced into North America
from Europe, as it is the only North American haplotype
within a European cluster on the phylogenetic tree
(Fig. 4). In addition, the network suggests that haplo-
type E13 was introduced into Europe from North
America, a conclusion that is supported by an earlier
study that used microsatellite data to suggest that T.
latifolia colonized Europe from North America (Ciotir
et al., 2013); these lines of evidence collectively
identify bidirectional intercontinental dispersal of T.
latifolia between North America and Europe. Eastern
European haplotypes share relatively recent ancestry
with Asian haplotypes, reflecting dual colonization of
Europe by T. latifolia: once from Asia into eastern
Europe, and once from North America into western
Europe (Fig. 7). In addition, North America is the most
plausible source of Australian T. latifolia, where it is
considered an introduced and invasive species (Smith,
2000; Parsons & Cuthbertson, 2001; ISSG, 2006).
Incomplete lineage sorting is unlikely to explain
inferred patterns of intercontinental dispersal in T.
latifolia because of the same arguments that were
applied to T. angustifolia, plus a strong pattern of
continental phylogeographic structuring (Figs. 4,7).
We also determined that a T. latifolia plant
purchased from a Canadian retailer was an Asian
lineage, which again raises questions about the
potential role that nurseries may play in facilitating
the long-distance dispersal of non-native lineages, and
also about the authenticity of some ‘native plant’
claims by retailers. This non-native lineage has not
been found in any natural North American T. latifolia
populations, and the likelihood of its naturalization is
difficult to evaluate, particularly when we do not know
how long it has been marketed by North American
nurseries; however, there are many precedents of
Asian invasive species and lineages becoming inva-
sive in North America (e.g. Reichard & White, 2001).
T. latifolia has increased its geographic distribution in
North America in recent decades (Shih & Finklestein,
2008), and if increasingly dominant behaviour is noted
within this species, researchers should monitor for the
potential involvement of non-native lineages, partic-
ularly those (such as the Asian lineage we recovered)
that can be plausibly introduced through garden
centres and water gardens.
In conclusion, our data strongly suggest cryptic
intercontinental dispersal of genetic lineages in both T.
angustifolia and T. latifolia, which has resulted in the
introduction of non-native lineages into North Amer-
ica. Our conclusions regarding T. domingensis are
more circumspect because of the potential influence of
incomplete lineage sorting, which should be further
investigated in future studies using additional markers.
We have also reiterated the known fact that commer-
cial retailers play a role in the global dispersal of plants
(e.g. Reichard & White, 2001; Mack & Lonsdale,
2007; Martin & Coetzee, 2011), both within and
between continents; further investigation into nurs-
eries as potential conduits of non-native Typha
lineages should include commercial samples from
multiple countries and continents. Additionally, our
data revealed that T. angustifolia is rendered
Hydrobiologia (2016) 768:137–150 147
polyphyletic by a highly divergent lineage, and further
investigation will be required in order to determine
whether the domination of wetlands by T. angustifolia
and its hybrid T. xglauca in North America involves
one or both of the divergent, polyphyletic T. angus-
tifolia lineages. Wetlands are particularly susceptible
to biological invasions, including invasions by species
in the genus Typha (Mills et al., 1993; Galatowitsch
et al., 1999; Brinson & Malvarez, 2002; Zedler &
Kercher, 2004). Hybrids and novel intraspecific
admixtures have been repeatedly implicated in bio-
logical invasions (Schierenbeck & Ellstrand, 2009),
including invasions by the hybrid Typha 9glauca
(Freeland et al., 2013), and future work should use
variable nuclear markers to infer specific pathways of
introductions and investigate the potential contribu-
tions of non-native lineages to regional patterns of
invasion by Typha spp. in North America.
Acknowledgments We are very grateful to Serena Caplins,
Jennifer Coughlan, Sarah Dungan, Heather Kirk, Jonathan
Mitchley Nicole Vachon, Morgan Wehtje, Walter Wehtje, Stan
Yavno, and Chris Yesson for collecting cattail samples during
their field trips in North America, Europe, and Africa. We are
grateful to Dr. Jonathan Mitchley who provided shelter,
transportation, and logistics during the fieldtrip in the UK and
Europe. Special thanks to Dr. Chris Yesson for his contribution to
the global map distributions, and for insightfulbiogeographic and
phylogenetic advice. Many thanks to the Jack Matthews
international scholarship at Trent University for covering the
costs of the European field trip. This study was also funded by a
Natural Sciences and Engineering Council (NSERC) Discovery
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Supplementary resource (1)

... Recent assessments indicate T. angustifolia was likely introduced to North America from Europe (Ciotir et al. 2013;Ciotir & Freeland 2016), and it has been present on the East Coast since at least the early 19 th century (Shih & Finkelstein 2008). Concurrent with its establishment was the emergence of hybrid T. x glauca, the offspring of T. ...
... This F1 hybrid is often sterile (Smith 1967;), but backcrosses and advanced generation hybrids have been recently confirmed in the Great Lakes Region Snow et al. 2010;Kirk et al. 2011;Zapfe & Freeland 2015). Initially restricted to the eastern margins of the continent, these taxa have rapidly expanded westward due to anthropogenic disturbances, commercial sales, and their high fecundity and dispersal ability (Shih & Finkelstein 2008;Ciotir & Freeland 2016;Bansal et al. 2019). ...
... T. angustifolia has been commercially-available in the region till recently (Ciotir & Freeland 2016), there is no evidence of the commercial sale of T. x glauca. This suggests its presence in the estuary is likely the product of natural hybridization, which presumably occurred after the establishment of its non-native parent, T. angustifolia. ...
Full-text available
Invasive species represent a significant and growing threat to biodiversity in ecosystems around the world. Research that can address key knowledge gaps is invaluable, particularly as managers grapple with diminishing time, resources, and data to deal with species invasions. Non-native narrow-leaved cattail (Typha angustifolia) is a wetland invader that has been detected in western Canada’s Fraser River Estuary (FRE) in recent decades, but questions around their degree of establishment, impact, manageability, and the potential emergence of invasive hybrid cattail (Typha x glauca), remain unanswered. This research aimed to address these knowledge gaps, investigating the threat potential of these taxa. Using a spectral analysis of aerial imagery, I found that invasive cattails are widespread, currently occupying approximately 4% of FRE marshes. Though never formally recorded in the FRE, T. x glauca is more abundant than T. angustifolia, and likely went undetected due to its cryptic nature. A species distribution model for invasive cattail predicted that 28% and 21% of the FRE has suitability (establishment and persistence) and susceptibility (risk of colonization when suitable) probabilities of > 50% respectively, indicating this invasion is likely to continue. Restoration projects were invasion hotspots, with proportionally more cattail, susceptible habitat, and suitable habitat than the overall estuary. Vegetation sampling demonstrated that cattail-invaded marshes contained lower richness and diversity than uninvaded habitats. Cattail leaf litter had a significant negative effect on richness and diversity, while ramet density and foliar cover did not, suggesting litter may be an important dominance mechanism behind this invasion. Results from a two-year management experiment suggest these impacts may be counteracted, but not without expending considerable resources. Belowground energy reserves declined in response to cutting, however cattail ramets remained unchanged or increased in abundance. Native plant communities have yet to respond significantly to cutting and litter removal, suggesting that more time may be required for their recovery. I conclude that the extent of this invasion, likelihood of further invasion, and management challenges presented by invasive cattail require a strategic shift towards preventative management approaches, such as surveillance and early eradication in uninvaded high-value habitats, along with restoration designs that inhibit litter accumulation.
... Numerous genetic studies of Typha demonstrated that different methods (AFLP, microsatellites, sequencing of different nuclear and plastid DNA regions) gave congruent results, being able to clearly distinguish five traditional European species (sensu Cook, 1980) and to reveal some within-species variability (e.g. Na et al., 2010;Kim and Choi, 2011;Ciotir and Freeland, 2016;Ciotir et al., 2017;Zhou et al., 2018). These studies were mostly focussing on North America, Asia (mainly China) and to a lesser extenton West and Central Europe, while samples from East Europe were not included in the analyses. ...
... We use sequences of a cpDNA region as reliable and easily applicable molecular marker in non-hybrid Typha (Kim and Choi, 2011;Ciotir and Freeland, 2016;Zhou et al., 2018). The dehydrated leaves were ground to powder using Mixer Mill 400 (Retsch) and 3-mm tungsten beads. ...
... Isolation of DNA was performed with DNA-Extran-3 kit (Syntol), following the manufacturer's instructions. We sequenced the intergenic spacer rpl32-trnL of cpDNA (Shaw et al., 2007) as it is the most variable and easily amplifiable of all cpDNA regions, used before for Typha (according to our preliminary tests and Kim and Choi (2011); Ciotir and Freeland (2016); Zhou et al. (2018)). Polymerase chain reactions (PCR) were conducted in 15 μl reaction volumes containing 3 μl of ScreenMix-HS (Evrogen), 10.7 μl deionised water, 0.39 pmol of forward and reverse primers and 1 μl of template DNA. ...
High morphological variation of Typha L. species (Typhaceae) inspires some authors to describe new taxa. We aim to test genetic distinctiveness of some taxa reported in East Europe on morphological basis to verify their taxonomical status. We use sequences of intergenic spacer rpl32-trnL of cpDNA that was shown to be a reliable molecular marker in non-hybrid Typha species. We found that T. caspica Pobed., T. elata Boreau, T. incana Kapit. et Dyukina, T. krasnovae Doweld, T. rossica Krasnova are genetically identical to T. latifolia L., as well as T. foveolata Pobed., T. austro-orientalis Mavrodiev, T. elatior Boenn., T. angustata Bory et Chaub., T. linnaei Mavrodiev et Kapit. to T. angustifolia L. Thus, until some additional evidence of their distinctiveness is not found, we suggest to treat T. caspica, T. elata, T. krasnovae, T. rossica as synonyms of T. latifolia, while T. foveolata, T. austro-orientalis, T. elatior, T. angustata should be synonymized with T. angustifolia. Consequently, T. linnaei is a superfluous name (coined in attempts of neotypification T. angustifolia) and should be also considered synonymous to the latter. The hypothesis of hybrid origin of T. incana should be tested further with microsatellite DNA repeats – if correct, this would indicate T. latifolia as plastid donor. Full-text available on request.
... We examine the threat of two potential non-native invaders to tidal marsh ecosystems in the Pacific Northwest (PNW), narrow-leaved cattail (Typha angustifolia L.), and hybrid cattail (Typha × glauca Godr.), to understand their current distribution and future risk of expansion. Recent assessments suggest T. angustifolia was possibly introduced to North America from Europe Ciotir and Freeland 2016), though it has been present on the East Coast since at least the early nineteenth century (Shih and Finkelstein 2008). Concurrent with its continental establishment was the emergence of hybrid T. × glauca, the offspring of T. angustifolia and native broad-leaved cattail (Typha latifolia). ...
... Concurrent with its continental establishment was the emergence of hybrid T. × glauca, the offspring of T. angustifolia and native broad-leaved cattail (Typha latifolia). Initially restricted to the eastern margins of the continent, these non-native taxa have rapidly expanded westward over the last century due to habitat disturbance and commercial sales (Shih and Finkelstein 2008;Ciotir and Freeland 2016). ...
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The early detection of invasive species is an important predictor of management success. Non-native narrow-leaved cattail (Typha angustifolia) has been detected in the Fraser River Estuary (FRE) in recent decades, but questions around their degree of establishment, and the potential emergence of hybrid cattail (Typha×glauca), remain unanswered. This study models the current and potential future distribution of non-native cattail in the FRE using a combination of spectral imagery analysis and species distribution modeling. Contrary to our expectation, we find that non-native cattails are widespread, currently occupying approximately 4 or 50 ha of FRE tidal marshes. Though never formally recorded in the estuary previously,T. × glauca appears to be the more abundant taxon, suggesting heterosis may be facilitating this invasion. We describe these taxa as cryptic invasive species, as their resemblance to native cattail (Typha latifolia) likely inhibited their detection. In our species distribution model, we distinguish between site suitability (ability to establish and persist) and susceptibility (risk of colonization when suitable). Our model predicts the scale of this invasion may increase over time, as 29% and 20% of the estuary has moderate or high suitability and susceptibility probabilities, respectively, while 16% and 24% of these habitats are currently occupied. Estuary-wide containment and eradication are unlikely given the extent of this invasion. Consequently, we recommend management prioritize monitoring and early eradication in areas of high conservation and cultural value. This study highlights the vulnerability of estuaries to cryptic invasions and the invasibility of Pacific Northwest estuaries by non-native cattail.
... Non-native invasive species, as well as aggressive hybrids, can cause considerable ecologic and economic impacts on terrestrial ecosystems and wetlands (e.g., Lovell et al. 2006;Olson 2006;Pejchar and Mooney 2009;Richardson and Rejmánek 2011;Vilà et al. 2011). While drivers of invasion include natural factors (Dogra et al. 2010), human activities often lead to the rapid spread of invasive species through enhanced dispersal pathways and activities that disturb or alter natural habitats and provide an opportunity for invasive species to displace native species (e.g., Hodkinson and Thompson 1997;Wilcox et al. 2008;Ciotir and Freeland 2016). Climate change also alters wetland habitats in ways that favor invasive species (Rahel and Olden 2008). ...
... (southern cattail). Typha latifolia is native and ubiquitous throughout North America (Grace and Harrison 1986); T. angustifolia was likely introduced from Europe along with early European settlers Ciotir and Freeland 2016) and can now be found throughout the central and northern United States and southern Canada; and T. domingensis is native and primarily found in the southern United States (Bansal et al. 2019). The parental species of T. 9 glauca are sympatric throughout much of North America, giving the hybrid a continental-scale potential hybrid zone. ...
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The Prairie Pothole Region (PPR) of North America has experienced extreme changes in wetland habitat due to proliferation of invasive plants. Typha × glauca is a highly competitive hybrid between native T. latifolia and non-native T. angustifolia, and it is likely the predominant taxon in PPR wetlands. Genetics-based studies are limited, and distributions are poorly known for the first-generation (F1) hybrid and advanced-generation hybrids from F1 mating. Information pertaining to the distribution of T. × glauca could benefit efforts to understand the mechanisms of its spread and to develop management strategies to limit hybrid expansion and preserve progenitors. We used microsatellite markers of field-collected tissue samples from 131 wetlands spread over approximately 350,000 km2 in the PPR to assess the distribution of hybrid T. × glauca relative to its parental species and to examine the prevalence of F1 hybrids and advanced-generation hybrids. Typha × glauca was found in over 80% of wetlands throughout the PPR, compared to 26 and 18% of wetlands with T. latifolia and T. angustifolia, respectively. Advanced-generation hybrids were more common than F1 hybrids, suggesting that hybridization is not a recent phenomenon. Hybrids were significantly taller than T. latifolia, indicating heterosis. Only 7% of sampled individual genets were pure T. latifolia. These results suggest that T. × glauca is pervasive throughout the PPR and may spread independently of both parents. In addition, limited prevalence of native T. latifolia indicates the need for active management to preserve the species.
... Typha species grow in bogs, swamps, wetlands, roadside ditches, lakeshores, pond shores, irrigation canals, and ponds agricultural irrigation ditches [50][51][52]. Although Typha species are ecologically important, they can also be considered an invasive native species in aquatic ecosystems because of their high growth rate and ability to adapt to saline environments, nutrient deficiencies, floods, and drought [48,49,53]. ...
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Heavy metal pollution is a severe concern worldwide, owing to its harmful effects on ecosystems. Phytoremediation has been applied to remove heavy metals from water, soils, and sediments by using plants and associated microorganisms to restore contaminated sites. The Typha genus is one of the most important genera used in phytoremediation strategies because of its rapid growth rate, high biomass production, and the accumulation of heavy metals in its roots. Plant growth-promoting rhizobacteria have attracted much attention because they exert biochemical activities that improve plant growth, tolerance, and the accumulation of heavy metals in plant tissues. Because of their beneficial effects on plants, some studies have identified bacterial communities associated with the roots of Typha species growing in the presence of heavy metals. This review describes in detail the phytoremediation process and highlights the application of Typha species. Then, it describes bacterial communities associated with roots of Typha growing in natural ecosystems and wetlands contaminated with heavy metals. Data indicated that bacteria from the phylum Proteobacteria are the primary colonizers of the rhizosphere and root-endosphere of Typha species growing in contaminated and non-contaminated environments. Proteobacteria include bacteria that can grow in different environments due to their ability to use various carbon sources. Some bacterial species exert biochemical activities that contribute to plant growth and tolerance to heavy metals and enhance phytoremediation.
... The narrow-leaf cattail Typha angustifolia L. was introduced to North America from Europe (Finkelstein 2003;Ciotir et al. 2013). In contrast, broad-leaf cattail Typha latifolia L. is naturally occurring and widespread across North America, although bidirectional exchange of genotypes of T. latifolia has occurred between Europe and North America (Ciotir and Freeland 2016). Expansion of T. angustifolia across North America has generated the invasive hybrid cattail Typha xglauca Godr. ...
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The hybrid cattail Typha xglauca Godr. is morphologically intermediate between Typha latifolia L. and Typha angustifolia L. We propose a method to distinguish these taxa based on morphology throughout emergent life stages. We evaluated four traits of gross morphology and four more from microscopic examination of leaf cross sections. All eight traits were assessed for 45 cattails collected from various types of wetlands in Manitoba and Saskatchewan, Canada, these shoots being identified by sequencing of microsatellite DNA as 17 specimens of T. latifolia and 14 specimens each for T. angustifolia and T. xglauca. Decision-tree analysis indicated that the single trait of mean leaf-apex angle for all leaves on the shoot was able to correctly align all specimens with their genetic identities. However, single-leaf measurements for leaf-apex angle were successful in this regard in only 80–85% of attempts. Ignoring mean leaf-apex angle and using a combination of all remaining seven traits, 44-out-of-45 samples were aligned correctly. Measurement of mean leaf-apex angle for a shoot can be used to distinguish reliably the parental Typha species and the hybrid. The remaining seven morphological traits can then be employed to provide additional support for determinations, possibly as an alternative to genetic determinations.
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Some of the most impactful invasive plants are hybrids that exhibit heterosis and outperform their parent species. Heterosis can result from multiple genetic processes, and may also be more likely when parental populations are inbred. However, although outcrossing between relatives and self-fertilization occur in many widespread plants, no study to our knowledge has investigated whether inbreeding in parental populations could help to explain heterosis in hybrid plants that have displaced their parent species. In the wetlands of southeastern Canada there is a widespread Typha (cattail) hybrid zone in which native T. latifolia (broad-leafed cattail) interbreeds with introduced T. angustifolia (narrow-leafed cattail) to produce the invasive hybrid T. × glauca . Typha reproduce through self-fertilization, outcrossing, and clonal propagation. Heterosis has been identified in T. × glauca by comparing proxy fitness measures between hybrids and parent species, but these studies did not consider the potential importance of inbreeding in parental populations. Because F1 hybrids have higher heterozygosity than their parent species, the self-fertilized offspring of hybrids should have higher heterozygosity than the self-fertilized offspring of parent species; the latter should therefore be more inbred, and potentially more susceptible to inbreeding depression (ID). We tested the hypothesis that self-fertilization leads to greater ID in the offspring of T. latifolia and T. angustifolia compared to the offspring of F1 T. × glauca. We conducted common-garden and wetland experiments using seeds from hand-pollinated plants sourced from natural populations, and quantified several fitness-related measures in the offspring of self-fertilized versus outcrossed parent species and hybrids. Our experiments provided no evidence that inbreeding leads to ID in self-fertilized T. angustifolia, T. latifolia or T. × glauca in either a common garden or a natural wetland, and thus show that heterosis in a widespread invasive hybrid does not rely on comparisons with inbred parents.
Pollen dispersal regulates the formation of the invasive, wind-pollinated hybrid cattail T. × glauca, the F1 offspring of the broadleaf (T. latifolia) and narrowleaf (T. angustifolia) cattail. An earlier study suggested that pollen dispersal by T. latifolia might be spatially restricted, with most dispersal occurring over distances less than 2 m. Restricted pollen dispersal would imply that hybrid formation primarily occurs within mixed stands of cattails. Hybrid formation might also be affected by preferential receipt of conspecific pollen, but this has not been investigated for cattails. We compared patterns of pollen dispersal for T. latifolia and T. angustifolia using a wind tunnel. We then tested whether patterns of pollen receipt were biased toward the capture of conspecific versus heterospecific pollen using monospecific cattail stands with a single local pollen source. Results from the wind tunnel partially supported the previous finding of spatially restricted pollen dispersal for T. latifolia, the paternal parent of F1 hybrids. Pollen receipt by T. angustifolia was biased toward the capture of conspecific pollen. Localized pollen dispersal by T. latifolia and preferential conspecific pollen capture by T. angustifolia should reduce rates of hybrid formation below that expected under random mating.
Macrophytes play an important role in aquatic ecosystems, and thus are often used in ecological risk assessments of potentially deleterious anthropogenic substances. Risk assessments for macrophyte populations or communities are commonly based on inferences drawn from standardized toxicity tests conducted on floating non-rooted Lemna species, or submerged-rooted Myriophyllum species. These tests follow strict guidelines to produce reliable and robust results with legal credibility for environmental regulations. However, results and inferences from these tests may not be transferrable to emergent macrophytes due to their different morphology and physiology. Emergent macrophytes of the genus Typha L. are increasingly used for assessing phytotoxic effects of environmental stressors, although standardized testing protocols have not yet been developed for this genus. In this review we present a synthesis of previous toxicity studies with Typha, based on which we evaluate the potential to develop standard toxicity tests for Typha spp. with seven selection criteria: ecological relevance to the ecosystem; suitability for different exposure pathways; availability of plant material; ease of cultivation; uniform growth; appropriate and easily measurable toxicity endpoints; and sensitivity toward contaminants. Typha meets the criteria 1–3 fully, criteria 4 and 5 partly based on current limited data, and we identify knowledge gaps that limit evaluation of the remaining two criteria. We provide suggestions for addressing these gaps, and we summarize the experimental design of ecotoxicology studies that have used Typha. We conclude that Typha spp. can serve as future standard test species for ecological risk assessments of contaminants to emergent macrophytes.
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This is the third and final report of a programme investigating border control for potential aquatic weeds in New Zealand. We investigate whether the 25 potential weed species identified in the Stage 2 report are present in New Zealand, evaluate the weed potential of Hygrophila polysperma, Hydrocotyle verticillata, Cabomba caroliniana and Saururus cernuus, recommend a protocol for the determination of aquatic plants as Unwanted Organisms, and review Import Health Standards relating to the importation of aquatic plants. Four potential aquatic weed species were confirmed in New Zealand: Butomus umbellatus, Typha laxmannii, T. latifolia and a Sagittaria species. These plants, excluding T. laxmannii, were recommended for eradication as they pose an immediate threat to aquatic habitats in New Zealand. Further investigation of the weed potential of T. laxmannii is recommended. None of the four were regarded as significant threats to natural ecosystems in New Zealand or recommended as candidates for Unwanted Organism status. A series of criteria were recommended for future determination of aquatic plants as Unwanted Organisms, including the use of the weed risk assessment model developed in Stage 1. The recommendations for aquatic plant imports include: divide imported plant material into risk categories and design an appropriate Import Health Standard for each; review protocols for post-entry quarantine inspectors to increase their awareness of potential pest plant imports; and review current legislation for the importation of plant material providing more incentives for the screening of new material entering New Zealand.
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Species identification and analysis of phylogenetic relationships within the genus Typha are difficult because of the high degree of variability among morphological characters and frequent interspecific hybridization. Traditionally, two sections (T. sect. Ebracteolatae and sect. Bracteolatae) have been recognized within the genus based on the presence or absence of bracteoles in the female flowers. The aims of this study were to reconstruct the phylogeny of Typha using DNA sequence data from nuclear LEAFY and three plastid regions, and to evaluate previous classifications. We sampled nine species from various regions that were each invariant at the molecular level. A parsimony consensus tree recovered three clades in the genus: clade I including T. angustifolia, T. elephantina, T. domingensis, and T. capensis; clade II including T. orientalis and T. laxmanni; and clade III comprising T. latifolia and T. shuttleworthii. Typha minima was found sister to the rest of the Typha species with maximal bootstrap support. The results do not support previous classifications of Typha. Character analysis showed that bracteole loss, spatulate stigma, lack of a gap between staminate and pistillate inflorescences, and monad pollen are derived characteristics in Typha.
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In northeastern North America, an important wetland invader is the cattail Typha × glauca, a hybrid of native Typha latifolia and introduced Typha angustifolia. Although intensively studied in localized wetlands around the Great Lakes, the distributions of the hybrid and its parental species across broad spatial scales are poorly known. We obtained genotypes from plants collected from 61 sites spanning two geographical regions. The first region, near the Great Lakes and St. Lawrence Seaway (GLSL), has experienced substantial Typha increases over the last century, whereas more modest increases have occurred in the second region across Nova Scotia, New Brunswick, and Maine (NSNB). We found that hybrids predominate in the GLSL region, thriving in both disturbed and undisturbed habitats, and are expanding at the expense of both parental species. In contrast, the native T. latifolia is by far the most common of the three taxa across all habitat types in the NSNB region. We found no evidence that the formation of backcrossed and advanced-generation hybrids is limited by the reproductive barriers that are evident in F1 hybrids. However, although backcrossed individuals arise in both regions, they are much less common than F1 hybrids, which may explain why the parental species boundary remains. We conclude that F1 hybrids are playing a key role in the invasion of wetlands in the GLSL region, whereas their low frequency in the NSNB region may explain why Typha appears to be much less invasive further east. An improved understanding of these contrasting patterns of distribution is necessary before we can accurately predict future wetland invasions.
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The full effects of biological invasions may be underestimated in many areas because of cryptogenic species, which are those that can be identified as neither native nor introduced. In North America, the cattails Typha latifolia, T. angustifolia, and their hybrid T. × glauca are increasingly aggressive invaders of wetlands. There is a widespread belief that T. latifolia is native to North America and T. angustifolia was introduced from Europe, although there has so far been little empirical support for the latter claim. We used microsatellite data and chloroplast DNA sequences to compare T. latifolia and T. angustifolia genotypes from eastern North America and Europe. In both species, our data revealed a high level of genetic similarity between North American and European populations that is indicative of relatively recent intercontinental dispersal. More specifically, the most likely scenario suggested by Approximate Bayesian Computation was an introduction of T. angustifolia from Europe to North America. We discuss the potential importance of our findings in the context of hybridization, novel genomes, and increasingly invasive behaviour in North American Typha spp.
Rapid evolution following interspecific hybridization can facilitate biological invasions. Around the Great Lakes in North America, the hybrid cattail Typha × glauca is dominating wetlands and displacing both parental species. We measured water depth and height of T. × glauca and its parental species (Typha angustifolia and Typha latifolia) throughout the growing season at a site near Lake Ontario that harbors both parental species plus hybrids. We found no evidence of niche partitioning by water depth, nor was there evidence that water depth was influencing plant height. At the beginning of the growing season, T. latifolia comprised the tallest plants, but this potential advantage was short-lived, and for most of the growing season, F1 hybrids were taller than all or most other taxa (T. angustifolia, T. latifolia, and advanced-generation/backcrossed hybrids). Heterosis, inferred from height, is therefore evident in F1 hybrids, but not in advanced-generation/backcrossed hybrids. Typha stands often achieve high densities, and the competitive advantage of superior height is likely contributing to the invasive success of T. × glauca F1 hybrids in the Great Lakes region.
Alien aquatic plant species cause serious ecological and economic impacts to European freshwater ecosystems. This study presents a comprehensive overview of all alien aquatic plants in Europe, their places of origin and their distribution within the 46 European countries. In total, 96 aquatic species from 30 families have been reported as aliens from at least one European country. Most alien aquatic plants are native to Northern America, followed by Asia and Southern America. Elodea canadensis is the most widespread alien aquatic plant in Europe, reported from 41 European countries. Azolla filiculoides ranks second (25), followed by Vallisneria spiralis (22) and Elodea nuttallii (20). The highest number of alien aquatic plant species has been found in Italy and France (34 species), followed by Germany (27), Belgium and Hungary (both 26) and the Netherlands (24). Even though the number of alien aquatic plants seems relatively small, the European and Mediterranean Plant Protection Organization (EPPO, has listed 18 of these species as invasive or potentially invasive within the EPPO region. As ornamental trade has been regarded as the major pathway for the introduction of alien aquatic plants, trading bans seem to be the most effective option to reduce the risk of further unintended entry of alien aquatic plants into Europe.
A recent increase in the abundance of cattails (Typha spp.) in North American wetlands has been anecdotally linked with hybridization between Typha latifolia and Typha angustifolia. In this study, we used molecular genetic markers (microsatellites) to investigate whether the hybrid lineage (Typha × glauca) is restricted to The Great Lakes region, or exists across a much broader spatial scale. We also investigated the possibility of backcrossing and genetic introgression in natural populations. Parental species could be distinguished from one another based on the distribution of alleles at six microsatellite loci. Species identification based on genetic data corresponded well with species identifications based on leaf width, a key morphological trait that can distinguish the two parental species. We found that hybrids occur in Ontario, Quebec, New Brunswick, and Nova Scotia, but we did not detect hybrids in Maine. F1s are more abundant than backcrossed or intercrossed hybrids, although we also found evidence of backcrossing, particularly in Ontario. This indicates that hybrids are fertile, and are therefore potential conduits of gene flow between the parental species. Further work is needed to determine whether T. × glauca is particularly successful in the Great Lakes region relative to other areas in which the two parental species co-exist, and to assess whether introgression may lead to increased invasiveness in the species complex.