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Critical Reviews in Plant Sciences
ISSN: 0735-2689 (Print) 1549-7836 (Online) Journal homepage: http://www.tandfonline.com/loi/bpts20
The Worldwide Spread, Success, and Impact of
Ragweed (Ambrosia spp.)
C. Montagnani, R. Gentili, M. Smith, M. F. Guarino & S. Citterio
To cite this article: C. Montagnani, R. Gentili, M. Smith, M. F. Guarino & S. Citterio (2017) The
Worldwide Spread, Success, and Impact of Ragweed (Ambrosia spp.), Critical Reviews in Plant
Sciences, 36:3, 139-178, DOI: 10.1080/07352689.2017.1360112
To link to this article: http://dx.doi.org/10.1080/07352689.2017.1360112
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The Worldwide Spread, Success, and Impact of Ragweed (Ambrosia spp.)
C. Montagnani
a
, R. Gentili
a
, M. Smith
b
, M. F. Guarino
a
, and S. Citterio
a
a
Department of Earth and Environmental Sciences, University of Milano-Bicocca, Milano, Italy;
b
Institute of Science and the Environment,
University of Worcester, Worcester, UK
ABSTRACT
The Ambrosia species represent one of the most problematic groups of invasive weeds around the
world. The ease with which they are introduced and spread in new countries, their generalist
ecological requirements, and functional traits facilitate their invasion and subsequent naturalization
in new areas. All of these aspects contribute to increasing their global social and economic impact,
which is mostly related to pollen allergy. Here we analyze available scientific publications about
Ambrosia artemisiifolia, A. psilostachya, A. tenuifolia, and A. trifida, with the aim of defining the
current level of knowledge and summarizing important data that are currently scattered
throughout the literature. Specifically, we analyzed the following: (1) their current global
distribution and current stage of invasion; (2) traits and requirements promoting their introduction,
reproductive success, and adaptation to climate and environment in the nonnative range; as well as
(3) current knowledge about allergens and elements increasing their impact.
KEYWORDS
Ambrosia artemisiifolia;A.
psilostachya;A. tenuifolia;A.
trifida; invasive alien plants;
pollen allergy
I. Introduction
There are over 40 species in the genus Ambrosia L.
(Asteraceae) (Rich, 1994; Makra et al.,2015;www.the
plantlist.org), most of which are native to the Americas.
Over the last 200 years, human impacts on land use
(i.e. urbanization, the intensification of farming practi-
ces, and increased transportation networks) have had
serious effects on the distribution and ecology of several
Ambrosia species, in particular, the introduction of the
following species in nonnative continents: A. artemisiifo-
lia L. (common or short ragweed), A. trifida L. (giant
ragweed), A. tenuifolia Spreng. (slender or slim-leaf burr
ragweed), and A. psilostachya DC. (Western or perennial
ragweed).
These Ambrosia (ragweed) species have been intro-
duced into new countries since the 19th century, espe-
cially A. artemisiifolia which has quickly become an
invasive species (Smith et al.,2013 and references
therein) and is presently a species of concern for
public health in both its native and invasive ranges
because of its highly allergenic pollen. In North Amer-
ica, Ambrosia pollen is the second most important
cause of seasonal allergic rhinitis and asthma, affecting
more than 15 million people (about 20% to 25% of the
United States population), with a prevalence of about
45% in atopic individuals (Wopfner et al.,2005;Kats
and Carey, 2014). In Europe, Ambrosia has become a
serious problem in the past decades, contributing to
an evident increase in respiratory allergic reactions in
areas where it is distributed (D’Amato, 1992;D’Amato,
2007). It is therefore recognized globally that the
Ambrosia species represent one of the most problem-
atic groups of invasive weeds.
Biological invasions can be represented as a chrono-
logical series of decisive stages that can allow or halt the
entry and establishment of an organism in a new range
(Blackburn et al.,2011; Richardson and Pysek, 2012). A
nonnative organism needs to overcome geographical,
environmental, and reproductive barriers to establish
itself in a new area; and some factors and traits can be
more meaningful than others in predicting or explain-
ing its success or failure during the process of introduc-
tion, establishment, and spread (Van Kleunen et al.,
2015). Expressing the invasion process formulaically
as “introduction–naturalization–invasion continuum,”
Richardson and Pysek (2012) stressed the importance
of focusing on “naturalization,”which is the fundamen-
tal preliminary step before invasion. According to their
review, this “naturalization”is understudied, but its
predictors/mediators can be more robust than those
CONTACT C. Montagnani chiara.montagnani@unimib.it Department of Earth and Environmental Sciences, University of Milano-Bicocca, Piazza della
Scienza 1, 20126 Milano, Italy.
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/bpts.
© 2017 Taylor & Francis
CRITICAL REVIEWS IN PLANT SCIENCES
2017, VOL. 36, NO. 3, 139–178
https://doi.org/10.1080/07352689.2017.1360112
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formulated for the invasion phase as they depend on
factors less unpredictable and highly context-dependent.
On this basis, our review examines the main predic-
tors of introduction-naturalization of the most wide-
spread Ambrosia species at a global level, considering the
environmental requirements and traits discussed and
reported in scientific literature. After starting with a brief
description of the taxa considered, this review then fol-
lows the logical sequence of the continuum in order to
examine factors and traits involved in overcoming:
Geographical barriers: Mediators of the introduction
of species into new areas: native extent of occur-
rence, pathways of introduction, and their effective-
ness in terms of space (extent of the invasive range)
and time (protraction of invasion).
Environmental barriers: Predictors of the likelihood
of persistence of Ambrosia species: environmental
and climatic (broad-scale) matching between
native and invasive range, requirements and toler-
ance to the main environmental abiotic factors
(temperature, soil, light) in sensitive phases of the
life cycle, resilience (strategies) to disturbances and
competition.
Reproductive and dispersal barriers: Predictors of
successful propagation and spread of species, such
as: specific pollinators, reproduction and dispersal
strategies, propagule pressure.
The review ends with an overview of the allergenic
impact of ragweed and how environmental factors and
plant traits influence the magnitude of pollinosis.
II. Literature screening
Google Scholar, Web of Science and Scopus databases
were consulted to identify scientific literature about the
genus Ambrosia. However, given the availability of inter-
esting information in additional web repositories,
technical reports and online databases (national/regional
floras, CABI, IUCN, EPPO, DAISIE, HEAR) were
examined.
III. Species considered and their description
The Ambrosia species considered in this review are
presently introduced in more than ten countries: A.
artemisiifolia, A. trifida, A. psilostachya,andA. tenui-
folia. All taxa are herbaceous or slightly suffruticose
species. A. artemisiifolia and A. trifida are annual
plants, while A. psilostachya and A. tenuifolia are per-
ennials. Besides the presence of different below-ground
organs, diagnostic elements are mainly leaves, whose
shape and clefts, as well as the presence of petioles, are
useful in identifying different species. Leaves are
variously pubescent or glaborous. They are monoic
species with inflorescences of unisexual heads. All taxa
produce1-seededcypselaeanditssizeandcoatorna-
ments may differ: A. trifida produces the biggest seeds
and, among other species, spines may differ in number
and bluntness.
A. trifida is an easily identifiable taxon, whose height
(up to 4 m) and shape of leaves are unmistakable. How-
ever, the determination of other taxa can often be hard
owing to a high variability in leaf or seed shape. Further-
more, the taxonomy is complicated by the possible
presence of hybrids between A. artemisiifolia and
A. psilostachya (A. £intergradiens; Wagner and Beals,
1958) and A. artemisiifolia and A. trifida (Ambrosia £
helenae; Wagner, 1958; Strother, 2006).
Recently, the SMARTER project (COST Action
FA1203) brought together a European team of botanists
from different countries who reviewed the discriminat-
ing characters among species to provide a proper key of
identification; as the most recent and reliable source,
their findings relevant for this section are summarized in
Table 1. Ambrosia species characteristics: morphological data allowing the identification of the four ragweeds.
Species Ambrosia artemisiifolia L. Ambrosia trifida L. Ambrosia psilostachya DC Ambrosia tenuifolia Spreng
Life form Annual Annual Perennial Perennial
Plant size (cm) 10–250 40–400 10–90 20–100
Below-ground Taproot Taproot Root sprouter Root sprouter
Stem C/¡intensively branched,
branches with wide angles
C/¡intensively
branched
Few branches, with narrow
angles
Few branches, with narrow
angles
Leaves Pinnatifid to bipinnate, rarely
entire; leaf segments broadened
and separated, rarely narrow;
lower leaves with distinct
narrow petiole; upper leaves
alternate; long and short hairs
mixed
Palmate, 1–5 lobes;
glabrous or few short
hairs; all leaves
opposite
Pinnatifid, rarely entire; leaf
segments lineal and
connected, often sharped
toward the tip; C/¡sessile;
upper leaves alternate; dense
short hairs
Bipinnate to pinnatifid; leaf
segments as narrow as the
rachis, lineal, connected;
lower leaves with distinct
narrow petiole; upper
leaves alternate; dense
short hairs
Diaspore coat Few hairs and glands; 2–5 short
lateral spines with sharpened
tips; dark brown
Glabrous or few hairs; 2–4
indistinct lateral
spines; dark brown to
black
Few glands and short hairs;
blunt, short lateral spines few
or none; dark brown
Short hairs and glands, 2–5
lateral short blunt spines;
olive to dark brown
140 C. MONTAGNANI ET AL.
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Table 1 and they are also available at http://international
ragweedsociety.org/
IV. Geographical barriers
Geographical barriers are the first obstacle an organ-
ism has to overcome before reaching a new range
(Richardson et al.,2000;Blackburnet al.,2011). All
the taxa considered here are native to the Americas,
where the highest number of species of the genus
have occurred: the genus appears to have originated
and diversified from arid and semi-arid regions in
Southwestern North America (Payne, 1970;Gerber
et al.,2011).
From the current distribution of ragweed, it is clear
that these species have often successfully crossed the
natural borders of their broad native ranges (Figure 1).
Pathways of introduction are linked to involuntary
human actions and the flux of propagules has been in
operation for at least a century. Here the pathways of
introduction from native to invasive ranges are explained
and the present global distribution is discussed, starting
from a description of the native environments of the
single species.
A. Native range
A. artemisiifolia is native to North America and is pres-
ently widespread in the United States and Canada except
for Yukon and Nunavut (Strother, 2006; Essl et al.,
2015). In its native area, it was first recorded before 1838
in the United States (Kazinczi et al.,2008) and in 1822 in
Canada (Bassett and Crompton, 1975; Mitich, 1996;
Lavoie et al.,2007). It is, however, difficult to understand
its primitive range of distribution because its spread has
been human-mediated for a long time (McAndrews,
1988). According to Basset and Crompton (1982) the
species spread widely with the increase of settlements of
white men in North America. As a consequence of this,
and due to taxonomic disagreements, there are several
incongruities among floras about the native or intro-
duced status of A. artemisiifolia in a number of coun-
tries, especially Central and South America (Figure 1).
Like A. artemisiifolia, A. trifida is native to North
America. According to Bazzaz (1979), it was found in
repeatedly disturbed ground only in the Midwestern and
Eastern United States. However, based on more recent
sources, A. trifida occurs in a wider range, covering
almost all of United States (except for Nevada) and
Canada (except for the Northwest Territories, Nunavut,
and Yukon (Strother, 2006); it moved into Canada from
the South, following the retreat of the last glacial ice
(Figure 1) (Bassett and Crompton, 1982).
A. psilostachya is also native to Western North
America. As with A. trifida, it migrated to Canada after
the glacial retreat, colonizing the Eastern Canada, where
it has been present for a considerable time (Figure 1)
(Mitich, 1996). Bovey (1966) confirmed that A. psilosta-
chya is widely distributed from California, Texas, Mex-
ico, Idaho, and Saskatchewan eastward to Illinois and
Louisiana, on pasture land in Nebraska but especially in
the Rocky Mountain States (Bovey, 1966). According to
Strother (2006), its native range in the United States
includes almost all states (except for Maryland,
Delaware, and New Jersey) and the southern part of
Canada (from Columbia to Nova Scotia and
Newfoundland).
In contrast to the other three species, A. tenuifolia is
native to temperate South American countries, particu-
larly Brazil, Paraguay, Uruguay, Argentina, and probably
Per
u(Figure 1) (Randall, 2012).
B. From native to invasive range: Pathways
of introduction
Due to their ethnobotanical value, Ambrosia spp. have
been used in traditional medicine since ancient times. In
North and Central America, A. artemisiifolia, A. psilosta-
chya, and A. trifida were medicinal plants for native
Americans (Chamberlin, 1911; Shemluck, 1982;
Mamedov et al.,2015) and today some of them are still
used (i.e. A. psilostachya, see Gioanetto et al.,2010).
Moreover, A. trifida was domesticated by indigenous
North Americans, who collected and planted seeds
mainly for alimentary purposes (Simon, 2009; Jurney,
2012), In South America, predominantly in the Southern
Cone, A. tenuifolia has also been a traditional medicinal
plant (Mongelli et al.,1996; Del Vitto, 1997; Trillo et al.,
2014). Thus, owing to the long-lasting utilization of
ragweed in traditional medicine and uses, it is likely that
European colonizers carried seeds to their countries by
growing plants in botanical gardens (Essl. et al.,2015).
However, the scientific or ethnobotanical interest was
probably not the main root of introduction for these spe-
cies, as the amounts of seeds or plants moved were small.
Ragweed plants are not suitable for flower market
trading or collection, and so it is likely that their massive
expansion followed involuntary human pathways.
Today, owing to the frequency and abundance of
ragweeds in anthropic environments in their native
range, it is widely accepted that seeds and/or propagules
of plants have been unintentionally transported outside
the Americas by human activities along trade routes.
The introduction of A. artemisiifolia into different
parts of the world has been ascribed to contaminated
seed lots of grain, vegetables (e.g. potatoes), seed for
CRITICAL REVIEWS IN PLANT SCIENCES 141
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forage or oil-seeds (e.g. sunflower) (Genton et al.,2005;
Chauvel et al.,2006; Smith et al.,2013; Essl et al.,2015)
and also seed found in bird food (Brandes and Nitzsche,
2006; Frick et al.,2011), fodder, ship ballasts, and
military movements (Kazinczi et al.,2008; Gaudeul
et al.,2011). During the 20th century, particularly during
the World Wars, A. artemisiifolia was introduced into
Europe principally through agricultural products from
several North American sources. Based on molecular
studies, repeated introductions occurred during the inva-
sion in different parts of the new range (Genton et al.,
2005; Kiss and B
eres, 2006; Gaudeul et al.,2011; Hodgins
and Rieseberg, 2011; Smith et al.,2013; Ciappetta et al.,
2016).
The seeds of A. artemisiifolia were not the only
ragweed species to follow such routes. Frick et al. (2011)
Figure 1. Global distribution of Ambrosia species (ragweeds). Alien: the species is not native to a country. Status (invasive, naturalized,
and casual) is attributed when the condition is confirmed at country and/or local level; “?”indicates uncertainty due to lack of confir-
mations. Alien status unknown: the species is alien to a country, but its status is indefinite. Species occurring: the species occurs in one
country, but there are uncertainties/inconsistencies about its origin (alien/native). Native: the species is not introduced from other
countries; it is part of local flora. Doubtful occurrence: the occurrence of the species is not confirmed.
142 C. MONTAGNANI ET AL.
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showed that Ambrosia sp. seeds, including A. artemisiifo-
lia as well as other ragweed species, occur in 21% to 75%
of the bird feed products available on the German,
Hungarian, and Danish markets. For instance, A. trifida
was introduced by imports of commercial grain and oil-
seed, e.g. between North America and European coun-
tries, which repeatedly ensured the reinforcement of
populations into new areas (Follak et al.,2013). Military
movements during World War II were also vectors of
introduction for A. trifida in several sites in Northern
Italy (Ardenghi and Polani, 2016).
The mechanism of introduction into the invasive
range of A. psilostachya and A. tenuifolia was likely the
same as those mentioned previously (Makra et al.,
2015). Data from Moskalenko (2001) and CABI (2017)
revealed that Russian cereals coming from Canada were
contaminated by seeds of A. psilostachya. Verloove
(2016b) ascribed the arrival of A. psilostachya in
Belgium to the American forces during the World
War I, while Parsons and Cuthbertson (2001) under-
lined the contribution of United States’military move-
ments during World War II to the spread of A.
psilostachya in Australia and other parts of the world.
These latter assumptions were mainly based on the fact
that the species was unknown before the arrival of US
troops. On the other hand, A. tenuifolia, was mentioned
(Nelson, 1917)asa“ballast-plant,”a species involuntary
transported in solid sailing ballasts (currently replaced
by water ballasts) and then released in new countries
during the de-ballasting phase. This pathway was
inferred by the author after the finding of A. tenuifolia
and other nonnative species in dumping areas near har-
bors in Oregon; nevertheless, this route is also plausible
if past transoceanic travels to Europe are considered
(Thellung, 1912). In any case, at present, the pathways
of introduction of A. psilostachya and A. tenuifolia are
less clear than those of A. artemisiifolia, given the few
studies available. Moreover, considering that the species
have different dispersal strategies, additional vectors
should be taken into consideration. Specifically, the
reproduction strategy of A. psilostachya is mainly vege-
tative and the amount of seeds produced is quite small.
Thus, the role of alternative propagules (i.e. rhizomes)
and different vectors in the global spread of the taxon
should be considered in defining reliable pathways of
introduction.
C. Global distribution: Current status and
invasion history
Vectors for the spread of ragweed work in very effective
ways. The percentage of countries where the species are
native or alien and their status (casual, naturalized, or
invasive) are shown in Figure 2.Figure 2 was developed
according to the database reported in Table 2.
At the moment three species out of four (A. artemisii-
folia, A. psilostachya, A. tenuifolia) are present in every
continent and the fourth (A. trifida) has colonized all
continents except for Africa and Oceania. In its nonna-
tive range, A. artemisiifolia occurs in eighty countries
(including those where its native status is uncertain) and
it is classified as invasive in 32% of them. A. psilostachya
is alien in almost forty countries; but, although it is natu-
ralized in at least fourteen countries representing 36% of
its nonnative range, only in seven (19%) countries does
it show invasive behavior. Also A. trifida has colonized
almost forty countries, but it is included among invasive
plants only in three of these (one doubtful), representing
7% of the total. To date, A. tenuifolia appears not to be
an invasive taxon in its nonnative range, consisting of
fewer than fifteen countries, but it is naturalized in over
half of the range of introduction (64%).
Without considering its cultivation in botanical gar-
dens, which dates back to the 18thcentury, the first
record of A. artemisiifolia outside its native range comes
from the United Kingdom, where the species was
recorded as casual in 1836 (Essl et al.,2015). Then, in
1854, it was found in the Hawaiian Islands (Wagner
et al.,1990) and in the same decade it was recorded again
in Europe, in Switzerland (Bullock et al.,2012). Later, in
1860 and 1863, it was found respectively in Germany
(Brandes and Nitzsche, 2006) and France (Chauvel et al.,
2006) (Western Europe). In all these countries the spe-
cies is still present. The native or alien status of A. arte-
misiifolia is uncertain in many countries in the
Americas. Essl et al. (2015) asserted that A. artemisiifolia
is surely alien to Argentina, Chile, Brazil, Bahamas, and
the island of Hispaniola. Villase~
nor and Espinosa-Garcia
(2004) listed A. artemisiifolia among the alien species in
Mexico, while for Cuban populations there are clearly
uncertainties (Acevedo-Rodrıguez and Strong, 2012).
Going back to Europe, from the second half of the 19th
century onwards, the species has rapidly spread over all
the continent. Records of A. artemisiifolia in Northern
countries are later than Germany and France: Denmark
in 1865 (Bullock et al.,2012) and Sweden in 1866
(Anderberg, 2000a). In Eastern Europe, it appeared in
1873 in Poland (Tokarska-Guzik et al.,2011) and
10 years later in the Czech Republic (Bullock et al.,
2012). In Southern Europe the first signs of introduction
probably occurred in 1879 in Croatia (Galzina et al.,
2010) and then in Italy (1902; Gentili et al.,2016). Newly
colonized countries have continued to be recorded in
recent times also (e.g. Greece) (Greuter and Raus, 2008).
Concerning Asia, the first record dates back to 1877
and is from Japan, where A. artemisiifolia was found as a
CRITICAL REVIEWS IN PLANT SCIENCES 143
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casual (naturalization stage was recorded around 1925;
https://www.nies.go.jp/biodiversity/invasive/DB/detail/
80400e.html), while in China the species was found later
(1930s) (Qin et al.,2014). The invasive behavior of A.
artemisiifolia was reported by Washitani (2004) as begin-
ning in the 1960s. In Taiwan, South Korea, and Turkey,
A. artemisiifolia was found later in the 1990s, whereas in
other Asian countries (e.g. Armenia, Kazakhstan, Iran
and India) information about when they were introduced
is not available.
In other parts of the world, Qu
ezel and Santa (1963)
reported the presence of A. artemisiifolia in Africa in
Algerian flora and Lawlree (1947) asserted that the spe-
cies was found there later than 1890. The species was
recorded in other African countries more recently and,
at the moment, it is also naturalized in Egypt (Boulos,
2002). Moreover it appears that the species is expanding
toward Southern Africa (Botswana, South Africa, and
Swaziland) (Setshogo, 2005; Henderson, 2007; Randall,
2012; Swaziland’s Alien Plants Database at: http://www.
sntc.org.sz/alienplants/index.asp). Skalova et al. (2015)
also reported the presence of A. artemisiifolia in Mada-
gascar, while Kull et al. (2012) mention only A. maritima
as an introduced and naturalized taxon on the island.
Figure 2. Status of Ambrosia species (ragweeds) at world level. Each pie chart describes the percentage of countries where the species is
native or alien, their status and the table below the numbers for each category.
144 C. MONTAGNANI ET AL.
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Table 2. Geography of Ambrosia (ragweed) species: distribution, time of arrival (first record in the wild), current status of ragweeds, and
references supporting reported data.
Continent Country Species First record Status References
Europe Albany Ambrosia artemisiifolia L. —Doubtful occurrence Barina et al. (2013,2014)
Africa Algeria A. artemisiifolia >1890 Alien Casual Lawalree (1947), Qu
ezel and Santa (1963),
and Greuter (2006)
Africa Algeria A. psilostachya DC. 1916 Alien Naturalized Maire (1928), Qu
ezel and Santa (1963),
and Greuter (2006)
America (S) Argentina A. artemisiifolia —Species occurring Freire et al. (2008), Gerber et al. (2011),
and Essl et al. (2015)
America (S) Argentina A. tenuifolia Spreng. —Native Freire et al. (2008) and Novara and
Guti
errez (2010)
Asia Armenia A. artemisiifolia —Alien Naturalized Tamanyan and Fayvush (2010) and
Randall (2012)
Oceania Australia A. artemisiifolia 1908 Alien Invasive Parsons and Cuthbertson (2001) and Essl
et al. (2015)
Oceania Australia A. psilostachya 1922 Alien Invasive Parsons and Cuthbertson (2001)
Oceania Australia A. tenuifolia 1932 Alien Naturalized Parsons and Cuthbertson (2001)
Europe Austria A. artemisiifolia 1883 Alien Invasive Essl et al. (2009) and Smith et al. (2013)
Europe Austria A. trifida L. 1948 Alien Casual Essl and Rabitsch (2002) and Follak et al.
(2013)
Europe Austria A. psilostachya —Alien Casual Essl and Rabitsch (2002)
Asia Azerbaijan A. artemisiifolia —Alien Invasive Greuter (2006) and Gerber et al. (2011)
America (C) Bahamas A. artemisiifolia —Species occurring Acevedo-Rodrıguez and Strong (2012) and
Essl et al. (2015)
Europe Belarus A. artemisiifolia —Alien Naturalized Greuter (2006)
Europe Belarus A. psilostachya —Alien status unknown EPPO (2016)
Europe Belarus A. trifida —Alien Casual EPPO (2016)
Europe Belgium A. trifida 1829 Alien Casual Verloove (2016a)
Europe Belgium A. psilostachya 1917 Alien Naturalized Verloove (2016b)
Europe Belgium A. artemisiifolia 1883 Alien Naturalized? Bullock et al. (2012) and Verloove (2016c)
America (S) Bolivia A. artemisiifolia —Alien status unknown Jørgensen et al. (2014)
America (S) Bolivia A. tenuifolia —Native Jørgensen et al. (2014)
Europe Bosnia Herzegovina A. artemisiifolia —Alien status unknown Kazinczi et al. (2008) and Smith et al.
(2008)
Africa Botswana A. artemisiifolia —Alien Naturalized Setshogo (2005), Randall (2012), and
Skarpe et al. (2014)
America (S) Brazil A. artemisiifolia —Species occurring Mondin and Nakajima (2015), Essl et al.
(2015), and Alves and Rocha (2016)
America (S) Brazil A. tenuifolia —Native S
aenz and Guti
errez (2008)
Europe Bulgaria A. artemisiifolia 1975 Alien Naturalized Kazinczi et al. (2008) and Bullock et al.
(2012)
Europe Bulgaria A. trifida 2014 Alien status unknown Stoyanov et al. (2014)
America (S) Canada A. artemisiifolia —Native Bassett and Crompton (1975) and Kazinczi
et al. (2008)
America (N) Canada A. psilostachya —Native Bassett and Crompton (1975)
America (N) Canada A. trifida —Native Bassett and Crompton (1982)
America (S) Chile A. artemisiifolia 1959 Alien Naturalized Essl et al. (2015), Ugarte et al. (2011), and
Fuentes et al. (2013)
America (S) Chile A. tenuifolia 1923 Alien Naturalized? Ugarte et al. (2011)
Asia China A. artemisiifolia 1930s Alien Invasive Qin et a. (2014)
Asia China A. trifida 1935 Alien Invasive Qin et a. (2014)
Asia China A. psilostachya —Alien status unknown Chen and Hind (2011)
America (S) Colombia A. artemisiifolia —Species occurring Gerber et al. (2011) and CABI (2017)
Europe Croatia A. artemisiifolia 1879 Alien Invasive Galzina et al. (2010), Csontos et al. (2010),
and Kazinczi et al. (2008)
America (C) Cuba A. artemisiifolia <1873 Species occurring Sauvalle Chanceaulme (1873) and
Acevedo-Rodriguez and Strong (2012)
Europe Czech Republic A. artemisiifolia 1883 Alien Invasive Kazinczi et al. (2008), Smith et al. (2008),
and Bullock et al. (2012)
Europe Czech Republic A. trifida 1960 Alien Casual Py
sek et al. (2012)
Europe Czech Republic A. psilostachya 1999 Alien Casual Py
sek et al. (2012)
Europe Denmark A. psilostachya —Alien Casual Greuter (2006)
Europe Denmark A. trifida —Alien Casual EPPO (2016)
Europe Denmark A. artemisiifolia 1865 Alien Casual Bullock et al. (2012)
America (S) Ecuador A. artemisiifolia —Species occurring Jørgensen and Le
on-Y
anez (1999)
America (S) Ecuador (Galapagos) A. artemisiifolia —Alien Casual Tye (2001) and Jaramillo D
ıaz and Gu
ezou
(2013).
Africa Egypt A. artemisiifolia 2002? Alien Naturalized Greuter (2006) and Shaltout (2004).
Europe Estonia A. artemisiifolia 1954 Alien Casual Gudzinskas (1993)
Europe Estonia A. psilostachya —Alien Casual Greuter (2006)
Europe Estonia A. trifida —Alien Casual EPPO (2016)
(Continued on next page)
CRITICAL REVIEWS IN PLANT SCIENCES 145
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Table 2. (Continued).
Continent Country Species First record Status References
Europe Finland A. artemisiifolia 1900<1950 Alien Naturalized Finnish Ministry of Agriculture and
Forestry (2012) and Lampinen and
Lahti (2016)
Europe Finland A. trifida 1900<1950 Alien status unknown Lampinen and Lahti (2016)
Europe Finland A. psilostachya 1990s Alien status unknown Lampinen and Lahti (2016)
Europe France A. tenuifolia 1839 Alien Naturalized Thellung (1912) and Chauvel et al. (2015)
Europe France A. artemisiifolia 1863 Alien Invasive [Corse-
Alien Casual]
Chauvel et al. (2006) and Csontos et al.
(2010)
Europe France A. trifida 1901 Alien Naturalized Chauvel et al. (2015)
Europe France A. psilostachya 1931 Alien Naturalized
(Invasive?)
Hibon (1942) and Fried et al. (2015)
Asia Georgia A. artemisiifolia —Alien Invasive Kikodze et al. (2010) and EPPO (2016)
Asia Georgia A. trifida —Alien status unknown Kikodze et al. (2010)
Europe Germany A. artemisiifolia 1860 Alien Naturalized Buttler and Harms (1999), Brandes and
Nitzsche (2006), Otto (2006), Kazinczi
et al. (2008), Bullock et al. (2012), and
Buttler (2016).
Europe Germany A. trifida 1877 Alien Naturalized Buttler and Harms (1999), Follak et al.
(2013), Buttler (2016); DAISIE, Species
Factsheet: A. trifida. available at http://
www.europe-aliens.org/speciesFact
sheet.do?speciesIdD21722# (Accessed
in January 2017); Deutschlandflora
WebGIS. Floristische
Verbreitungskarten in Deutschland:
https://deutschlandflora.de (Accessed
in January 2017)
Europe Germany A. psilostachya 1897 Alien Naturalized Buttler and Harms (1999), Buttler (2016),
Bundesamt f€
ur Naturschutz –Floraweb
(2017): http://www.floraweb.de/pflan
zenarten/artenhome.xsql?suchnrD20
068& (Accessed in January 2017);
Deutschlandflora WebGIS. Floristische
Verbreitungskarten in Deutschland:
https://deutschlandflora.de (Accessed
in January 2017)
Europe Germany A. tenuifolia —Alien Casual Buttler and Harms (1999) and Buttler
(2016)
Europe Greece A. psilostachya 2016 Alien Naturalized? Von Raab-Straube and Raus (2016)
Europe Greece A. artemisiifolia 2008? Alien status unknown Arianoutsou et al. (2010) and Greuter and
Raus (2008)
America (C) Guadeloupe A. artemisiifolia —Alien status unknown Gerber et al. (2011)
America (S) Guatemala A. artemisiifolia —Alien status unknown Gerber et al. (2011)
America (C) Hawaiian Islands A. artemisiifolia 1854 Alien Invasive Wagner et al. (1990) and Pacific Island
Ecosystems at Risk (PIER) (2013a)
America (N) Hawaiian Islands A. psilostachya —Alien status unknown Randall (2012) and Pacific Island
Ecosystems at Risk (PIER) (2013b)
America (C) Hispaniola (Dominican
Republic)
A. artemisiifolia —Species occurring Acevedo-Rodrıguez and Strong (2012) and
Essl et al. (2015)
Europe Hungary A. psilostachya 1900ca. Alien Invasive Puc (2004) and CABI (2017)
Europe Hungary A. trifida —Alien Invasive? Plank et al. (2016)
Europe Hungary A. artemisiifolia 1922 Alien Invasive Csontos et al. (2010)
Europe Iceland A. artemisiifolia 1948 Alien Casual Wasowicz et al. (2013)
Asia India A. artemisiifolia —Alien Invasive Khuroo et al. (2012) and Kohli et al. (2012)
Asia India A. psilostachya 1990s Alien Invasive Ramachandra Prasad et al. (2013)
Asia India A. trifida 2004–2009 Alien status unknown Kumar et al. (2009) and Randall (2012)
Asia Iran A. artemisiifolia —Alien status unknown Gerber et al. (2011), Randall (2012), and
Bararpour (2014).
Asia Iran A. psilostachya —Alien status unknown Cheraghian (2016a)
Asia Iran A. trifida —Alien status unknown Randall (2012), Bararpour (2014), and
Cheraghian (2016b)
Europe Ireland A. trifida 1894 Alien Casual Reynolds (2002)
Europe Ireland A. artemisiifolia 1900 Alien Casual Rich (1994), Reynolds (2002), Bullock et al.
(2012), and Essl et al. (2015)
Asia Israel A. artemisiifolia 1925 Alien Casual Waisel et al. (2008) and Yair et al. (2017)
Asia Israel A. tenuifolia 1984 Alien Naturalized Greuter and Raus (1995), Danin (2000),
Waisel et al. (2008), and Yair et al.
(2017)
Asia Israel A. trifida 1987 Alien Casual (still
present?)
Danin (2000), Waisel et al. (2008), Danin
(2016), and Yair et al. (2017)
(Continued on next page)
146 C. MONTAGNANI ET AL.
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Table 2. (Continued).
Continent Country Species First record Status References
Asia Israel A. psilostachya 2006 ca. Alien Naturalized Yair et al. (2017)
Europe Italy A. trifida 1899 Alien Naturalized Vignolo-Lutati (1935), Mandrioli et al.
(1998), Celesti-Grapow et al. (2009),
and Chauvel et al. (2015)
Europe Italy A. psilostachya 1927 Alien Invasive Vignolo-Lutati (1935), Mandrioli et al.
(1998), and Conti et al. (2005)
Europe Italy A. tenuifolia 1935 Alien Naturalized Vignolo-Lutati (1935), Mandrioli et al.
(1998), and Conti et al. (2005)
Europe Italy A. artemisiifolia 1902 Alien Invasive Gentili et al. (2016)
America (S) Jamaica A. artemisiifolia —Alien status unknown Gerber et al. (2011)
Asia Japan A. artemisiifolia 1877 Alien Invasive Auld et al. (2003), Kazinczi et al. (2008),
Fukano and Yahara (2012), Essl et al.
(2015); Invasive Species of Japan
(NIES). A. artemisiifolia. Available at:
https://www.nies.go.jp/biodiversity/
invasive/DB/detail/80400e.html
(Accessed January 2017)
Asia Japan A. trifida 1952 Alien Invasive Auld et al. (2003)
Asia Japan A. psilostachya —Alien Invasive Auld et al. (2003), Mito and Uesugi (2004),
and Ramachandra Prasad et al. (2013).
Asia Kazakhstan A. artemisiifolia —Alien status unknown Gerber et al. (2011)
Asia Kazakhstan A. psilostachya —Alien Naturalized Von Raab-Straube and Raus (2016).
Asia Korean Peninsula A. trifida 1964 Alien Invasive Lee et al. (2010) and Kim and Kil (2016)
Asia Korean Peninsula A. artemisiifolia 1955 Alien Invasive Song et al. (2012) and Kim and Kil (2016).
Europe Latvia A. trifida 1900 Alien Casual? Gudzinskas (1993)
Europe Latvia A. artemisiifolia 1936 Alien Casual Gudzinskas (1993)
Europe Latvia A. psilostachya —Alien Casual DAISIE, Species Factsheet: A. coronopifolia
available at http://www.europe-aliens.
org/speciesFactsheet.do?speciesId D2
1701# (Accessed in January 2017)
Europe Liechtenstein A. artemisiifolia 1995 Alien Casual Greuter (2006) and Waldburger and Staub
(2006)
Europe Lithuania A. trifida 1987 Alien Casual Gudzinskas (1993)
Europe Lithuania A. artemisiifolia 1884 Alien Casual Gudzinskas (1993)
Europe Luxembourg A. artemisiifolia —Alien Naturalized Ries (2017)
Africa Lybia A. artemisiifolia —Doubtful occurrence Greuter (2006)
Africa Madagascar A. artemisiifolia —Doubtful occurrence Kull et al. (2012) and Sk
alov
aet al. (2015)
America (C) Martinique A. artemisiifolia —Alien status unknown Gerber et al. (2011)
Africa Mauritius A. psilostachya —Alien Invasive Macdonald et al. (2003)
America (C) Mexico A. artemisiifolia —Species occurring Villase~
nor and Espinosa-Garcia (2004) and
Gerber et al. (2011)
America (C) Mexico A. psilostachya —Native Vibrans (1998) and Rold
an and Vibrans
(2009)
America (C) Mexico A. trifida —Species occurring Villase~
nor and Espinosa-Garcia (2004),
EPPO (2016), and CABI (2017)
Europe Moldova A. artemisiifolia 1975? Alien Naturalized Greuter (2006) and Bullock et al. (2012)
Europe Moldova A. trifida —Alien Casual EPPO (2016)
Asia Mongolia A. trifida —Alien status unknown EPPO (2016)
Europe Montenegro A. artemisiifolia ? Alien status unknown Ste
sevi
c and Petrovi
c(2010) and Karrer
(2016)
Europe Montenegro A. psilostachya —Alien status unknown Greuter (2006)
Africa Morocco A. psilostachya 1994 Alien status unknown Tanji (2005)
Europe Netherlands A. artemisiifolia 1875 Alien Naturalized Van Denderen et al. (2010) and Od
e and
Beringen (2017a)
Europe Netherlands A. psilostachya 1905 Alien Naturalized Van Denderen et al. (2010) and Od
e and
Beringen (2017b)
Europe Netherlands A. trifida more frequent
from 1960s
Alien Casual Van Denderen et al. (2010) and Od
e and
Beringen (2017c)
Oceania New Zealand A. tenuifolia 1950 Alien Casual Howell and Sawyer (2006)
Oceania New Zeland A. artemisiifolia 1911 Alien Casual Webb et al. (1988) and Essl et al. (2015)
Europe Norway A. artemisiifolia 1930 Alien Casual Fremstad and Elven (1997) and Kazinczi
et al. (2008)
Europe Norway A. psilostachya —Alien Casual Greuter (2006)
Europe Norway A. trifida —Alien Casual Randall (2012), EPPO (2016), CABI (2017);
DAISIE, Species Factsheet: A. trifida.
available at http://www.europe-aliens.
org/speciesFactsheet.do?speciesIdD
21722# (Accessed in January 2017)
(Continued on next page)
CRITICAL REVIEWS IN PLANT SCIENCES 147
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Table 2. (Continued).
Continent Country Species First record Status References
America (S) Paraguay A. artemisiifolia —Species occurring Zuloaga et al. (2008), Essl et al. (2015),
CABI (2017); Tropicos.org. Missouri
Botanical Garden. 1 February 2017
<http://www.tropicos.org/Name/
2701648
America (S) Paraguay A. tenuifolia —Native S
aenz and Guti
errez (2008)
America (S) Per
uA. artemisiifolia —Species occurring Gutte (1978), Gerber et al. (2011), Z
arate
et al. (2015); Tropicos.org. Missouri
Botanical Garden. 20 January 2017
<http://www.tropicos.org/Name/
2701648>
America (S) Per
uA. tenuifolia —Native Randall (2012)
Europe Poland A. artemisiifolia 1873 Alien Naturalized Gudzinskas (1993), Kazinczi et al. (2008),
and Tokarska-Guzik et al. (2011)
Europe Poland A. psilostachya —Alien Naturalized Kazinczi et al. (2008) and Tokarska-Guzik
et al. (2011)
Europe Poland A. trifida —Alien Casual Kazinczi et al. (2008) and Tokarska-Guzik
et al. (2011)
Europe Portugal A. artemisiifolia 1972 Alien Invasive (Isle of
Madeira Alien Casual)
Borges et al. (2008) and Amor Morales
et al. (2012)
America (C) Puerto Rico A. tenuifolia —Alien Naturalized Liogier (1997), Acevedo-Rodriguez and
Strong (2012), and Gann et al. (2015–
2017)
Europe Romania A. artemisiifolia 1907 Alien Invasive Kazinczi et al. (2008), Csontos et al. (2010),
Bullock et al. (2012), and S
^
ırbu (2012)
Europe Romania A. trifida 1970–1980 Alien Naturalized S
^
ırbu (2012) and Stoyanov et al. (2014)
Europe Romania A. psilostachya —Alien Naturalized S
^
ırbu (2012)
Europe Russia A. psilostachya —Alien Naturalized EPPO (2016)
Europe Russia (European) A. artemisiifolia 1918 Alien Invasive Gudzinskas (1993), Csontos et al. (2010),
Vinogradova et al. (2010), and Randall
(2012)
Europe Russia (European) A. trifida —Alien Naturalized Randall (2012) and EPPO (2016)
Europe Russia (European) A. psilostachya —Alien Naturalized EPPO (2016)
Europe Serbia A. artemisiifolia 1935 Alien Invasive Vrbni
canin et al. (2004), Kazinczi et al.
(2008), and Bullock et al. (2012)
Europe Serbia A. trifida 1982 Alien Naturalized Vrbni
canin et al. (2004), Follak et al.
(2013), and EPPO (2016)
Europe Serbia A. tenuifolia —Alien Naturalized Vrbni
canin et al. (2004)
Europe Slovakia A. artemisiifolia 1949 Alien Invasive Medvecka et al. (2012)
Europe Slovakia A. trifida 1980 Alien Casual Medvecka et al. (2012)
Europe Slovenia A. artemisiifolia 1993 (after WW
II?)
Alien Invasive Kazinczi et al. (2008), Galzina et al. (2010),
and Zelnik (2012)
Europe Slovenia A. trifida late 1980s Alien Casual Follak et al. (2013) and EPPO (2016)
Africa South Africa A. artemisiifolia —Alien Naturalized Germishuizen and Meyer (2003),
Henderson (2007), and Essl et al. (2015)
Africa South Africa A. psilostachya —Alien Naturalized Wells et al. (1986), Germishuizen and
Meyer (2003), Randall (2012), and
SANBI (2015a)
Africa South Africa A. tenuifolia —Alien Naturalized Germishuizen and Meyer (2003) and
SANBI (2015b)
Europe Spain A. tenuifolia 1954 Alien Naturalized Amor Morales et al. (2012)
Europe Spain A. psilostachya 1981 Alien Invasive Amor Morales et al. (2012)
Europe Spain A. artemisiifolia 1983 Alien Invasive Amor Morales et al. (2012)
Europe Spain A. trifida 1983 Alien Naturalized Amor Morales et al. (2012)
Europe Spain-Baleares A. tenuifolia 2004 Alien Naturalized Fraga and Garc
ıa(2004)
Africa Swaziland A. artemisiifolia —Alien Naturalized Randall (2012); Swaziland’s Alien Plants
Database. http://www.sntc.org.sz/alien
plants/index.asp
Europe Sweden A. trifida 1909 Alien Casual Anderberg (2000), Gerber et al. (2011),
Randall (2012); DAISIE, Species
Factsheet: A. trifida. available at http://
www.europe-aliens.org/speciesFact
sheet.do?speciesId D21722# (Accessed
in January 2017)
Europe Sweden A. psilostachya 1928 Alien Naturalized Dahl et al. (1999) and Anderberg (2005)
Europe Sweden A. artemisiifolia 1866 Alien Casual Dahl et al. (1999), Anderberg (2000), and
Smith et al. (2008,2013)Dahl et al.
(1999) and Smith et al. (2013)
Europe Switzerland A. trifida 1900 Alien status unknown Follak et al. (2013) and EPPO (2016).
Europe Switzerland A. psilostachya —Alien status unknown Greuter (2006) and Hess et al. (2006)
(Continued on next page)
148 C. MONTAGNANI ET AL.
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Finally, in Oceania the species officially appeared in 1908
in Australia, spreading rapidly only after 1940s (Parsons
and Cuthbertson, 2001), and in 1911 in New Zealand
(Webb et al.,1988).
Europe was the first continent where A. trifida was
introduced. It is recorded in the 17th century in
botanical gardens (e.g. 1699 in the United Kingdom—
see Online Atlas British and Irish Flora http://www.
brc.ac.uk/plantatlas/index.php?q Dplant/ambrosia-tri
fida). However, the oldest collection in the wild was
reported from Western Europe where A. trifida was
recorded in Belgium in 1829 and has been found with
more continuity from 1896 onward (Verloove, 2016a). It
was later collected in Germany in 1877 (Follack et al.,
2013). In Northern Europe, the species was found first in
Ireland (1894) and, in 1897, in the United Kingdom
(Rich, 1994; Sell and Murrell, 2006), Finland (Lampinen
and Lahti, 2016), Switzerland (Follak et al.,2013), and
Latvia (Gudzinskas et al.,1993). In Southern Europe, the
species was first recorded in South Tyrol in 1899 (Chau-
vel et al.,2015) and recorded in 1909 in Northwest Italy
(Vignolo Lutati, 1935); in other countries it has been
found in more recent times (1982 in Serbia and 1983 in
Spain) (Amor Morales et al.,2012; Follak et al.,2013). In
Eastern Europe A. trifida was mentioned much later
than in other parts of the continent, starting from 1960
(e.g. Czech Republic) (Py
sek et al.,2012) up to the 1980s
and beyond.
In comparison to A. artemisiifolia, A. trifida
appeared later in Asia. In 1935 it was observed in China
(Qin et al.,2014), and it was recorded in Japan almost
20 years later (1952; Invasive species of Japan: https://
www.nies.go.jp/biodiversity/invasive/DB/detail/80410e.
html). In other countries in Asia, records have been
made mostly since 1970 (South Korea) and the following
decades (Israel, India). In Central America, A. trifida has
been introduced into Mexico (Villase~
nor and Espinosa-
Garcia, 2004). Unlike common ragweed, giant ragweed
rarely shows invasive behavior (e.g. China and Japan)
and it is often casual (e.g. Austria and British Isles) (Essl
and Rabitsch, 2002; Reynolds, 2002; EPPO, 2016), which
suggests that its persistence in some areas is only possible
due to repeated introductions (Follak et al.,2013).
A. psilostachya has a wider invasive range than A.
trifida, but it is not listed alongside giant and common
ragweed as invasive species by EPPO (EPPO, 2016). The
species occurs in all continents and is naturalized in a
large number of countries, although it is not as aggressive
as A. artemisiifolia (Table 2). In any case, it should be
remembered that A. psilostachya has not been as deeply
Table 2. (Continued).
Continent Country Species First record Status References
Europe Switzerland A. artemisiifolia 1850s Alien Invasive Taramarcaz et al. (2005), Kazinczi et al.
(2008), and Bullock et al. (2012)
Asia Taiwan A. artemisiifolia 1971 Alien Naturalized Wu et al. (2004), Wu et al. (2010), and
Peng (2013)
Asia Taiwan A. psilostachya 2000 Alien Naturalized Tseng et al. (2004), Ramachandra Prasad
et al. (2012), Wu, et al. (2010), and
Chen and Hind (2011)
Asia Turkey A. artemisiifolia 1995 Alien Invasive Byfield and Baytop (1998), Zemmer et al.
(2012), Beh¸cet (2004), Onen et al.
(2014); and Arslan et al. (2015)
Asia Turkey A. tenuifolia 2000 Alien Naturalized? Beh¸cet (2004) and
€
Ozhatay and K€
ult€
ur
(2006)
Europe Ukraine A. artemisiifolia 1925 Alien Invasive Smith et al. (2013), Bullock et al. (2012),
and EPPO (2016).
Europe Ukraine A. psilostachya —Alien status unknown Greuter (2006)
Europe Ukraine A. trifida —Alien Casual Yavorska (2009)
Europe United Kingdom A. artemisiifolia 1836 Alien Invasive Rich (1994), Bullock et al. (2012), and Essl
et al. (2015)
Europe United Kingdom A. trifida 1897 Alien Casual Rich (1994), Sell and Murrell (2006), EPPO
(2016); Online Atlas British and Irish
Flora: http://www.brc.ac.uk/plantatlas/
index.php?qDplant/A.-trifida
Europe United Kingdom A. psilostachya 1880s Alien Naturalized Rich (1994), Sell and Murrell (2006); On
line Atlas of the British and Irish Flora:
http://www.brc.ac.uk/plantatlas/index.
php?q Dplant/A.-psilostachya
Europe United Kingdom A. tenuifolia —Doubtful occurrence Stace (2010) and Randall (2012)
America (N) United States of America A. psilostachya —Native Bassett and Crompton (1975)
America (N) United States of America A. tenuifolia —Alien status unknown Liogier (1997) and USDA –NRCS (2017)
America (N) United States of America A. trifida —Native Bassett and Crompton (1982)
America (N) United States of America A. artemisiifolia —Native Bassett and Crompton (1975)
America (S) Uruguay A. artemisiifolia —Species occurring Tejera and Beri (2005), Zuloaga et al.
(2008), and Essl et al. (2015)
America (S) Uruguay A. tenuifolia —Native S
aenz and Guti
errez (2008)
CRITICAL REVIEWS IN PLANT SCIENCES 149
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studied and is often confused with A. artemisiifolia or
other taxa. For these reasons, its distribution may be
affected by misidentification, and dates of introduction
are often uncertain. On the American continent, outside
its recognized native range, the position of A. psilosta-
chya as an independent taxon is discussed (Pruski,
2017). On the Hawaiian Islands it is listed as a quaran-
tine weed (Randall, 2012), while it is reported as both
wild and cultivated in Guadeloupe (Hibon, 1942). In
Europe, it has been found in the United Kingdom since
the 1880s (Rich, 1994), where today it is naturalized.
However, it is not as widespread in the UK as it is in
Germany, where it appeared a few years later in 1897
(NetPhyD: Deutschlandflora WebGIS). At the beginning
of the 20th century, A. psilostachya was found in Hun-
gary (Puc, 2004) and then in the Netherlands (1905; Od
e
and Beringen, 2017b), where according to Van Denderen
et al. (2010) it is the only well-established taxon.In
Southern Europe, it first appeared in Italy at the end of
the 1920s (Vignolo Lutati, 1935). In France, colonization
probably dates back to the same time, although this may
be influenced by misidentification of the specimens
(Hibon, 1942; Queney, 1942). New European records of
the species have also been collected recently, since the
1980s for instance in Spain, Finland, Czech Republic,
and Greece (Anderberg, 2005; Amor Morales et al.,
2012;Py
sek et al.,2012; Von Raab Straube and Raus,
2016). Concerning Africa, information about the arrival
of the taxon is quite fragmented. The oldest date of col-
lection (1916) relates to Algeria (Maire, 1928), although
an earlier record by Battandier (1888) discusses the pres-
ence of a perennial plant growing on maritime sands
“with Ambrosia leaves”different from A. maritima (the
only ragweed identified in other Algerian localities, prob-
ably native to the Old World (Montagnani et al.,2017).
A. psilostachya has also been alien to Moroccan flora
since the 1990s (Tanji, 2005). In Southern Africa, it is a
weed of sugar cane fields in Mauritius (Macdonald et al.,
2003) and it is naturalized in different areas (Germishui-
zen and Meyer, 2003; SANBI, 2015a). In Australia, the
plant was found in 1922 (Parsons and Cuthbertson,
2001). Records from Asia are quite recent, from the
1990s in India (Ramachandra Prasad et al.,2013)to
2000 in Taiwan (Tseng and Peng, 2004), and the plant is
often naturalized and shows an invasive behavior in sev-
eral countries (e.g. Japan and India).
A. tenuifolia is widespread at the global level, but is
usually much more localized than the other species
outside its native range. Fairly close to its native area, A.
tenuifolia has been introduced into Louisiana (North
America), Puerto Rico, and Chile, where it was identified
for the first time in 1923 (Ugarte et al.,2011;
USDA-NRCS, 2017; Acevedo-Rodrıguez and Strong,
2012). In Europe, according to the available data, the
oldest record (1839) of A. tenuifolia is from France
(Thellung, 1912). Successive records date one century
later—1935 in Italy (Vignolo Lutati, 1935) and 1954 in
Spain (Amor Morales et al.,2012). According to Randall
(2012), A. tenuifolia also occurs in the United Kingdom,
but there is no bibliographic evidence of this. In Asia, the
collections of A. tenuifolia are few and quite recent: in
Israel in1991 (Waisel et al.,2008) and Turkey in 2000
(Beh¸cet, 2004;
€
Ozhatay and K€
ult€
ur, 2006). In Australia
and New Zealand, the presence of the species has been
confirmed since 1932 and 1950 (Parsons and Cuthbert-
son, 2001; Howell and Sawyer, 2006) while in Africa, the
species is only present in South Africa (Germishuizen
and Meyer, 2003; SANBI, 2015b).
V. Environmental barriers
In this section, the main environmental requirements
and plant traits, predictor of the likelihood of persistence
of the species in new ranges are reported and discussed.
Slatyer et al. (2013) found a positive relationship between
niche breadth and range size, suggesting that a wide tol-
erance to abiotic conditions facilitates occupancy of a
larger area, and that habitat breadth is a good predictor
of a wide distribution. Environmental matching is
important along the naturalization-invasion continuum
(Richardson and Pysek, 2012). Such generalist, com-
mon-habitat colonizer, species are highly competitive
and tolerant to disturbance and have a great potential to
become invasive (Volta et al.,2013). Looking at the
global distribution of ragweed species (Figure 1), they
have generally found suitable conditions to persist and
spread, often becoming naturalized (Figure 2). Thus,
overcoming environmental barriers appears to be a solv-
able issue for ragweed species.
A. Habitat types and environmental matching
Before describing and discussing the habitats elected by
the ragweed species in both their native and invasive
ranges (Table 3), it is necessary to point out that it is cur-
rently quite difficult to define the native habitat of A.
artemisiifolia with any certainty, because, as already
mentioned, its distribution has been human-mediated
for such a long time (McAndrews, 1988).
It has been suggested that A. artemisiifolia should be
native to the Great Plains (Hodgins and Rieseberg, 2011;
Hodgins et al.,2013). However, both in the United States
and in its invasive range A. artemisiifolia has rarely been
found in natural habitats, such as prairies, while it is
abundant and often invasive in ruderal ones (roadside
verges, wastelands, railway embankments, construction
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sites, quarries etc.), at the edge of croplands or in arable
fields, and also on riverbanks (Bassett and Crompton,
1975; Fumanal et al.,2008a; Milakovic et al.,2014; Essl
et al.,2015; Gentili et al.,2016). Consistent with this,
floras and specialized sources indicate synantropic envi-
ronments as the main habitats for common ragweed
(Basset and Crompton, 1975; Smith et al.,2013).
It is likely that common ragweed has shifted gradually
from its primary habitat to ruderal areas and croplands,
following the advance of human settlements into unex-
ploited American lands, when synantropic environments
became more frequent (Basset and Crompton, 1975;
Smith et al.,2013). In support of this hypothesis, the
analysis of herbarium records by Lavoie et al. (2007)
showed that in Quebec common ragweed spread along
rivers at first, and only later entered agricultural fields.
In the last 30 years in the United States (native range),
A. trifida has also shown the tendency to colonize culti-
vated fields (e.g. corn, soybean and cotton), probably as
local adaptation of the species that originally lived in
riparian (riverbanks, floodplains) or nonriparian edge
habitats near cultivated areas or railroads and wastelands
(Basset and Crompton, 1982; Regnier et al.,2016). On
floodplains, where floods occasionally occur, it does not
grow at the lowest elevation but dominates in communi-
ties located 60 cm above the water level (Menges and
Waller, 1983). Outside of North America, A. trifida lives
along rivers and generally shares the ruderal behavior of
A. artemisiifolia, occurring especially in cultivated fields,
along railways (Gudz
ınskas, 1993; Chauvel et al.,2015),
on maritime docks (e.g. Britain) (Rich, 1994), and fluvial
ports (e.g. along Rhine and Elbe rivers in Europe)
(Chauvel et al.,2015). Nevertheless, in France, Follak
et al. (2013) and Chauvel et al. (2015) found that A.
trifida is more often recorded in ruderal places and along
railways than in native elective riverine habitats.
Regarding A. psilostachya and A. tenuifolia, elective
habitats are more recognizable than the ragweed species
previously described. According to Albertson (1937)A.
psilostachya “invades the short grasses from the disturbed
places along the slopes.”In its native range in North
America, A. psilostachya shares ruderal habits with A.
artemisiifolia, as it is common in open disturbed habitats
such as abandoned fields, vacant lots, and along trans-
portation corridors (Basset and Crompton, 1975). In
contrast to A. artemisiifolia, however, it is also common
in semi-natural/natural environments: it is a typical forb
of tallgrass prairies (temperate grasslands) of the
Table 3. Environmental requirements of Ambrosia species (ragweeds): main data related to colonized habitat types (native and invasive
range), suitable climatic, soil, and light conditions.
Species Ambrosia artemisiifolia L. Ambrosia trifida L. Ambrosia psilostachya DC. Ambrosia tenuifolia Spreng.
Native habitat Disturbed open habitat Disturbed open habitat Disturbed open habitat Disturbed open habitat
Semi-natural grasslands Semi-natural grasslands Semi-natural grasslands Semi-natural grasslands
Croplands Croplands Croplands Croplands
Along transportation corridors Along transportation
corridors
Along transportation corridors Along transportation
corridors
Wastelands Wastelands Wastelands Wastelands
Riparian habitat Riparian habitat Riparian habitat Riparian habitat
Dunes Dunes Dunes Dunes
Non dense wood Non dense wood Non dense wood Non dense wood
Habitat in invasive
range
Disturbed open habitat Disturbed open habitat Disturbed open habitat Disturbed open habitat
Semi-natural grasslands Semi-natural grasslands Semi-natural grasslands Semi-natural grasslands
Croplands Croplands Croplands Croplands
Along transportation corridors Along transportation
corridors
Along transportation corridors Along transportation
corridors (?)
Wastelands Wastelands Wastelands Wastelands
Riparian habitat Riparian habitat Riparian habitat Riparian habitat (?)
Dunes Dunes Dunes Dunes
Non dense wood Non dense wood Non dense wood Non dense wood
Climate Warm temperate climate (with
exceptions)
Warm temperate climate Warm temperate climate (with
exceptions)
Warm temperate climate
Drought tolerant Drought tolerant Drought tolerant Drought tolerant
Freeze tolerant Freeze tolerant Freeze tolerant Freeze tolerant
Soil Alkaline Alkaline? Alkaline Alkaline?
Acid Acid Acid Acid
Silty Silty Silty Silty
Sandy Sandy Sandy Sandy
Well drained/dry Well drained/dry Well drained/Dry Well drained/Dry
Moist/wet Moist/wet Moist/Wet Moist/Wet
Saline Saline Saline Saline
Metal Metal Metal Metal
Light Heliophylous Heliophylous Heliophylous Heliophylous
Shady-tolerant Shady-tolerant Shady-tolerant Shady-tolerant
Requirements of each species are highlighted in grey and doubtful attributions are signaled by “(?)”.
CRITICAL REVIEWS IN PLANT SCIENCES 151
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American Great Plains (Reece et al.,2004) and a weed in
pastures and rangelands where it is favored by overgraz-
ing and fire (Baker and Guthery, 1990; Abrams, 1988;
Vermeire and Gillen, 2000; Funderburg et al.,2014). It is
a sand-loving species and colonizes dry sand prairies on
sand hills (Hart and Gleason, 1907; Hulett et al.,1988;
Ebinger et al.,2006; Uresk, 2012). It also colonizes
coastal dunes, mainly secondary dunes and vegetated
flats behind them (Carls et al.,1991) mostly where there
is a certain grade of human impact (e.g. vehicle passage)
(Stephenson, 1999). It is also listed among halophytic
plants living in harsh environments such as inland saline
plains (Flores-Olvera et al.,2016) and is referred to as a
colonizer of riparian habitats, where it is considered a
“mesoriparian plant,”i.e. not typical of the wettest areas
of riverbeds (Stromberg, 2013). Contrary to the other
ragweed species, A. psilostachya also lives in the under-
story of nondense woodland (e.g. Pinus ponderosa for-
ests) (Bojorquez Tapia et al.,1990). There is little
information in the literature concerning the habitats of
A. psilostachya outside of its native range. However, it
suggests that this species, as in its native range, fre-
quently colonizes coastal areas, dunes, sandy soils usually
exposed to human impacts (Rich, 1994; Mandrioli, 1998;
Weeda, 2010; Del Vecchio et al.,2015; Fried et al.,2015),
rivers, and ruderal habitats (Amor Morales et al.,2012;
Ardenghi and Polani, 2016). In a recently colonized area
of India, A. psilostachya has also been observed in crop-
lands and pastures (Ramachandra Prasad et al.,2013).
As with the congeners examined previously, in South
America, A. tenuifolia is a plant typical of open habitats
and, like A. psilostachya, it is native to grasslands tradi-
tionally subjected to disturbing factors that in this case are
ascribable to grazing and periodic flooding (as the result
of heavy rainfall, flat topography, and poor drainage). In
Argentina, it represents a characterizing element of the
flooding Pampa grasslands, as one of the co-dominant
taxa of one of the most widespread plant communities of
the area (e.g. communities characterized by Piptochaetium
montevidense, A. tenuifolia, Eclipta bellidioides and
Mentha pulegium) (Burkart et al.,1990; Insausti et al.,
1995; Insausti and Grimoldi, 2006). The typical commu-
nity of A. tenuifolia usually lives in raised flat lowlands,
less subjected to inundation. However, A. tenuifolia can
also dominate communities typical of more humid condi-
tions, localized along river valleys, drainage basins, and
coastal salty lagoons (Burkart et al.,1990). It is also a char-
acteristic element of coastal dune vegetation (Fontana,
2005; Marcomini and L
opez, 2013). In Argentina,
Marcomini et al. (2016) found it in stable dune systems,
occurring between dunes where the vegetation cover is
more relevant and dominated by Cortadera selloana (cor-
taderal community). As in the Pampean Plains, these
environments are subjected to periodic floods, although
they are also subjected to drought (Marcomini et al.,
2016). Furthermore, A. tenuifolia has been listed in
Paraguay as an agricultural weed (De Egea et al.,2016).
Outside its native range, specifically Spain, A. tenuifolia
lives in habitats very similar to those colonized by A. psi-
lostachya (Amor Morales et al. (2012) and in other Euro-
pean countries the two species can be found in the same
sites, for instance sharing an halophytic behavior (e.g. in
some areas of Italy) (Mandrioli et al.,1998). Additional
findings in Turkey revealed that A. tenuifolia can be also
found in orchards and cultivated fields (tomatoes, cucum-
bers, wheat) and that it could prefer humid ruderal places
(Beh¸cet, 2004;
€
Ozhatay and K€
ult€
ur, 2006).
Overall, analysis of the spectrum of colonized envi-
ronments shows that a limited shift of habitat types
between native and invasive ranges can be observed. All
species are in fact typical of naturally or artificially
disturbed open areas, both in America and in the rest of
their acquired range. However, all species are more
frequently present in natural environments in their
native ranges, likely representing their original habitats.
It is difficult to have an idea of the primary environments
of A. artemisiifolia, whereas A. trifida spreads from
riparian habitats, and the perennial A. tenuifolia and A.
psilostachya originated from temperate grasslands and
colonize inland and coastal sand dunes. On the whole, it
is clear that all these species spread gradually from their
primary habitat to synanthropic environments. It follows
that although the spreading of each of these species
requires specific conditions, they are capable of quickly
shifting their habitat in changing circumstances and
taking advantage of environmental disturbance. Being
tolerant to disturbance, these common-habitat colonizer
species have a great potentiality as invader. They can be
considered pioneer species naturally colonizing harsh
environments and ready to spread in ruderal habitats,
where conditions are maintained suitable mainly by
human action.
B. Climate matching and temperature tolerance
Climate matching is a basic requirement for persistence
in a new area. According to their global distribution, all
these species come from temperate areas (Figure 1).
Although with several exceptions, they mainly “move”
from/to warm temperate climate regions, generally
avoiding equatorial, arid, and snow climates (Figure 1).
Petitpierre et al. (2012) observed a limited shift of cli-
matic niche between the native and adventive range of
A. artemisiifolia. Analogously, a limited shift also
appears valid for the other ragweed species on the basis
of our preliminary and basic comparison (Figure 1).
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In keeping with these observations, many studies dem-
onstrate the influence of climate on ragweed germina-
tion, growth, and reproduction. Regarding this, A.
artemisiifolia has been the most widely studied species.
With regard to germination, it has been reported that A.
artemisiifolia seeds can germinate in a wide range of
temperatures; the minimum temperature of germination
ranges from 3.4 to 3.6C (Essl et al.,2015) while germi-
nation decreases up to 40C (Bullock et al.,2012). Never-
theless, Leiblein-Wild et al. (2014) observed differences
between native and introduced populations: in the inva-
sive range, seeds generally have a larger mass and can
germinate faster under a wider range of conditions. The
authors attributed this better performance to favorable
biotic and abiotic factors occurring in the invasive range
and speculated about a possible case of Evolution in
Increased Competitive Ability (EICA). In any case, A.
artemisiifolia seeds follow a quite complicated cycle of
primary/secondary dormancy and they need an exposure
to winter temperature or stratification in lighting condi-
tions to break primary dormancy (Baskin and Baskin,
1980). In sites where the growing season is too short for
seed maturation (e.g. Northern Europe) or seasonal tem-
peratures are too high for vernalization (e.g. some areas
of the Mediterranean basin), the species cannot become
naturalized and occurs just in few small ephemeral
populations (Dahl et al.,1999; Kazinczi et al.,2008; Van
Denderen et al.,2010; Makra et al.,2014; Smith et al.,
2013).
Seasonal temperature variations also play an impor-
tant role for A. trifida (Davis, 1930; Bazzaz, 1979) and A.
tenuifolia (Insausti et al.,1995), whose seeds need low
temperatures to germinate (primary/secondary dor-
mancy cycle). The range of germination temperatures
for A. trifida is wide (from 4 to 41C, with an optimum
between 10 and 24C), but only if soil moisture
conditions are suitable (17% to 55% soil moisture, with
an optimum at 20% to 30%) (Abul-Fatih and Bazzaz,
1979a; Ballard et al.,1996). For A. tenuifolia, the lack of
alternating temperatures prevents seed germination
(Insausti et al.,1995).
The climatic requirements for the germination of A.
psilostachya are not clear (Basset and Crompton, 1975).
Martison et al. (2011) identified, among climatic and soil
variables, mean annual temperature as the factor that
mostly contributes to explaining the distribution of A.
psilostachya in the United States, whereas in Europe Ras-
mussen et al. (2017) found that minimum temperature
to be highly influential. The life cycle of the species in
relation to seasonality in its native habitat (e.g. snowing,
freezing winter and summer drought), indicates that the
seeds of A. psilostachya should also be characterized by
dormancy and they may need a vernalization phase to
germinate (Baskin and Baskin, 2014). Nevertheless, the
propagation of A. psilostachya is mainly vegetative, so if
the root system can survive, environmental limits on
germination are less important. According to Rich
(1994) and Bassett and Crompton (1975), roots are
generally cold-resistant, able to survive in the extremely
cold Canadian winters, and can continue growing the
following spring for over 30 years. It has been supposed
that independence from germination requirements may
allow A. psilostachya to colonize those countries where
A. artemisiifolia cannot successfully conclude its life
cycle (e.g. The Netherlands; Van Denderen et al.,2010).
Concerning plant development, data are available
mainly for A. artemisiifolia. Cunze et al. (2013) estimated
that it requires an accumulated temperature sum of
1400C to produce mature seeds. In their report, Bullock
et al. (2012) found that the maximum photosynthetic
rate is at 20C (halved at 30C). Nevertheless, they also
highlighted that A. artemisiifolia persists where the cli-
mate is hotter, deducing that high temperatures are likely
to have a lesser impact on its performance than low
temperatures. Bazzaz (1974) attributed its tolerance to
high temperatures to high transpiration rates, which
allow a transfer of latent heat in leaves at temperatures
below ambient temperature. Frost in late spring or early
autumn can be fatal for seedlings and adult plants (Essl
et al.,2015), although Leiblein Wild et al. (2014)
observed that seedlings are more frost tolerant in Europe
than in native countries, thus supporting the assumption
of local adaptation. In general, Rasmussen et al. (2017)
recently found that common and giant ragweed perform
better in relatively wet conditions, while perennial rag-
weed in drier ones. Growing degree days are generally
cited as the most influential climatic factor explaining
the distribution of short-day plants A. artemisiifolia, A.
trifida, and A. psilostachya in Europe. The main climatic
requirements of the four ragweed species considered are
summarized in Table 3.
C. Moisture and soil types tolerance
Soil is another factor determining the colonization and
successful survival of plants. Concerning soil pH, few
studies were undertaken and the results are not totally
consistent. Fumanal et al. (2008a) demonstrated that A.
artemisiifolia can grow both on acid and alkaline soils
(extreme values of pH KCl: 4.1 to 8.6), even if it preferen-
tially occupys sites with a pH range between 7 and 8.
Coherntly, Essl et al. (2015) reported that A. artemisiifo-
lia grows best under moderately basic condition (pH D
8). On the other hand, Pinke et al. (2011) found the
highest common ragweed cover at the edge of Hungarian
sunflower fields when the soil pH was acid (<5); this in
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agreement with the information reported in Hungarian
literature, namely that this weed thrives best on acidic
sandy soils (Ujv
arosi, 1973; Szigetv
ari and Benko
,2008).
Regarding germination, Sang and collaborators (2011)
demonstrated that A. artemisiifolia germination success
exceeded 48% in solutions with pH values between 4 and
12, with maximum rates occurring in distilled water at
pH 5.57. However, under laboratory conditions, germi-
nation occurs in a wider range of pH (Bullock et al.,
2012). Silt loam and silt clay loam soils are elected as the
optimum by Basset and Crompton (1975) and, in France,
Fumanal et al. (2008a) found the plant on sand to clay or
silty loam, but mostly on sandy soils. Regarding soil
water content, A. artemisiifolia can be very resilient to
short-term drought (Bullock et al.,2012). Nevertheless,
Hodgins and Rieseberg (2011) demonstrated the poor
survivorship under drought conditions of the European
populations in comparison to the American ones, proba-
bly due to the evolution of a life-history that has favored
a more rapid growth and reproduction than drought tol-
erance in the invasive range. Leiblein and L€
osch (2011)
observed a major growth of A. artemisiifolia in moist soil
conditions, but also the capacity to survive in dry, moist,
and waterlogged soils (5%, 22% and 39% of water). In
the latter situation, the plants are far smaller, but able to
reach maturity and produce seeds, although in small
quantities. In keeping with Essl et al. (2015), A. artemisii-
folia is not typical of wet areas, but its seeds can poten-
tially tolerate and remain viable in soils with high water
content. Concerning salinity (Table 3), Di Tommaso
(2004) showed that the seeds of A. artemisiifolia can also
germinate at high levels of sodium chloride (5% to 12%
of germinated seed at 400 mmol L
¡1
). However, he
highlighted that the percentage of germination in his
experiment was negatively correlated to the increase in
salt, but the recovery in distilled water of viable nonger-
minated seeds was rapid. This study also suggested an
adaptation of A. artemisiifolia to local conditions, as the
seeds collected from plants living along roadsides
showed a higher percentage of germination than those
collected in cultivated fields. Another soil parameter that
A. artemisiifolia appears to manage quite well is the pres-
ence of metals. Bae et al. (2016) proved that under metal
stresses (Zn, Pb, Ni, Cd, Cu), A. artemisiifolia performs
better in germination and seedling growth in comparison
with native flora. This experiment simulated roadside
conditions and delineated a potential empty niche where
the species would have almost no competitors.
Information about soil requirements for the other rag-
weed species is not as exhaustive as for A. artemisiifolia,
although it is possible to understand several differences
by reviewing available data. A. trifida is typical of more
mesophytic conditions than A. artemisiifolia (Abul-Fatih
and Bazzaz, 1979a; Basset and Crompton, 1982), consis-
tent with its native habitat (e.g. floodplains temporarily
including presence of standing water; Menges and Wal-
ler, 1983). Wortman et al. (2012) and Follak et al. (2013)
showed how the distribution of A. trifida is more closely
related to the seasonality of precipitation and summer
precipitation than other variables such as land use and
landscape structure. Low rainfall is a limiting factor in its
native range (Basset and Crompton, 1982); germination
occurs in a wide range of soil moisture with an optimum
of 20% to 33% (Abul-Fatih and Bazzaz, 1979a). Nonethe-
less, Schutte et al. (2008a) found that giant ragweed seed-
ling emergence is insensitive to dry conditions of the top
layers of soil (1 cm of soil) and that emergence usually
occurs during relatively dry periods. Soil texture is not
specified, but based on habitat (floodplains, drainage
ditches, open stream banks), it can be deduced that A.
trifida colonizes incoherent soils; in cultivated fields, it is
usually found in low, silty substratum (Basset and
Crompton, 1982). There are no data regarding preferen-
ces of soil pH and salinity tolerance, while Cui et al.
(2007) showed that A. trifida can live where the concen-
tration of metals (Pb, Zn, Cu, Cd) is quite high and can
be considered a good accumulator at root level.
Concerning A. psilostachya, as previously stated, it is a
sand-loving species and prefers well-drained, alkaline
soils (Basset and Crompton, 1975). It lives in soils char-
acterized by high salinity both in the native and invasive
ranges, although salt can strongly limit the growth of
plants (Salzman, 1985). Salzman and Parker (1985)
experimentally demonstrated that the wide root system
can balance stress through the connection between
ramets; taking advantage of local salinity variations,
ramets living in lower salinity conditions contribute to
the survival of those living in high salinity conditions.
This physiological integration (exchange of resources
among connected ramets) helps A. psilostachya persist in
stressful conditions. It boosts its efficiency of coloniza-
tion and habitat exploration, thus promoting a greater
dispersal ability (through rhizomes) in adverse condi-
tions, to increase the probability of finding favorable
microsites (Salzman, 1985). Furthermore, A. psilostachya
persists even when high concentrations of metals in soil
are lethal for other plants (e.g. Zn, Cu, Mn, etc.) (Basset
and Crompton, 1975). The successful survival of A. psi-
lostachya in metal-rich soils appears to be positively
mediated by mycorrhizal symbiosis (Rivera-Becerril
et al.,2013). Habitats colonized by Western ragweed are
typically subjected to seasonal drought. It is a xeric-
adapted species (Corbett and Anderson, 2006), with a
very long root able to draw water from deep sources, and
persists without desiccating at more humid, deep soil lev-
els (1.83 m in depth according to Stromberg, 2013). In
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the grasslands of the Nebraska Sandhills, A. psilostachya
is relatively stable through drought (and grazing), while
other resistant perennial grasses are damaged (Reece
et al.,2004; Stubbendieck and Tunnell, 2008). Although
severe events leading to a serious desiccation of rhizome
(¡60% of weight), can have negative effects on shoot
emergence (Karnkowsky, 2001). Regarding tolerance to
waterlogged conditions, A. psilostachya prefers drained
soils, but it lives in the riparian habitat and according to
Stromberg (2013) it is a mesoriparian species. Finally,
from data by Towne (2000), who monitored the impact
of large ungulate carcasses (e.g. bison, cattle and deer) on
grassland dynamics, it can be argued that A. psilostachya
dominates in nutrient-rich soils and easily tolerates high
levels of organic compounds.
Information about soil preferences of A. tenuifoilia is
quite dispersed. It prefers fertile, well-aerated (Insausti
and Soriano, 1987), not very deep hydro-halomorphic
soils (Burkart et al.,1990; Anton et al.,2012). Soil water
content can be determinant in the life cycle of the plant.
A. tenuifolia co-/dominates plant communities fre-
quently exposed to floods of varying intensity and dura-
tion, usually brief (1 to 2 months), of reduced magnitude
(water cover does not exceed the depth of 7 cm in
spring), with only occasionally prolonged events with
heavy impact occurring (water cover 10 to 30 cm deep
for 3 to 5 months) (Insausti and Grimoldi, 2006).
Insausti and Soriano (1987) observed that A. tenuifolia
frequently grows on anthills, and argued that those sites
are suitable as they are not affected by prolonged water-
logged soil conditions and the subsequent anoxia is not
tolerated by roots for more than 1 to 2 months (Insausti
and Grimoldi, 2006). On the other hand, seeds can toler-
ate immersion in water and low temperature even for
long periods, without negative effects on dormancy
release (Insausti et al.,1995). Resilience to drought has
not been specifically investigated but a certain degree of
tolerance can be inferred as environments where A. ten-
uifolia lives are involved in periods of drought, both on
the Pampean Plains (summer drought) and coastal areas
(Marcomini et al.,2016). A summary of the aforemen-
tioned soil requirements is shown in Table 3.
D. Light requirements and tolerance
The tolerance to light/shade has been briefly discussed
in the description of habitats and the main require-
ments for ragweed species are reported in Table 3.In
general, ragweed species are pioneer plants living in
open sunny environments. However, based on habitat
preferences, tolerance to moderate shade has been
shown by A. psilostachya, and Essl et al. (2015)affirmed
that A. artemisiifolia is also medium shade-tolerant.
Generally, shade suppresses A. artemisiifolia (Bullock
et al.,2012) and the lack of adequate light intensity
strongly contributes to a progressive decrease in plant
performance and recruitment (Gentili et al.,2015,
2017). Conversely, A. artemisiifolia, both at mature and
seedling stage, is extremely tolerant to high light inten-
sities, which are characteristic of open environments
(Bazzaz, 1974). Not only is A. trifida tolerant to high
light intensities but Menges and Waller (1983) indicated
it to be a high light specialist or light-loving species.
The authors distinguished this species from the low
light specialists and light generalist herbs in floodplain
communities; the early emergence, development of
seedlings and the great growth of plants would indicate
that the life cycle of A.trifida is strongly shaped around
light exploitation. However, several studies show that the
species is tolerant also to shady conditions likely to occur
along both the natural vegetation dynamic and cultivated
fields. It appears that A. trifida can allocate resources dif-
ferently, based on light situations (Hartnett et al.,1987;
Abul-Fatih et al.,1979; Webster et al.,1994; Jurik, 1991).
Although a multifactorial process, A. artemisiifolia
germination is also light-induced, for instance, in this
species the secondary dormancy (Baskin and Baskin,
1980,1985) is induced by the lack of light in combina-
tion with low temperature fluctuations, high CO
2
concentration in the soil, and hot dry summer periods
(Bazzaz, 1979; Essl et al.,2015), in lab experiments, seeds
germinated also in the dark in a range of temperature
corresponding to late spring and summer (Bullock et al.,
2012; Baskin and Baskin, 1980).
Along with alternating temperatures, light and in
particular the R:FR ratio also promotes A. tenuifolia
seed germination and plant growth, which benefits
from vegetation gaps (Insausti et al.,1995; Insausti and
Grimoldi, 2006). Concerning germination, the same can
probably be said for A. psilostachya (CABI, 2017). Con-
versely, light is not one of the main factors promoting
the germination of A. trifida seeds (Davis, 1930; Schutte
et al.,2012), which are bigger in comparison to those of
the other species and have different mechanisms of
quiescence release mediated by pericarp and/or
embryo-covering structures (Harrison et al.,2007;
Schutte et al.,2012).
E. Plant traits involved in resistance and resilience
To support and explain environmental requirements,
changes in several plant traits have been highlighted as
key strategies in enhancing resistance or resilience to abi-
otic stresses (e.g. dormancy, rhizome features, early
emergence of seedlings, etc.). However, stress can also
derive from unfavorable biotic interactions with parasites
CRITICAL REVIEWS IN PLANT SCIENCES 155
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and predators, as well as from competition with the local
plant community. Furthermore, on observing colonized
environments, there is a series of potential human-medi-
ated disturbances such as fire, grazing, mowing, agricul-
tural practices, and human settlement development. All
these factors can affect the reproductive and vegetative
fitness of individuals or prevent their persistence through
direct suppression or a dramatic change in environmen-
tal parameters. Ragweed plant traits involved in stress
resistance and resilience are analyzed and discussed
below.
1. Resistance
Starting from strategies and traits that enhance the resis-
tance of individuals to natural or human perturbation
(intending resistance as the capacity of an individual to
resist the displacement of its biomass) (Grime, 2001), it
is found that morphological adaptations can avoid or
limit the effect of several perturbations. Development of
spines, pubescent or sclerophyllous leaves, or incorpo-
ration of granular minerals into plant tissues are typical
defensive mechanisms against grazing (Hanley et al.,
2007). In a xeric habitat, waxy leaves or a particular form
of plants (e.g. cushion plants) can prevent desiccation
and damage from wind, drought, or frost, while other
morphological structures can promote the persistence of
individuals in flooded and waterlogged riparian areas
(Catford and Jansson, 2014).
Ragweed plants (Table 4) do not show any evident
morphological adaptation to overcome stressing factors
that damage aerial parts. Only perennials (A. psilosta-
chya, A. tenuifolia) have quite densely short-haired
leaves that play a relatively protective role in avoiding
desiccation; A. psilostachya may assume a prostrate habit
that enhances resistance to several stresses. The presence
of phytoliths (mineral deposits in epidermal cell walls) in
aerial parts has been reported for A. psilostachya and A.
trifida (Bozarth, 1992) and this increases resistance to
leaf-eating invertebrates (Hanley et al.,2007).
Rather than morphological adaptations, chemical
protections, such as leaf-coating resins, are important
in ragweeds: Ambrosia species characteristically pos-
sess glandular trichomes, especially on the lower leaf
surfaces but also on stems, thus producing resinous
excreta rich in secondary metabolites such as sesqui-
terpenes and flavonoids (Mitchell et al.,1971;Wollen-
weber et al.,1987,1995). In general, like many other
Asteraceae (Heinrich et al.,1998), Ambrosia species
can biosynthesize many types of secondary metabolites
(Hodgins et al.,2013;Wanet al.,2002;Wanget al.,
2005;Kong,2010;S
€
ulsen et al.,2008,2013)that
contribute to protecting plants from abiotic and biotic
perturbations (Table 4).Partsofplantsandseedscan
be included in the diet of several wild mammals, birds,
and insects, and due to secondary metabolites ragweed
species are unpalatable for cattle that only resort to
eating the plants when there is no alternative forage
(Marten and Andersen, 1975; Reece et al.,2004;
Bullock et al.,2012). It is worth noting that many
authors (Gerber et al.,2011; Essl et al.,2015;Goeden
and Ricker, 1976) have pointed out that Ambrosia
species are attacked by specialized parasites that affect
their life cycles in their native range, rather than in
their invasive range where the parasites are less spe-
cialized and the damage inflicted is often not relevant.
The allelopathic effects of ragweeds on other plants
are also well documented (Table 4). Root exudates, leaf
leachate, and decaying leaves produce allochemical com-
pounds that inhibit germination and growth of other
species, both in natural and agricultural environments.
Table 4. Life strategies of Ambrosia species (ragweeds): relevant traits contributing to strenghten resistance, resilience, and competition
of ragweeds in the wild.
Species Ambrosia artemisiifolia L. Ambrosia trifida L. Ambrosia psilostachya DC. Ambrosia tenuifolia Spreng.
Resistance Morphologic structures Morphologic structures Morphologic structures Morphologic structures
Chemical defence against stress
and predators
Chemical defence against stress
and predators
Chemical defence against stress
and predators
Chemical defence against
stress and predators
Allelopathy Allelopathy Allelopathy Allelopathy
Mychorrhiza Mychorrhiza Mychorrhiza Mychorrhiza
Reallocation biomass Reallocation biomass Reallocation biomass Reallocation biomass
Resilience Resprouting Resprouting Resprouting Resprouting
Rhizome Rhizome Rhizome Rhizome
Secondary dormancy Secondary dormancy Secondary dormancy Secondary dormancy
Soil seed bank Soil seed bank Soil seed bank Soil seed bank
Long-lasting soil seed bank Long-lasting soil seed bank Long-lasting soil seed bank Long-lasting soil seed bank
Competition Advantages from vegetation
gaps
Advantages from vegetation
gaps
Advantages from vegetation
gaps
Advantages from vegetation
gaps
Weak competitor in more
evolved vegetation stages
Weak competitor in more
evolved vegetation stages
Weak competitor in more
evolved vegetation stages
Weak competitor in more
evolved vegetation stages
Persistence in more evolved
vegetation stages
Persistence in more evolved
vegetation stages
Persistence in more evolved
vegetation stages
Persistence in more evolved
vegetation stages
Traits of each species are highlighted in grey.
156 C. MONTAGNANI ET AL.
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Most studies relate to A. artemisiifolia (Rice, 1965;
Bullock et al.,2012; Vidotto et al.,2013) and A. trifida
(Wang et al.,2005; Kong et al.,2007), which have been
taken into account as a potential bioherbicide (Kong,
2010; Molinaro et al.,2016). However, allelopathy is
known also for A. psilostachya (Neill and Rice, 1971;
Dalrymple and Rogers, 1983) and A. tenuifolia (Mongelli
et al., 1997).
Another important factor involved in resistance of
ragweed species to stress and disturbance is the pres-
ence of mycorrhizal fungi (Table 4). Mycorrhiza
improve plant growth and health by enhancing min-
eral nutrition and increasing tolerance to abiotic and
biotic stresses (Lenoir et al.,2016). A. artemisiifolia is
considered in obligatory symbiosis with mychorrizal
fungi (arbuscular mychorrizal fungi, AMF) and stud-
ies have demonstrated that fungal colonization is pos-
itively correlated to environment disturbance (Essl
et al.,2015). Similarly, A. psilostachya has also been
found associated with mycorrhizal fungi in disturbed
and polluted environments (Busby et al.,2011;Pend-
leton and Smith, 1983; Rivera-Becerril et al.,2013).
For A. trifida, evidence of root colonization by
mycorrhizal fungi are few (MacDougall and Glasgow,
1929; Bassett and Crompton, 1982) and no data are
available for A. tenuifolia. Both the species live natu-
rally in environments subjected to seasonal flooding
and wet areas are not suitable to mycorrhizal coloni-
zation, probably due to the lack of well-aerated soils
(Entry et al.,2002;EscuderoandMendoza,2005).
The reallocation of resources is considered a further
important mechanism allowing ragweed plants to tol-
erate and respond to environmental stresses (Table 4).
For instance, A. trifida allocates resources differently
as a reaction to light variations (see above). Following
defoliation due to herbivore attacks, A. artemisiifolia
can efficiently re-allocate resources from root to shoot
biomass and avoid evident costs for fitness (Gard
et al.,2013); it can also enhance ramification when the
stem apex has been removed (Brandes and Nitzsche,
2006).
Interestingly, when environmental stress is lower or
absent, as can occur in introduced ranges, alien plants
can reallocate resources and thereby improve their
growth and competitive ability. This is at the foundation
of the EICA hypothesis which has been associated with
A. artemisiifolia in relation to changes in climate
(Leiblein-Wild et al.,2014), environmental conditions
(Hodgins and Rieseberg, 2011), and parasites (Fukano
and Yahara, 2012). Nevertheless, further studies have
demonstrated that the hypothesis is not always valid for
A. artemisiifolia (Genton et al.,2005; MacKay and
Kotanen, 2008).
2. Resilience
Traits and strategies related to resilience ensure rapid
recovery from disturbance and stress and a return to
control levels (Grime, 2001). In the case of highly disrup-
tive natural and human-related perturbations, species
need to rely on a series of regenerative strategies to have
a speedy and complete return to the earlier status. Attrib-
uting traits and strategies of plants to resistance or resil-
ience can often be tricky, and this paragraph focuses on
the main strategies involved in recovery from severe
events that definitely lead to suppression of individuals
or their aerial part in the case of geophytes.
Resprouting capacity (a resistance/resilience trait) can
be considered one of the main functional traits related to
successfully overcoming fire, mowing, intensive grazing,
and some severe atmospheric events leading to suppres-
sion of the aerial parts of plants (Table 4; Keeley et al.,
2011). A. psilostachya and A. tenuifolia live on plains tra-
ditionally subjected to these types of severe perturbations
and are not highly affected by them (Wolfe, 1973;
Menghi et al.,1993; Hartnett et al.,1996; Madanes et al.,
2007); on the contrary, they are often favored and thus
show their weediness (Abrams, 1988; Hartnett et al.,
1996; Vermeire and Gillen, 2000; Vermeire et al.,2005;
Insausti and Grimoldi, 2006). This is related to their rhi-
zome, a “resistance”structure that confers resilience on
these species. As already underlined, the life strategy of
A. psilostachya is mainly based on its below-ground sys-
tem which allows it to overcome adverse moments and
unpredictability deriving from human action or climate:
through the rhizome, A. psilostachya can form clones of
plants occupying areas larger than 100 m
2
(Karnkowski,
2001). In suitable situations, the presence of the weed
can be very massive: 1132 kg ha
¡1
dry weight according
to Bovey et al. (1966). It has been estimated that the
establishment of a “competitive”root system takes
1 year; after the emergence of a seedling from one of the
few mature seeds, a shoot emerges from the root during
the second year and in only one season it can colonize
an area of 2 m
2
(Basset and Crompton, 1975; Mitich,
1996). Reece et al. (2004) demonstrated that A. psilosta-
chya can maintain primordia for several years even with
limited plant growth, and Wan et al. (2002) showed that
clipping stimulates the growth of new stems. Limits to
rhizome viability/resprouting derive from several cli-
matic conditions and burial depth (Miziniak and Prac-
zyk, 2002). Several authors affirm that sprouting from
buds is possible when soil thickness is up to 5 cm
(Miziniak and Praczyk, 2002; Vermeire et al.,2005). In
comparison to A. psilostachya, the life strategy of A. ten-
uifolia is based not only on rhizome sprouting but also
on seeds as explained below. Although fewer investiga-
tions have been carried out on the A. tenuifolia rhizome,
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it is clear that resprouting from below-ground buds per-
mits the recolonization of vegetation gaps after distur-
bance (Insausti and Grimoldi, 2006), thus ensuring the
persistence of the species (Semmartin et al.,2010).
A. tenuifolia is a highly productive species, with 1,330
gm
¡2
of total biomass according to Semmartin et al.,
(2010) and it can advance quite rapidly thanks to rhi-
zomes, with an estimated rate of 1.72 to 0.2 m
2
/month
(Insausti and Grimoldi, 2006). As already mentioned,
rhizome persistence in this species is limited by anaero-
biotic condition. Resprouting is also important for A.
artemisiifolia resilience: removal of stem, as can occur in
the mowing or grazing regime, induces the resprouting
of plants from buds at the base (Brandes and Nitzsche,
2006; Patracchini et al.,2011; Milakovic and Karrer,
2016). By contrast, resprouting capacity has never been
reported for A. trifida species.
In addition to their reproductive capacity, seeds also
play a crucial role as “survival structures”deputized to
respond to environmental unpredictability and adversity,
and so confer resilience to species. Through dispersal,
seeds can allow the species to strategically escape from
unsuitable conditions. Moreover, seed dormancy leads to
a“delayed germination”that prevents the germination
of fresh seeds when the environmental parameters are
unsuitable and promotes the establishment of a soil seed
bank (Finch-Savage and Leubner-Metzger, 2006; Gioria
et al.,2016), which buffer plant populations against envi-
ronmental variability and increase the time of (local)
extinction (Thompson, 2000).
Apart from A. psilostachya, ragweed species produce
large amounts of seeds, which establishes conspicuous
soil seed banks (Table 3). For instance, the density of
seeds of A. artemisiifolia ranged from 4.5 to 536 units
per m
2
in the upper 20 cm of soil depending on the habi-
tat type (Fumanal et al.,2008b). As seeds can remain via-
ble in the soil for decades, even more than 40 years
(Toole and Browne, 1946), they can be considered as
forming long-lasting soil seed banks. However, it must
be taken into account that burial depth is crucial for the
viability of seeds, decreasing to 4 years on the soil surface
(Essl et al.,2015). Experiments and observations have
been conducted at a depth between 0 and 25 cm, which
is considered the living seed bank limit (Fumanal et al.,
2008b; Essl et al.,2015; Karrer et al.,2016). Fumanal
et al. (2008b) recorded a lower viability of seeds between
0 and 5 cm than at 5 to 15 cm. Karrer et al. (2016) con-
firmed that the deep soil condition (down to 25 cm) is
more suitable for lengthening seed viability, but differen-
ces between seeds buried at 5 and 25 cm are not so pro-
nounced as in the study by Fumanal et al. (2008b). The
authors also speculated that viability is more influenced
by seed origin and habitat than burial depth. In any case,
beyond viability, germination of seeds is strongly influ-
enced by burial depth: if seed germination is quite high
on the soil surface, it decreases with increasing depth
(below 8 cm), where parameters dramatically change
and dormancy cannot be interrupted (Essl et al.,2015).
Guillemin and Chauvel (2011) observed a decrease in
germination for seeds buried from 2 to 8 cm and null
germination between 10 and 12 cm of depth. It is likely
that with the decrease of soil depth most seeds tend to
germinate and leave a greater amount of nonviable seeds
in the upper soil. Moreover, seed mass also appears to
influence the percentage of germination, and the lightest
seeds are more sensitive to burial (Guillemin and
Chauvel, 2011). On the other hand, the time of germina-
tion is also important as demonstrated by Ortmans et al.
(2016) who showed that A. artemisiifolia seed traits have
a minimal effect, while foliage cover and above-ground
biomass (AGB) are more relevant.
Burial depth also has a determinant effect on seed ger-
mination and seedling emergency for A. trifida; germina-
tion decreases with depth after the first winter burial
period (vernalization) (Harrison et al.,2007). According
to Harrison et al. (2007), the lowest depth from which
giant ragweed can emerge is probably between 16 and
20 cm and no seedling emerges beyond 20 cm of depth.
Soil seed bank viability in A. trifida is lower than that
observed for A. artemisiifolia, as the total percentage of
germination strongly decreases after 4 years (Harrison
et al.,2007), and the combination of low viability and
high post-dispersal predation of seeds leads to a limited
effectiveness of soil seed banks in this species (Harrison
et al.,2001,2003). In any case, in suitable conditions, A.
trifida enriches its soil seed bank by repeated dispersal of
seeds year after year. Moreover, this species produces
polymorphic seeds and, in contrast to A. artemisiifolia,
their size is relevant for their persistence in soil. Even
with some exceptions, small seeds appear to be viable for
a longer than larger ones (Schutte, 2008b). Nevertheless,
the likelihood of the emergence of seedlings from large
seeds is higher at 5 and 10 cm of soil depth (Harrison
et al.,2007).
A viable soil seed bank also allows A. tenuifolia to be
more resilient to critical phases such as floods. As
reported above, the root system of this perennial species
does not survive in anaerobic conditions due to pro-
longed water coverage, while seeds remain viable.
According to Insausti and Grimoldi (2006), seeds are
released in large quantities and they can remain viable
for several years in soil seed banks. Unfortunately, infor-
mation such as germination percentage and critical
depth are not available for this species.
Seed production of A. psilostachya is very low and, in
some studies, the species was even classified as a
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nonseeded forb (Table 4; Grygiel et al.,2012). Moreover,
studies performed in tallgrass prairies and coastal areas
showed no seed of this species in the soil seed bank
(McNicoll and Augspurger, 2010; Barton et al.,2016).
Nevertheless, from samples of soils collected in North
American mixed prairies and then stored in artificial
conditions, Lippert and Hopkins (1950) observed emer-
gence of seedlings of A. psilostachya but in very low
numbers. Information about seed viability is very scarce
but is likely to be around 3 to 5 years, independent of
persistence in the soil (Barton et al.,2016). Thus,
resilience strategies in A. psilostachya do not include
soil seed banks, but the rhizome is likely to be the
target organ in overcoming stressful conditions and
disturbances.
F. Competition with local plant communities
From previous sections, it is clear that ragweed species
colonize habitats quite far from equilibrium, character-
ized by the influence of several stresses and disturbances.
They also occur in “stable”situations, but usually when
the equilibrium is determined and “arrested”by particu-
lar conditions, such as a high concentration of salt or
metal in soil. Essl et al. (2015) underlined that germina-
tion and early seedling establishment are mostly related
to disturbance and lack of competition from local com-
munities. This would explain the rarity of plants in natu-
ral habitats. As pioneer species, their life strategies are
shaped to harsh situations mostly in early successional
stages of vegetation. Accordingly, almost all biological
and functional traits of ragweeds can be related to these
less evolved environments. For instance, the need of light
intensity to break seed dormancy and the need for rather
shallow and compact soils, suitable to the growth of
seedlings from soil seed banks and resprouting from
rhizomes, are all requirements related to poorly evolved
or disturbed vegetation. The main characteristics of the
four ragweed species, related to their ability in competing
with local plants, are compared in Table 4.
Considering A. artemisiifolia, environmental condi-
tions are only suitable for its growth when human action
or natural events influence the natural evolution of vege-
tation by removing competitors or operating on soil
components (agricultural practices, excavations, floods,
etc.). Gentili et al. (2015) demonstrated that the plant is
a weak competitor in evolved stages of vegetation. These
authors showed that germination and recruitment, as
well as plant growth, are mainly inhibited by the pres-
ence of perennial and/or winter annual grassland species
characteristic of more advanced stages (Gentili et al.,
2015). In keeping with this, Fenesi et al. (2014) reported
that in a competitive regime, A. artemisiifolia seed
germination is delayed and seedling development is
restrained by the presence of heterospecific neighbors
(e.g. Erigeron spp.). They reported that on average the
cost of A. artemisiifolia biomass associated with only a
3-day emergence delay is very high (¡97%).
In contrast to A. artemisiifolia, A. trifida is usually a
good and vigorous competitor. Its life strategies are
mostly based on very rapid and relevant growth: early
germination, followed by very rapid growth, allowing the
plant to reach a height and biomass superior to other
plants. Accordingly, the growth of later growing plants is
strongly inhibited by the canopy shadow determined by
its large leaves (Abul-Fatih and Bazzaz, 1979b). There-
fore, once giant ragweed finds good conditions in which
to persist, it inhibits species diversity, biomass and den-
sity of the local community. In its native community, A.
trifida is in fact a dominant species, one that strongly
inhibits the colonization and growth of other annual
plants (Abul-Fatih and Bazzaz, 1979b). Early emergence
also ensures a timely capitalization of resources that
avoid the competition of dominant perennials as well
(Hartnett et al.,1987; Schutte et al.,2012). As A. trifida
is one of the most problematic crop weeds in the United
States, its impact on other plants is extremely evident as
shown also by the analysis of crop yield losses (Regnier
et al.,2016). Interestingly, in agricultural environments,
but not in rarely disturbed natural successional areas, A.
trifida has been reported as being able to modulate its
emergence time to adapt to different, “scheduled”selec-
tive pressures (Hartnett et al.,1987; Schutte et al.,2012;
Regnier et al.,2016). In general, environmental or
human-mediated disturbance must surely contribute to
A. trifida persistence but, contrary to A. artemisiifolia,it
does not disappear when the natural vegetation dynamic
evolves and perennials become dominant. Hartnett et al.
(1987) reported that A. trifida can persist for years, even
penetrating dense vegetation.
Similarly, perennial ragweed species, being pioneer
plants, take advantage from vegetation gaps and also per-
sist in more evolved environments when suitable condi-
tions are maintained. Nevertheless, unlike A. trifida, A.
psilostachya is not a superior competitor of grasses under
“normal circumstances,”and is in fact present in undis-
turbed, healthy pastures, but in low quantities (Vermeire
et al.,2005). Vermeire and Gillen (2000) demonstrated
that its abundance does not affect the presence of other
grasses in mixed prairies, and there is a positive correla-
tion between them. However, they speculate that West-
ern ragweed is less abundant where there are grasses
with roots forming a dense mat in the upper soil level; in
this way the vegetative propagation of the plant is inhib-
ited, as upper soil roots compete with the quite superfi-
cial creeping rhizome of A. psilostachya. Thus, the
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species only endures competition with some plants. This
is inferred by observing its allopathic effect, which only
negatively affects some species.
Again, A. tenuifolia takes advantage of gaps in vegeta-
tion covers (caused by floods, grazing, etc.) which make
light, nutrients, and water more available for seed germi-
nation and recruitment (Insausti et al.,1995; Insausti
and Grimoldi, 2006). As a result, this species is a good
competitor in poorly evolved environments, although it
usually persists in the following stage of vegetation suc-
cession where it can become co-dominant (see above).
After disturbance, gaps constitute focal points where
recolonization of the grassland by A. tenuifolia originates
from seedlings, which initially have a slow growth phase.
It then grows rapidly and continues outside the original
gaps by lateral clonal expansion, thus allowing the spe-
cies to occupy new areas. In any case, independent of the
starting population’s abundance, the species multiplies
many times the surface of colonization in the quite short
time of about 4 months (Insausti and Grimoldi, 2006).
VI. Reproductive and dispersal barriers
Survival without reproduction reduces an exotic species
to a casual alien taxon as it cannot reach the naturaliza-
tion phase (Blackburn et al.,2011). In this section, repro-
ductive and dispersal strategies (also human-mediated)
of ragweed species are analyzed. Dependence on special-
ized pollinators or particular requirements within
reproduction phases (e.g. obligatory outcrossing) are
often indicated as traits that prevent the establishment of
plants in new ranges (Van Kleunen et al.,2015). In gen-
eral, when a species does not encounter unfavorable fac-
tors that strongly limit reproduction, the road to
establishment is much less difficult. As already seen, the
life cycle of ragweed species includes a series of adapta-
tions useful in avoiding adversity. However, the chance
of easily shifting its range through reproductive structure
dispersal can be a positive trait determinant in facing
unpredictability and escaping unfavorable conditions
(Estrada et al.,2016).
A. Pollination
In ragweed species, flowers are organized in heads con-
taining either male or female flowers. The pollen-pro-
ducing male raceme grows at the tips of the principal
stem and lateral branches; seed-producing female heads
containing one or a few pistillate flowers are sessile and
situated in the axils of the leaves immediately below the
staminate spikes (Smith et al.,2013). According to Smith
et al. (2013), within the Asteraceae family, ragweeds pos-
sess a strongly modified inflorescence, highly adapted to
wind pollination (Table 5). As highlighted by Franz Essl
and co-authors (2015), A. artemisiifolia is strongly self-
incompatible and has high outcrossing rates, both in its
invasive and native ranges. This may limit its reproduc-
tive efficiency, but due to the large production of
Table 5. Reproduction and disperasal of Ambrosia species (ragweeds): relevant data in understanding the reproductive and dispersal
potential of ragweeds.
Species
Ambrosia
artemisiifolia L.
Ambrosia
trifida L.
Ambrosia
psilostachya DC.
Ambrosia tenuifolia
Spreng.
Pollination Anemophylous Anemophylous Anemophylous Anemophylous
Reproduction Sexual Sexual Sexual Sexual
Vegetative Vegetative Vegetative Vegetative
Seed dimension 3.5 mm long more than 6 mm long 3–4.5 mm long 3–5 mm long
Seed production Very high Very high Very high Very high
High High High High (?)
Scarce Scarce Scarce Scarce
Seed predation Existing Existing Existing Existing?
Highly relevant Highly relevant Highly relevant Highly relevant
No evidences No evidences No evidences No evidences
Germination
requirements
Vernalization Vernalization Vernalization Vernalization
Light Light Light Light
Soil moisture Soil moisture Soil moisture Soil moisture
Primary seed dispersal Barochory Barochory Barochory Barochory
Secondary seed
dispersal
Anemochory Anemochory Anemochory (?) Anemochory (?)
Epizoochory Epizoochory Epizoochory Epizoochory
Endozoochory Endozoochory Endozoochory (?) Endozoochory
Hydrochory Hydrochory Hydrochory Hydrochory
Human-mediated
dispersal (medium/
long-distance)
Movement of soils Movement of soils (?) Movement of soils (?) Movement of soils (?)
Mowing or agricultural
machinery
Mowing or agricultural
machinery (?)
Mowing or agricultural
machinery (?)
Mowing or agricultural
machinery (?)
Car and train passage Car and train passage (?) Car and train passage (?) Car and train passage
Grain, vegetables, fodder, bird
food and oil-seeds
commercial exchanges
Grain, vegetables, fodder, bird
food and oil-seeds
commercial exchanges
Grain, vegetables, fodder, bird
food and oil-seeds
commercial exchanges
Grain, vegetables, fodder, bird
food and oil-seeds
commercial exchanges
The characteristic of each species is highlighted in gray and doubtful attributions are signaled by “(?)”.
160 C. MONTAGNANI ET AL.
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airborne pollen, genetic flux is also maintained between
distant or isolated populations. Unfortunately, there is
no information about the other ragweed species concern-
ing this.
B. Seed and propagule pressure
In the literature, the term “seed”usually indicates the
whole diaspore unit of ragweed, which is a one-seeded
cypsela for the species considered. The characteristics of
ragweed seeds are shown in Table 5. It can be observed
that A. trifida produces the largest seeds (more than
6 mm long) with a consistent outer coat (Bassett and
Crompton, 1982). The other ragweed species produce
smaller seeds: seeds of A. tenuifolia are slightly larger, 3
to 5 mm long (Parsons and Cuthbertson, 2001; Beh¸cet,
2004), than those of A. artemisiifolia (»3.5 mm long)
(Bassett and Crompton, 1975) and A. psilostachya (3 to
4.5 mm long) (Table 5) (Barton et al.,2016).
Propagule pressure of common ragweed can be very
high because the species produces between 3,000 and
100,000 seeds per plant, depending on the size of individ-
uals and thus on growth conditions (Dickerson and
Sweet, 1971; Bassett and Crompton, 1975;https://gd.
eppo.int/reporting/article-3032; Fumanal et al.,2007).
Seed production is also quite noteworthy for giant rag-
weed and varies between a few hundred and 5000ca.
units per plant, depending on plant density and environ-
mental conditions (Abul-Fatih and Bazzaz, 1979a;
Baysinger and Sims, 1991; Harrison et al.,2001;
MacDonald and Kotanen, 2010). Nevertheless, unlike A.
artemisiifolia, the potential dissemination of this species
in its native range can be strongly reduced by a relevant
post-dispersal predation by rodents and invertebrates
(Harrison et al.,2003; Regnier et al.,2008). Moreover,
the viability of its seeds is not very high, 50% to 66%
(Goplen et al.,2016; Harrison et al.,2001).
In contrast to common and giant ragweed which,
being annual species, have seeds as their main dispersal
units, Western and slender ragweed are perennial and
show additional dispersal structures. Wagner and Beals
(1958) observed that only 66 out of 118 flowering heads
developed to maturity in one plant and speculated that
the reproductive potential by seeds of A. psilostachya is
six times less than that of A. artemisiifolia. Similarly, Bas-
set and Crompton (1975) showed that A. psilostachya
produces just one seed per flowering head, thus indicat-
ing that vegetative reproduction is predominant for the
species. In agreement with this, the main dispersal struc-
ture of the species is its highly vigorous creeping root
system, capable of sprouting from pieces of rhizome,
which make this ragweed species an even harder weed
to fight than common ragweed (Table 5). Vegetative
reproduction through rhizomes is also relevant for A.
tenuifolia, even though it produces a large number of
seeds (Table 5; Insausti and Grimoldi, 2006). Indeed, in
this species both these strategies are important for its
success in different stages of its life, as they react to dra-
matic environmental events, such as floods that are fre-
quent on the Pampean Plains or human pressures such
as agriculture and grazing (Insausti and Soriano, 1987;
Insausti et al.,1995; Insausti and Grimoldi, 2006;
Soriano, 1982). As already discussed in previous sections,
the rhizome of A. tenuifolia is less resistant to extreme
conditions (i.e. anoxia due to floods) than seeds that
showed a longer viability (Insausti and Grimoldi, 2006).
Furthermore, there is no evidence of enemies in the
native range that affect the persistence and productivity
of this plant, given its toxicity or unpalatability to cattle
and the low dietary interest for other vertebrates such as
rodents (Freire et al.,2005; Semmartin, 2010; Ellis et al.,
1998).
C. Dispersal
Regarding ways of dispersal relevant to local movements
(medium-short-range dispersal in native and invasion
range), ragweed seeds show no morphological structure
strictly representing a specific dispersal vector. Accord-
ing to Basset and Crompton (1975), the primary way of
dispersal of A. artemisiifolia seeds is barochory. Anemo-
chory is often cited as a potential dispersal vector, but
owing to the absence of suitable structures and the
weight of seeds, wind may represent only a “facilitator”
of spread rather than a driver of diffusion (Table 5;
Bullock et al.,2012). Zoochory and hydrochory (Table 5)
were considered by Essl et al. (2015), who reviewed all
vectors contributing to A. artemisiifolia diffusion.
Regarding the first, epizoochory by bison was proven in
the native range of common ragweed, and endozoochory
was also reported as an additional plausible mechanism
of dispersion (Rosas et al.,2008; Bullock et al.,2012).
Viable seeds of common ragweed resulting from feed
intake have been found in cattle manure both in the
United States and Europe (Pleasant and Schlather, 1994;
Vitalos and Karrer, 2008). In addition, Wright, (1941)
and Vitalos and Karrer (2008) proved that seeds are part
of the diet of some birds (e.g. sparrows, pheasants, and
quails), and Essl et al. (2015) reported that these vectors,
along with rodents, play a role in dispersal. Hydrochory
(intended both as streams, flowing water, and as runoff),
has been indicated as a way of dispersal in the native
range of the species (Table 5; Payne, 1970). Recently,
Fumanal et al. (2007) underlined how the polymorphism
of seeds of A. artemisiifolia contributes to dispersal
by flowing water and indicated this mechanism as
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fundamental in the spread of the taxon within France,
and also as a long-distance means of diffusion.
Compared to A. artemisiifolia and the other ragweed
species considered, A. trifida produces the largest seeds,
reaching almost 1 cm in length (Bassett and Crompton,
1982). Seed size and weight point to barochory are the
main way of dispersal for this species also (Table 5).
However, Osawa et al. (2013) indicated hydrochory and
zoochory as additional important mechanisms for A. tri-
fida diffusion, mainly supporting the former in accor-
dance with the shape and size of the seeds. Yoshikawa
et al. (2013) demonstrated that owing to its weight, a
giant ragweed seed transported by a stream settles quite
rapidly when the current velocity decreases, thus suggest-
ing that these seeds are transported by water flow rather
than floating. Concerning zoochory, although giant
ragweed seeds have a quite developed crown of large
spines, their size and weight represent a limiting factor
for epizoochory. Hejny and Jel
ık(1972) mentioned the
presence of A. trifida seeds in wool scraps, but as an
exceptional circumstance in the former Czechoslovakia.
In addition, Verloove (2016a) reported that it is rarely
seen as a wool alien in Belgium and Py
sek (2005)
excludes the possibility that A. trifida dispersal could be
associated to wool processing in Czech Republic. As
already mentioned, owing to their palatability, rodents
and invertebrates eat seeds (Harrison et al.,2003,2007),
but if they cached instead of being immediately eaten
then post-dispersal predation allows an estrangement of
viable seeds from the mother plant. An association
between A. trifida and earthworms has only very recently
been observed: in the native range of A. trifida, nonnative
earthworms (Lumbricus terrestris) cache its seeds in
burrows. Beyond the benefits for the plants (reduction of
fast seed predation), giant ragweed appears to increase
dispersal opportunities through this acquired form of
diplochory (Regnier et al.,2008,2016; Schutte et al.,
2010). However, it allows a very short-range transloca-
tion, probably less than one meter from the mother
plant, considering the homing capability and movements
of earthworms (Nuutinen and Butt, 2005).
Little information is available regarding A. psilosta-
chya. However, considering that its seeds are slightly
larger than those of A. artemisiifolia (Basset and
Crompton, 1975), it is likely that this species also mainly
disperses through barochory (Table 5). Moreover, the
crown of rudimental spines is less developed or even
absent in Western ragweed seeds compared to those of
common ragweed, which suggests that epizoochory is
probably not as important a dispersal mechanism in this
species (Wagner and Beals, 1958). However, Amor
Morales et al. (2012) and Parsons and Cuthbertson
(2001) cited epizoochory for A. psilostachya seed
dispersal in Spain and Australia, respectively. Finally,
although the species is not highly palatable to cattle or
bison, endozoochory was also inferred by Rosas et al.
(2008), who found a percentage of Ambrosia spp. seeds
in dung of bison grazing in prairies where A. psilostachya
was a common forb. In any case, although studies about
the role of Western ragweed seed intake in bird diets
have been published (Campbell-Kissock et al.,1985),
clear evidence of seed dispersal by animals is yet to be
collected, as well as other means of diffusion. For
instance, CABI (2017) reported that in springtime A. psi-
lostachya seed can be “transferred by water in ditches,
canals and rivers”(hydrochory). Moreover, as discussed
above, seeds are probably not the main dispersal unit of
Western ragweed, owing to their paucity, but the role of
rhizome fragmentation is yet to be investigated.
Like A.psilostachya,A.tenuifoliais a perennial, but its
life strategy is not mainly based on vegetative propagation
and seed production is not low, although data on the pre-
cise quantity are not available. No real evidence for epi-
zoochory is present in literature, but several sources stress
the evidence that seeds are caught on sheep wool (http://
www.environment.gov.au/cgi-bin/biodiversity/invasive/
weeds/weeddetails.pl?taxon_id D17510#). Available stud-
ies suggest that seeds can be dispersed by water flow
without losing their viability (Insausti and Soriano, 1982;
Insausti et al.,2006).
D. Human-mediated dispersal pathways (medium-
and long-distance vectors)
Trade routes and all connected elements, previously dis-
cussed as important pathways of introduction and global
diffusion, are relevant for short- and medium-range
movements (Table 5; Ferus et al.,2015). Nevertheless, on
a regional scale, further important vectors of spread
linked to human activity stand out: movement of soils,
spread of seeds through mowing or agricultural machin-
ery and car and train passage (Table 5). All these vectors
are associated with the spread of A. artemisiifolia partic-
ularly within the European area as extensively reviewed
by Bullock et al. (2012) and Essl et al. (2015). The pres-
ence of common ragweed in a new area, after the set up
of a construction site, can easily be attributed to the
transport and dumping of contaminated soils from
different sites. Moreover, the abundance of common
ragweed along railways and road networks indicates
transportation corridors as one of the main drivers of
introduction. The importance of which is even more
stressed by the explanatory power of this variable in spa-
tial distribution models and other studies (e.g. Dullinger
et al.,2009 and Joly et al.,2011). However, few experi-
mental data about the dispersion mechanism of
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propagules are available. Two studies (Vitalos and
Karrer, 2009; Von der Lippe et al.,2013) tested the effect
of vehicles on dispersion of seeds and both demonstrated
that the sole car slipstream or seed attachment cannot
completely explain a long-distance dispersal. Even the
action of mowing machines along roads, which strongly
boosts the process, does not fully explain the distance of
dispersal (Vitalos and Karrer, 2009). As a result, the
spread of A. artemisiifolia along corridors of transporta-
tion appears to be a multifactorial phenomenon not yet
completely understood. Regarding the impact of agricul-
tural machinery, it is effective at the local and more
extended level. Karrer (2014) demonstrated that harvest-
ers and other machines can transport several thousands
of viable seeds, colonizing new fields or reinforcing
already present metapopulations of common ragweed.
Contaminated machines from already colonized French
regions are even thought to be responsible for the intro-
duction of A. artemisiifolia into some virgin Swiss areas
(Buttenschøn et al.,2010).
All these vectors may also be relevant for the other
species of ragweeds, and especially for A. tenuifolia and
A. psilostachya as light-seed producers (Table 5). Con-
versely, A. trifida produces large seeds and may exploit
these vectors less (Table 5). The transport of viable rhi-
zomes through soil movements may also be an effective
vector for the diffusion of A. psilostachya, but unfortu-
nately, no evidence for this is available.
VII. Allergenic impact and environment
The Ambrosia genus represents a global risk to public
health owing to the allergic reactions induced by pollen
allergens in atopic subjects. In Europe, ragweed pollen
affects more than 36 million people each year and the
prevalence of sensitization is growing mainly due to the
plant’s spread (Mihajlovic, 2015; Bordas-Le Floch et al.,
2015). Among all ragweed species, pollen of A. artemisii-
folia, A. psilostachya, and A. trifida have long been
acknowledged as a significant cause of allergic disease
(Ziska et al.,2011). Similarly, A. tenuifolia is reported to
be severely allergenic in its native range and produces a
huge amount of pollen (Giscafre and Ragonese, 1942;
Vaz Ferreira, 1946; Tejera and Beri, 2005; Del Vitto
et al.,2015; pollenlibrary.com). However, more specific
and up-to-date medical evidence needs to be collected to
better define the allergenic impact of this species (Tejera
and Beri, 2005; Marco and Pirovani, 2009).
A. Pollen characteristics related to allergy
The major source of allergenic proteins in ragweed plants
is pollen. Ragweed pollen grains are small particles
containing air chambers between the layers of the outer
wall. These characteristics allow them to become easily
airborne under favorable conditions and transported by
wind for very long distances at a continental scale, even
reaching areas not colonized by Ambrosia spp. plants
(Smith et al.,2013; Mahmoudi, 2016;
Sikoparija et al.,
2013). It is striking that these pollen grains maintain
their allergenic power over such long distances, even
after spending many days in the atmosphere (Makra
et al.,2016; Grewling et al., 2016). This means that
exposed individuals may become sensitized to ragweed
pollen allergens and develop symptoms even in areas
where the plant is not widely distributed (Grewling et al.,
2016). Furthermore, sub-pollen particles of respirable
size (0.5 to 4.5 mm) contain allergens that can be released
by A. artemisiifolia pollen after hydration (i.e. after thun-
derstorms). These particles, along with pollen fragments,
can also be transported for long distances, thus contrib-
uting to allergen exposure even when no airborne pollen
grains are identifiable. This generates out-of-season pol-
linosis in highly ragweed-sensitive subjects (Table 6)
(Busse et al.,1972; Bacsi et al.,2006; Pazmandi et al.,
2012).
The species’morphological characteristics are similar
(Table 6) and identifying pollen grains with a single spe-
cies by optical microscopy is not usually feasible. A few
authors have investigated the pollen structure of ragweed
species other than A. artemisiifolia. They show that A.
psilostachya pollen grains are likely to be larger than the
other species (Table 6) (Jacobson and Morris, 1976;
Robbins et al.,1979; Wan et al.,2002) and that A. arte-
misiifolia pollen is distinguishable from that of A. trifida
through the analysis of exine characters. Specifically, Bas-
sett and Crompton (1982) reported that A. trifida has 60
to 65 spines on one-half of the grain surface, whereas A.
artemisiifolia has 70 to 75 spines. No distinctive traits
are reported for A. tenuifolia pollen.
B. Pollen allergens
The allergens of the four ragweed species officially
recorded by the International Union of Immunological
Societies (IUIS) are shown in Table 7. The pectate lyase
Amb a 1 is currently considered the most important
allergenic group for the genus Ambrosia (Gadermaier
et al.,2014), although it has been identified only in A.
artemisiifolia and not in the other species. Concerning
A. artemisiifolia, ten different allergen groups are
reported in the IUIS database and they were extensively
reviewed by Gadermaier et al. (2014) and Bordas-Le
Floch et al. (2015). Briefly, the list includes: Amb a 1
(comprising the formerly called Amb a 2, recently desig-
nated as Amb a 1 isoallergen 5), to which more than
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95% of ragweed pollen-allergic patients are sensitized;
Amb a 3, classified as a minor allergen (sensitization
prevalence of 30% to 50%); Amb a 4 (defensin), to which
sensitization frequencies are variable; Amb a 5 (unknown
function) a minor allergen, affecting only 10% to 15% of
ragweed pollen-allergic individuals; the panallergen Amb
a 6 (nonspecific lipid transfer protein) which is consid-
ered a minor allergen (sensitization prevalence of 21%
among ragweed sensitized patients); Amb a 7 (plastocya-
nins), another minor allergen (reaction in 15% to 20% of
Table 6. Allergenic potential of Ambrosia species (ragweeds): relevant elements of plants contributing to determine and increase allergy
reaction.
Species Ambrosia artemisiifolia L. Ambrosia trifida L. Ambrosia psilostachya DC. Ambrosia tenuifolia Spreng.
Allergenic parts of plant Pollen Pollen Pollen Pollen
Plant debris Plant debris Plant debris Plant debris
Pollen dimension 18–22 mm 19.25 mm21–23 mm up to 26.4 mm?
Cross-reactivity Amb a 5 and Amb t 5 Amb a 5 and Amb t 5 Amb a 5 and Amb p 5 Poorly known
Factors increasing impact Long-distance transport
of pollen
Long-distance transport
of pollen (?)
Long-distance transport
of pollen (?)
Long-distance transport
of pollen (?)
Atmospheric pollution Atmospheric pollution(?) Atmospheric pollution (?) Atmospheric pollution (?)
Warming climate Warming climate Warming climate Warming climate (?)
Disturbance Disturbance (?) Disturbance Disturbance (?)
Pollen grain
(from Robbins et al.,1979)
—
Elements of each species are highlighted in grey.
Table 7. Allergens in Ambrosia species (ragweeds).: characteristics of identified allergens of each analyzed species.
Allergen
*
Isoform
*
MW(SDS-PAGE) (kDa)
*
Theoretical pI
**
Biological function
*
Allergenic potential (%)
*
Ambrosia artemisiifolia L.
Amb a 1 Amb a 1.0101 38 5.58 Pectate lyase 97
Amb a 1.0201 6.63
Amb a 1.0202 6.63
Amb a 1.0301 5.72
Amb a 1.0302 5.72
Amb a 1.0303 5.79
Amb a 1.0304 5.79
Amb a 1.0305 5.79
Amb a 1.0401 5.61
Amb a 1.0402 5.22
Amb a 1.0501 6.00
Amb a 1.0502 5.79
Amb a 3 Amb a 3.0101 11 6.11 Plastocyanin 51
Amb a 4 Amb a 4.0101 30 4.88 Defense-like protein Unknown
Amb a 5 Amb a 5.0101 5 8.19 unknown 10–20
Amb a 6 Amb a 6.0101 10 8.93 Lipid Transfer protein (LTP) 21
Amb a 7 Amb a 7.0101 12 —Plastocyanin 15–20
Amb a 8 Amb a 8.0101 14 4.79 Profilin 35
Amb a 8.0102 4.88
Amb a 9 Amb a 9.0101 10 4.17 Polcalcin 10–15
Amb a 9.0102 4.15
Amb a 10 Amb a 10.0101 18 4.25 Polcalcin-like protein 10–15
Amb a 11 Amb a 11.0101 37 kDa (natural purified mature
protein), 52 kDa (natural
purified zymogen)
6.43 Cysteine protease 54
Ambrosia psilostachya DC.
Amb p 5 Amb p 5.0101 Unknown Unknown
Amb p 5.0201
Ambrosia trifida L.
Amb t 5 Amb t 5.0101 5 Unknown 5
Source:
IUIS;
ExPASy.
164 C. MONTAGNANI ET AL.
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ragweed pollen-allergic patients); Amb a 8 (profilin),
highly cross-reactive with mugwort (Artemisia) profilin
(Art v 4); Amb a 9/Amb a 10 (polcalcins), minor panal-
lergens (reaction in 10% to 15% of ragweed pollen-
allergic patients). Finally, the list includes the very
recently discovered allergen Amb a 11 (cysteine
protease), which has been classified as one of the major
allergens along with Amb a 1 for this ragweed species
(Bouley et al., 2015). Additional IgE-reactive pollen
proteins, identified by trascriptomic and proteomic
approaches, have been indicated as “bona fide allergens,”
probably extending the list of A. artemisiifolia allergens
(Bordas-Le Floch et al.,2015).
In contrast to A. artemisiifolia, A. trifida and A.
psilostachya allergens are less characterized. Only two
(Amb t 5, Amb t 8) and one allergenic proteins (Amb
p 5) have been identified respectively in A. trifida and A.
psilostachya, and reported in IUIS and/or allergome
databases. Amb t 5 and Amb p 5 belong to the fifth
group of allergens of the genus Ambrosia and cross-react
with Amb a 5. In A. psilostachya, two isoforms of Amb p
5, Amb p 5.0101 and Amb p 5.0201, have been character-
ized. Ghosh et al. (1994) investigated the variants of
Amb p 5 from A. psilostachya pollen and suggested that
these forms are part of the natural variation within the
A. psilostachya species, which exhibits polyploidy and
can form hybrids with related ragweed species. Amb t 8
is a profilin, an actin binding proteins (Girodet, 2013).
However, these data are not present in the IUIS database
and only scanty information about it is available.
A. artemisiifolia, A. trifida, and A. psilostachya pollen
allergens have long been considered largely cross-reac-
tive (Weber et al.,2007), and it is generally believed that
one species is sufficient for skin testing and immunother-
apy. However, in the northern area of Milan (widely
invaded only by A. artemisiifolia), about 50% of patients
submitted to injection of specific immunotherapy with
A. trifida showed little or no clinical response, although
an excellent outcome was obtained if they were shifted to
A. artemisiifolia-specific immunotherapy (Asero et al.,
2005). By comparing the proteome of A. artemisiifolia
with those of A. trifida and A. psilostachya, Barton and
Schomacker (2017) recently found that only A. psilosta-
chya pollen contains all five Amb a 1 isoallergens identi-
fied in A. artemisiifolia and reported in the IUIS
database. In contrast, they found only three Amb a 1 iso-
allergens (Amb a 1.2, Amb a 1.4, and Amb a 1.5) in A.
trifida, the lesser IgE-reactive isoforms. Although more
specific analyses are needed to characterize the allergenic
profile of these species, this information suggests that A.
artemisiifolia is more similar to A. psilostachya than to
A. trifida, thus explaining the results reported by Asero
and collaborators (2005). The allergenicity of A.
tenuifolia is still poorly known (no allergens are reported
in allergen databases), but it shows little cross-reactivity
with the other Ambrosia species (Girodet, 2013).
C. Allergenic impact and environment
Regarding quantities of pollen, ragweed has the potential
to release billions of pollen grains: for A. artemisiifolia it
is well known that 1.19 §0.14 billion pollen grains can
be released per plant (Fumanal et al.,2007; Smith et al.,
2013). However, pollen production is closely related to
size, growth, phenology, and fitness of plants. For A.
artemisiifolia, there is a positive correlation between dry
plant biomass and reproductive success, as bigger
individuals produce more pollen grains (Fumanal et al.,
2007), although decreasing plant size is generally associ-
ated with increasing maleness and decreasing femaleness
(Paquin and Aarssen, 2004). Biomass and flowering phe-
nology can follow a latitudinal gradient (Allard, 1945;
Dickerson, 1968; Leiblein Wild, 2014): both in Europe
and North America, plants from southern populations
grow larger and flower later than northern populations
(e.g., Gudzinskas, 1993;Liet al.,2015). The time of
flowering greatly depends on germination time and the
average springtime temperature (April, May and June)
(Kazinczi et al.,2008); for instance, it has been shown
that earlier germination during spring leads to higher
biomass allocation and higher pollen and seed produc-
tion. Consequently, environmental conditions can alter
plant fitness and result in pollen production change
(Smith et al.,2013). It is worth noting that adaptations
to newly invaded environments (e.g. Europe) often have
a positive effect on the fitness of plants, reproduction,
and biomass allocation as well as influencing the length
of flowering time (Hodgins and Rieseberg, 2011; Leiblein
Wild, 2014).
Furthermore, pollen production is influenced directly
or indirectly by human practices. Sensitization of the
population to A. artemisiifolia is constantly increasing
and is probably correlated with the increased civilization,
urbanization, and pollution of the last decades
(D’Amato, 2007; Ghiani, 2012). Several studies warn that
global changes are going to worsen the situation in the
next few decades. Effects will include changes in ragweed
distribution, plant growth, and life cycle as well as pollen
allergenicity itself (e.g. Ziska and Caulfield, 2000; Rogers
et al.,2006). Species Distribution Models (SDMs) for A.
artemisiifolia predict that its potential distribution will
increase globally (Essl et al.,2015; Chapman et al.,2016).
In Europe, warmer summers and later autumn frosts will
allow a spread of A. artemisiifolia northward and uphill,
leading by the mid-21st century to the inclusion of
northern areas (e.g. southern Scandinavia and the British
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Isles) in its climatically suitable regions, and southward a
regression of the species’range. Regarding the genus
Ambrosia in North America, Ziska et al. (2011) showed
an increase in recent decades (since 1995) of the duration
of the ragweed (Ambrosia spp.) pollen season as a
function of latitude (latitudinal effects are primarily asso-
ciated with a delay in first frost of the fall season and
lengthening of the frost free period). A. trifida in China
is predicted to slightly increase its range (<1%) although
it had the potential to spread northward (Qin et al.,
2014). Recently Rasmussen et al. (2017) found that, by
the year 2100, the distribution range of A. artemisiifolia,
A. trifida, and A. psilostachya will increase toward
Northern and Eastern Europe under all climate scenarios
and consequently the high allergy-risk areas will expand
in Europe. Effects of the increase in temperature influ-
ence the flowering season length, but also the growth of
plants and pollen production. Wan et al. (2002) tested
the effects of warming and mowing on A. psilostachya,
and showed that both can increase AGB, and the ratio of
ragweed AGB to total AGB. With warming, total pollen
production increased by 84% because ragweed stems
were more abundant. Moreover, experimental warming
significantly increased pollen diameter (13% increase).
El Kelish et al. (2014) demonstrated that both an elevated
level of CO
2
and drought stress have an effect on A. arte-
misiifolia pollen allergenicity because expressed sequence
tags encoding allergenic ragweed proteins increased
under those conditions. Zhao et al. (2016) showed the
direct influence of elevated NO
2
on the increased
allergenicity of ragweed pollen and Ghiani et al. (2012)
demonstrated that traffic-related pollution enhanced rag-
weed pollen allergenicity, showing that pollen collected
along high-traffic roads had a higher whole allergenicity
than pollen from low-traffic roads and vegetated areas.
Conversely, several studies have shown no effect on the
content of the major ragweed allergen Amb a 1 due to high
concentrations of ozone or extended exposure of the plant
to this pollutant (S
en
echal et al.,2015;Kanteret al.,2013).
VIII. Conclusion
The successful invasion of the ragweed species considered
can be ascribed to a synergy of anthropogenic and bio-
ecological factors. The globalization of commerce and
changes in land use have dramatically favored their spread
into new areas. Firstly, the species were used as medicinal
plants in the Americas and were transported to Europe
and cultivated in botanical gardens. They then spread as a
contaminant of crop and forage seeds, and in a wide vari-
ety of goods, by means of transportation, to become nox-
ious pests. Climatic changes are predicted to worsen the
impact of these species by increasing both their
colonization range and allergenic potential. Thus, the set-
ting up of effective measures to prevent and stop their
spread is essential. Until now, researchers have mainly
focused on common ragweed, the most widespread spe-
cies, and the results have often been automatically associ-
ated with the other three species, although their ecology,
biology, and allergenic and ecological impact can differ
significantly. Although other ragweeds are less widespread
globally than A. artemisiifolia, their impact could differ in
terms of type and magnitude. For instance, A. psilosta-
chya,A.tenuifolia,andA. trifida are able to colonize envi-
ronments different from A. artemisiifolia,thuspotentially
expanding their range of impacts as one of the most
“black-listed”genera in the world. For this reason, further
research efforts and data collection about factors that have
allowed ragweed species to overcome geographical and
environmental barriers are needed. Specifically, more in-
depth research is necessary about:
The impact, biology, and ecology of ragweeds other
than A. artemisiifolia, which may represent a severe
threat to local plant communities, given their ability
to colonize semi-natural habitats;
dispersal vectors and introduction pathways and
their role in the spreading of taxa, with a particular
focus for the rhizomatous “low-seed producer”A.
psilostachya;
allergenic impact of ragweed species other than A.
artemisiifolia;
taxonomy of ragweeds to clarify their distribution
and relations among them;
competition mechanisms and strategies with local
plant communities (all ragweed species).
In conclusion, “for a fistful of ragweeds”a great deal of
work has been done, but it is mandatory to remain alert
and not underestimate the role of basic research in elaborat-
ing consistent strategies and models (e.g. SDMs) for better
understanding and controlling of the ragweed invasion.
ORCID
C. Montagnani http://orcid.org/0000-0003-2030-2535
R. Gentili http://orcid.org/0000-0002-9332-7963
M. Smith http://orcid.org/0000-0002-4170-2960
Funding
The research has been funded by Fondazione Banca del Monte
di Lombardia (2016-NAZ-0144).
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