Euphytica (2006) 148: 203–216
DOI: 10.1007/s10681-006-5951-7
C
Springer 2006
Selection strategies to reduce invasive potential in introduced plants1
N.O. Anderson∗ , S.M. Galatowitsch & N. Gomez
Department of Horticultural Science, University of Minnesota, 305 Alderman Hall, 1970 Folwell Avenue St. Paul,
MN, USA (∗ author for correspondence: e-mail: [email protected])
Key words: breeder trials, crop domestication, crop ideotypes, floriculture crops, invasive species, ornamentals,
plant breeding, plant competition, risk assessment
Summary
The crop domestication process is examined from plant collection to product release for various junctures at which
deliberate breeding, selection, and crop transformation may occur to prevent invasive potential. Four primary juncture opportunities for research on techniques and development of selection procedures for non-invasiveness include:
The Plant Exploration Phase, Initial Trial Phase, Fast-Tracking Phase, Selection and Improvement Phase. Avoiding
the collection of germplasm that appears weedy during plant exploration is an obvious, yet cost-effective way to
reduce invasiveness in a selection program. During initial trials, comparing genotypic differences in traits related
to invasiveness should allow plant breeders to identify cultivars that pose the least risk before undertaking comprehensive field trials. Genotypes with high commercial value, considered candidates for “fast-tracking”, should
only advance quickly to product release if they exhibit a minimum level of invasive risk, i.e., species with low
dispersal capacity and that have little potential to impact ecosystems. Fast-growing taxa, those with high seed
production, ones likely to be rapidly dispersed by wind, animals, water or people, and others that can significantly alter nutrient or light levels are examples of species that should not be “fast-tracked”. Field trials that have
typically been used to evaluate performance of genotypes across a broad range of cultivated environmental conditions need to be expanded to adequately evaluate invasive potential during the selection and improvement phase.
Testing in environments that mimic conditions where introductions could naturalize is crucial, as are evaluations
of competition with indigenous species. The time and resource investment needed to conduct adequate trials at
this stage is potentially very high; more research is needed to ensure the trials conducted are targeting important information gaps for decision-making. Additional research is also needed to develop modeling approaches
that effectively forecast long-term dynamics of introductions and to assist in developing field testing priorities.
Minimizing invasive potential could significantly reduce introductions that cause inadvertent damage to landscapes and ecosystems. The strategy proposed here will require further development, especially in the context
of understanding and assessing risks of pre- and post-release strategies for minimizing damage from invasive
species.
Introduction
Crop domestication is widely understood to be one of
the main pathways increasing the rate and geographic
1 Scientific Paper No. 051210156 of the Department of Horticultural
Science.
scope of biological invasions (Reichard & White,
2001). More frequently now than in the past, the potential adverse impacts of a new crop spreading uncontrollably across landscapes are being weighed against the
anticipated benefits (Barbier & Knowler, Kaiser in this
issue). Understanding how to best assess and manage
risks associated with species introductions is actively
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being addressed by ecologists, economists and policymakers, as evidenced by the articles included in this
special issue of Euphytica (Martinez-Ghersa & Ghersa,
McNeely, for example).
In contrast, there has been very limited involvement
in invasion risk assessment by plant breeders who are
the professionals directly involved in the collection, development and release of new crops that could become
invasive. Only a few breeding programs include noninvasiveness as an objective. All are in the public sector,
including the herbaceous perennial breeding program
at the University of Minnesota (Gaura lindheimeri;
Anderson, 2001, 2004d; Anderson & Gomez, 2004),
the University of Arkansas (Buddleja; Lindstrom
et al., 2002; Mecca et al., 2003), the Landscape
Plant Development Center (Spiraea bumalda, Potentilla fruticosa, Rosa × hybrida; http://lpdc.coafes.
umn.edu/Plant%20Breeding.htm), the U.S. National
Arboretum (Rose-of-Sharon, Hibiscus syriacus; Egolf,
1970, 1988), and the woody landscape tree/shrub
breeding program of the Hebrew University (various
woody perennials; Avishai, 2005). Some private sector
breeding programs may focus on non-invasiveness, although the companies and objectives/crops involved
are proprietary and unpublished (Corr, 2005, pers.
comm.). Private sector plant breeding programs have
released sterile cultivars (triploids) created by interspecific crosses between taxa differing in ploidy levels
to prevent competitors from creating competing cultivars (c.f. Anderson et al., in this issue). Such sterile products may be subsequently advertised as ‘noninvasive’ but are not, to the best of our knowledge,
the direct result of a breeding objective to reduce invasive potential. The invasive potential of commercial cultivars, e.g. Nandina domestica (Knox et al.,
2004) is under study by research programs not involved in breeding, although such information has not
translated directly into breeding objectives by breeding
programs.
Clearly, there is a critical need for research by plant
breeders, geneticists, and molecular biologists to study
how their plant breeding programs may implement selection procedures or develop crop hybrids with traits
which can aid in a priori reduction or elimination of
invasiveness. Intentionally introduced crops are bred
and selected for superior performance and survival in
target environments (Lonsdale, 1994) and thus, are
likely to have a greater probability of invasion than
non-crop species that are unintentionally introduced.
Crops that result in greater economic benefit are consequently marketed and distributed at a global scale,
thereby increasing the chances of invasion (Enserink,
1999). Integrating the principles of plant breeding and
genetics with those of ecology and economics is critical for reducing the risks of invasion while retaining
market value of new plant releases.
While other agriculture and horticulture sectors are
also involved in new crop development, the floriculture
industry can be used as an example to illustrate the possible creation and flow of invasive crops through the
commercial trade and how plant breeders may aid in
preventing their creation and spread during the domestication phase. Floriculture is the sector of horticulture
dedicated to the production of flowering and foliage
potted plants, cut flowers and foliage, annual bedding
plants and herbaceous perennials (Janick, 1999; Janick & Simon, 1993). A resurgence in the interest for
new crop domestication has resulted in the introduction of more than 100 new floriculture crop species in
the past decade (Anderson, 2001); this rate is unlikely
to decline (Anderson, 2004a). These new crops are introduced by amateur or professional plant explorers,
private sector flower breeders in breeding companies,
or public sector flower breeders in research programs
(Figure 1). Once new products enter the distribution
channel, marketing and sales forces of the distributors
begin creating the demand among commercial wholesale growers, retailers, landscape designers, turf specialists, and consumers through marketing and publicity strategies (Figure 1). If an invasive species makes it
into the distribution channel due to its superior performance as a crop then all parties, from the plant explorer
to the consumer, are factors in its spread. The more
successful a new product is on the world market, the
greater the number of units produced and sold, the more
likely that multiple introduction sites may enhance escape from cultivation as an invasive species (Reichard
& Hamilton, 1997; Reichard & White, 2001). Consequently, the most efficient phase of plant domestication
to limit undesirable introductions is during crop development, not distribution.
In this paper, we propose new strategies to assess invasive risk during the crop development process for horticultural species. We focus on the addition of trials at four different points along the
development process. The proposed methods are expected to minimize invasive potential while retaining commercial value of new crops. Finally, we
identify critical gaps in our knowledge to improve
pre- and post-release predictions of invasive potential
that currently limit invasion risk reduction during crop
domestication.
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Figure 1. The international distribution system of horticultural plant products (w: wholesale, r : retail), including classical (solid arrows) and
e-commerce/web-based (dashed arrows) marketing conduits (Anderson, 2004b). Potential sources or dispersal agents of invasive species may
distribute downstream in the system beginning with the plant explorers.
Opportunities to assess and reduce invasion risk in
plant breeding programs
It is well-established that predicting invasiveness based
on single factors such as plant traits alone or geographic
distributions is rarely successful (e.g., Anderson &
Gomez, 2004; Barrett & Richardson, 1986, Mulvaney,
1991, Virtue et al., 1999). In addition to assessments
that rely on multiple species attributes, trials intended
to discern invasive risk must be conducted in many environmental settings since post-release spread is dif-
ficult to predict. Consequently, risk assessments capable of adequately predicting invasiveness have the
potential to add significant, even prohibitive, effort
to a breeding program. While it is often assumed
that the most logical point for invasive risk assessment is immediately prior to crop release, there are
multiple decision points in the developmental pathway wherein invasive potential could be examined
and risks minimized. Screening for invasive potential
throughout the breeding program allows for species
posing the greatest risk of invasiveness to be identified
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Figure 2. Generalized approach for domesticating and developing new introductions. Hexagons represent potential selection opportunities for
reducing invasiveness and conducting risk assessments.
early in the breeding process, before making a longterm investment in crop development (Anderson, 2001,
2004d; Anderson & Gomez, 2004). A generalized
schematic used in developing new plant introductions
for the commercial market is proposed here as the
structural framework wherein the invasive screening
could be implemented at four decision junctures (Figure 2): Plant exploration phase, initial trial phase,
fast-tracking phase, and selection and improvement
phase.
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Figure 3. Increased market value (economic reward) and risk (research and development, invasiveness) as it relates to four categories of
commercial products, as illustrated with petunia, Petunia × hybrida (Anderson, 2004e). See text for explanation of the four product categories.
The plant exploration phase
The ultimate goal of floriculture breeders is to develop
an innovative product, one that is significantly meritorious among comparable products (cultivars) in the
market. Plant explorations are typically relied on to
bring in novel phenotypes to develop distinguishable
or innovative products. Developing truly unique phenotypes with high economic reward involves greater inputs into research and development, as well as higher
investment risks (Figure 3). When a distinguishable
product is developed, it has characteristics that allow
for novel marketing and, therefore, bring greater economic return than cultivar additions within a series and
the development of a new series. As crop domestication progresses, breeding new cultivars becomes increasingly easier (additions to existing series) as does
developing entirely new phenotypes (flower pattern
changes, dwarfism, increased branching, earlier flowering) within an existing product line to create a new
series (Anderson, 2004e).
Wild species are used to widen narrow germplasm
bases in established crops, provide desirable traits missing in elite breeding lines used to create hybrid cultivars, or to directly produce new crops (Anderson,
2004c, 2004e). Several long-distance collection trips –
often at considerable cost – may be needed before the
desired plant material is found growing at the proper
physiological state for collection of mature seed or
vegetative propagules. Most collected specimens require breeding and lengthy domestication to become
viable products since natural selection differs
from selection during domestication (Heiser, 1988;
Ladizinsky, 1979). Some wild collections may be used
as parents to cross with related crop species, providing new traits with perceived economic value (disease/insect resistance, drought tolerance) that can result
in distinguishable or innovative products (Figure 3). In
some instances, plants collected from the wild may
not require enhancement through breeding and selection and become direct-selected products in the public
domain (such cannot be protected by Plant Breeder’s
Rights or Plant Patents), provided they can be propagated and perform as well as existing products within
a product group (Figure 2). For instance, apple (Malus
domestica) plant collectors in Khazikstan, the center
of origin for apples, noted that, among the several elite
wild genotypes collected, more than 10% possess comparable horticultural merit to commercial cultivars in
subsequent side-by-side comparisons during the initial
trial phase (Figure 2) (Forsline & Aldwinckle, 2004;
Volk et al., 2005).
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Regardless of the extent of further development
needed, this initial plant exploration phase is likely one
of the most critical for reducing invasion risk. Manuals
of weedy plants, published flora, records from public
herbaria, and consultations with native plant experts
provide information on the country being visited and
the potential collection sites before embarking on plant
collection trips (Anderson, 2004b). It is not uncommon
for plant explorers to select plants with ornamental potential from species listed in weed manuals because
weedy species are easily adaptable to cultivation and
require little domestication. Traits conferring invasiveness are often similar to those that enable domestication as horticultural crops (Anderson et al., this issue).
Traits such as abundant fruit production, high germination and growth rate, and tolerance to a wide range
of environmental conditions aid in rapid domestication
and are also associated with invasive potential (Dozier
1999; Elton, 1958; Rejmanek & Richardson, 1996).
Plant breeders interested in reducing invasive potential of their crops should refrain from collecting
weedy taxa in the same way that they avoid genotypes
with undesirable ornamental traits. Observing the phenotypes of plants in many collection sites serves as an
initial visual screen to reject germplasm with undesirable characteristics (Forsline & Aldwinckle, 2004;
Volk et al., 2005) and increases the chances of finding desirable traits that match the breeding objectives.
Deliberately avoiding the collection of germplasm that
appears weedy may save the breeder the subsequent expense of breeding a crop that would be excluded from
market release because of its proclivity for invasiveness
(Figure 2). Likewise, if invasive traits are heritable, a
breeder might choose instead to collect the ‘weedy’
species and breed/select against invasiveness to retain
non-invasive traits during domestication. Generally, if
a species is determined to be ‘too aggressive’, based on
its ability to reseed easily in breeder trials, most breeding companies will not introduce it (Corr, 2003, pers.
comm.).
Initial trial phase
The initial trial phase is the first stage where selection under cultivated conditions commences. The initial trial phase allows the breeder to compare the phenotype when plants are grown in cultivation with the
observations recorded during the plant collection trip
(Figure 2). During the initial trial phase, germplasm
from the plant collection phase is screened to determine whether the observed phenotype in the wild has a
corollary expression in cultivated environments. Such
evaluative trials provide qualitative and quantitative
data to substantiate whether the existing germplasm
and selected traits have potential value. For example,
a breeder could determine whether a collected ‘early
flowering’ phenotype was early enough in a new crop to
warrant continued breeding or significantly earlier than
market comparisons to improve existing, domesticated
crops. During the initial trial phase the germplasm is
grown for a complete production cycle, from propagule to flowering plant, to determine the best mode of
propagation (vegetative versus seed), relative propagation capability (% rooting for vegetative; % germination and % yield potential for seeds), growth form
(including relative phase lengths of juvenility versus reproductive), flowering phenology (time and duration),
and potential consumer interest (flower power and convenience). These trials also provide the opportunity to
obtain useful information regarding traits associated
with invasive potential, stability across environments
and variability among germplasm accessions. Simultaneous selection for non-invasiveness and horticultural
value is likely to significantly decrease the proportion
of collected germplasm which is used at later steps of
the crop development process (Figure 2), resulting in
crops with reduced invasive potential.
Plasticity in the ability to grow in a wide range of
environmental conditions generally increases species’
invasive risk. Invasion trials during the initial trial
phase logically focus on a limited array of traits across
a broad range of environments: those that are readily observable and most likely to confer invasiveness.
Traits such as germination and growth potential are routinely performed in the initial trialing phase (Anderson,
2004e) and are often linked to invasive potential, as
well. Greenhouse and field trials in cultivated settings
should be supplemented with similar tests in noncultivated environments (Figure 2). As discussed in
Murphy and Lemerle’s contribution to this special issue of Euphytica, cultivated and non-cultivated environments differ in the environmental attributes that can
facilitate invasion. For example, studies with Cleome
hassleriana, an open-pollinated, seed-propagated ornamental crop which reseeds easily in cultivated settings and has become naturalized in certain areas of
the U.S. http://www.botany.wisc.edu/wisflora/) indicate that germination, establishment, and performance
in gardens are not predictive of growth response in
non-cultivated (roadsides, prairies) sites in Minnesota,
U.S.A. (Anderson & Gomez, 2004). Some Cleome cultivars may be less invasive relative to others due to
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differences in germination and stand establishment.
Is the Cleome response isolated or indicative that
other ornamental crops might have similar cultivarspecific differences? Significant cultivar-specific effects have been found in traits associated with invasiveness in other species (see Clark & Groves in
this special issue). Additional studies have shown significant differences between cultivars across environments, e.g. Ruellia tweediana (Wilson & Mecca, 2003),
R. brittoniana (Krumfolz & Wilson, 2002), and, to
a lesser extent in Nandina domestica (Knox et al.,
2004). For example, significant cultivar-specific effects and ranking change (instability) were found in
Ruellia brittoniana cultivars across day/night temperature treatments, replications, and cultivated environments (Krumfolz & Wilson, 2002). Nandina domestica cultivars differed in flowering and fruiting ability
in two cultivated sites (Knox et al., 2004), although
cultivar rankings (stability) were relatively constant
across sites for all genotypes except one (Knox et al.,
2004).
A lack of correlation between cultivated and noncultivated environments for cultivar response (GxE)
suggests that evaluating plants in standard plant breeder
trials might be insufficient to predict invasive potential
in non-cultivated habitats. Nonetheless, limited environmental trials in the initial trial phase of plant breeding programs have already led to the rejection of crops
that have exhibited invasive potential, e.g. tendency to
reseed (Corr, 2003, pers. comm.). Additional research
in the initial trial phase is critical to selecting genotypes
and cultivars with reduced invasive potential for use in
continued breeding and domestication.
Fast-tracking phase
In the rare event that a genotype is selected in the initial trial phase to directly become a potential product,
no breeding effort is required for market readiness as a
vegetative or open-pollinated seed product (Figure 2).
Occasional elite genotypes have been selected in the
wild that are as good as, or better than, commercial
cultivars (Forsline & Aldwinckle, 2004; Volk et al.,
2005). Such elite germplasm is advanced quickly or
‘fast-tracked’ through performance and production trials to reduce the time period until product release.
These trials are mandatory to prove stability across
multiple environments and demonstrate productivity.
We propose that such trials should also include evaluations in non-cultivated sites and focus on invasive
potential (Figure 2), especially since there are very few
opportunities to study these crops before they are released to the market.
A primary goal of a rapid assessment coupled to
“fast-tracking” (Figure 2) should be to accurately categorize the potential introduction according to its likelihood to spread and to cause a harmful impact to the
environment where it colonizes (Nijs et al., 2004).
Davis and Thompson (2000) devised a classification
system for colonizing and invasive species based on
their uniqueness to the region (novel or common), potential for short or long-distance dispersal, and potential environmental impact. Classifying species into one
of eight groups is accomplished by addressing three
questions: Is this species or genotype already present in
the region? Does the species typically disperse long distances or only short distances? Once established, does
the species have the potential to become a dominant or
keystone member of the community, changing the biotic and/or abiotic environment? Four of eight types of
colonizing species identified by Davis and Thompson
(2000) are native early successional species and not
relevant to the risk assessment of introduced species.
For introduced species and genotypes, the goal is to
be able to distinguish the remaining four groups: (1)
short distance dispersers, minimal impact, (2) longdistance dispersers, minimal impact, (3) short distance
dispersers, significant impact, and (4) long-distance
dispersers, significant impact. The invasive risk of a
new introduction increases with dispersal capacity and
the likelihood of impacts.
For domesticated species, evaluating dispersal capacity should be based on species traits as well as
human-mediated transport. Whether a species naturalizes in either cultivated or semi-natural habitats is dependent on species-specific traits (Kühn et al., 2004).
Martinez-Ghersa and Ghersa (in this issue) review
different plant traits that determine propagule pressure. Phenotypic traits (morphological, physiological)
of plant propagules may sustain each of the introduction, naturalization, and invasion phases of the invasion
process. Plant breeders focus on those traits allowing
successful introduction, rarely concerning themselves
with those traits correlated with invasion (see Anderson
et al., in this issue). A non-invasive crop ideotype is
proposed to alleviate this oversight.
Human-mediated crop and species transport is a
challenging arena for study. If we assume that all commercial products have market appeal and the potential for worldwide dispersal through commerce, the
number of units (propagules) of each product, termed
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source strength (Nathan et al., 2003), will still vary.
Species that are likely to be widely distributed because of their broad suitability and desirability (a typical commercial goal) will rapidly access broad geographic areas and many different ecosystems, as will
species with high seed output that are readily dispersed
by wind, long-distant migrating animals, and water
(Holzner & Numata, 1982). Species with only shortdistance dispersal capacity are those with much more
limited commercial potential, low seed output, limited environmental suitability, and/or little likelihood
of long-range transport (e.g., species that spread primarily by rhizomes). In most cases, introduced species
will be categorized as long-distance dispersers (due to
human-mediated transport); a much broader array of
conditions need to be considered when evaluating potential impacts. Although species that slowly diffuse
through their environment could eventually reach all
suitable regions, this rate is likely to be slow enough to
allow for population-limiting processes (e.g. disease,
predation) to become constraints and/or for weed control measures to limit spread. Neubert and Caswell
(2000) suggest that, when species distribution consists of long- and short-distance dispersal, the longdistance component governs invasion speed (even if it is
rare).
Kühn et al. (2004) theorized that sample size or
propagule pressure could be responsible for the degree
of naturalization. They found that the area occupied by
species in cultivated habitats was significantly lower
than the area naturalized in semi-natural habitats (e.g.
anthropogenic habitats such as old city parks, castle
walls). Likewise, a wider distribution of a species resulted in a higher probability of naturalization in these
semi-natural areas (Kühn et al., 2004). Species differed
in the greatest area occupied of cultivated versus seminatural habitats. More common species tended to have
a higher propagule pressure, a critical factor for invasion success (Lonsdale, 1999; Rouget & Richardson,
2003; Williamson, 1996). Statistically, larger populations could have a higher number of opportunities for
spreading into new habitats. Additionally, the occurrence of a higher number of new mutations would
provide the opportunity for increased microevolution
and adaptability (Lee, 2002; Sakai et al., 2001), which
may allow for easier invasion of semi-natural or natural
habitats.
According to Mack (2005), for a population of genetically identical individuals (clonal ramets – vegetative crops; inbred/F1 hybrid – seed crops), the larger
the number of individuals (Belovsky et al., 1999) and
the more widely dispersed (Bascompte et al., 2002),
the greater the chance that some genotypes will produce progeny. Barbier’s formulae (see this issue) argues
that, as propagule pressure and distribution of crops increase, the greater the chance that a crop will escape
and establish as a successful invader. Cultivated habitats provide an indefinite ‘buffer’ from environmental
stochasticity (present in natural or semi-natural habitats) which would otherwise destroy it (Mack, 2005).
Trial sites, nurseries, public gardens, commercial and
private landscapes deliberately maintain a continuous
source of propagules (primarily seeds) that can be
dispersed to non-cultivated habitats. Despite the fact
that most propagules fail to produce new populations
(Mack, 2005), the larger the number of propagules and
the wider the cultivation of a crop, the greater the likelihood of naturalization. If breeding programs can prevent the occurrence of invasive crops, then Barbier’s
(see this issue) ‘introducers’ pay tax’ would be used
only as a last resort to formulate a socially optimal
solution.
Fast tracking should not be pursued for any species
with the potential to cause environmental impacts,
regardless of its dispersal mode or region of origin
(Figure 2). Impacts caused by introduced species are
changes to the biological and/or physical environment that perpetuate the new colonizer at the expense
of the surrounding vegetation. Biological changes to
ecosystems precipitated by invasive species include
increased nitrogen levels, accumulations of salts, or
changes to herbivore populations. Increased erosion,
increased sedimentation, and reductions in light levels are examples of physical changes that can be associated with invasive species. Changes will generally
occur when a species has the potential for rapid population growth leading to dominance in a locale. Some
traits related to rapid population growth, most notably
rhizomatous spread and biomass accumulation, can
be directly evaluated from plants grown in artificial
conditions (and ideally are addressed during the initial trial phase). Others, such as nitrogen-fixation, will
vary in their importance based on the colonized environment. For example, van Riper (2005) found that
Melilotus officinalis has a greater impact to sparsely
vegetated areas in the South Dakota Badlands than to
wheatgrass (Agropyron smithii) communities, because
sparse vegetation is nitrogen-limited. An adequate, yet
rapid assessment to accompany fast tracking should
evaluate ecosystem-dependent traits under conditions
that mimic ecosystems most likely to exhibit impacts
(Figure 2).
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Selection and improvement phase
Species and genotypes advancing through the initial
trial phase without being rejected for lack of horticultural value, evidence of invasive tendencies, or which
were prevented from entering the fast-tracking phase,
are then ready for long-term development prior to market readiness (Figure 2). An extensive search of the
literature, as well as previous breeding records (mostly
unpublished data which may be available from previous breeding efforts), must be undertaken to create the
necessary knowledge base for breeding. Such a knowledge base will provide evidence of a taxon’s reproductive biology (existence of reproductive barriers),
genetics, cytogenetics, trait heritability, or potential
adaptability to seed or vegetative (cutting) production
(Figure 2). Though most information handled in breeding programs is highly confidential, there may be room
to exchange information about invasive potential of
germplasm accessions without infringing proprietary
law in order to reduce redundancy among breeding
companies testing similar crops and contribute to public records of invasive species.
With as much information about the species as can
possibly be obtained, plant breeders initiate the selection and improvement phase by developing a noninvasive crop ideotype from which to formulate their
breeding objectives, potentially including a desire to reduce the proclivity to invasiveness (see Anderson et al.,
in this issue). Initial approaches in developing breeding
populations that meet the specifications of the ideotype
focus on intraspecific hybridizations, followed by recurrent selection or other selection methodologies in an
effort to maximize genetic potential for trait expression.
For extensive reviews of breeding methodology consult Allard (1960), Anderson (2004e), Callaway and
Callaway (2000), or Craig and Laughner (1985). Each
methodology will have an impact on the time it takes to
produce plants of acceptable quality, the genetic variation in the crop and the extensiveness of the evaluations
that must be undergone before the crop is released to
the market. Selected parents would be tested for fertility
and general (GCA)/specific combining ability (SCA),
traits that can be informative in assessing invasive risk
(Figure 2). Inbred parents are routinely screened and
selected for high GCA or SCA levels, depending on the
seed production system for a product series. Progeny
evaluations would be conducted in each generation to
select for trait transmission by the parents, as well as
continued parent improvement via inbreeding. It would
be undesirable for progeny to have high GCA levels
for invasive characteristics, which could assure high
seed set and potential invasiveness in non-cultivated
habitats. Progeny with SCA requirements would limit
crossability and, potentially invasibility, with other hybrids or related crop taxa. Ideally, however, sterility
would be the optimal strategy to reduce invasiveness
due to fecundity; in lieu of this, however, low levels of
GCA and SCA in progeny would be desirable. These
evaluations offer often-unexplored knowledge regarding heritability and response to selection of traits associated with invasive potential. Since most horticultural
crops are polyploid, heterozygous, and outcrossers this
process may take many generations, depending on the
expression levels of reproductive barriers (such as self
incompatibility), inbreeding depression, and genetic
load (Liedl & Anderson, 1993) – offering numerous
opportunities to record evidence for invasive potential.
The process of developing new crops often involves interspecific and intraspecific hybridization and
selection for superior hybrids. Reproductive barriers
to hybridization are often broken, later enhancing the
probability of successful hybridization with native taxa
in the wild (Galatowitsch et al., 1999) and facilitating invasiveness (Ellstrand & Schierenbeck, in this issue). Crop domestication brings together, through the
plant exploration and selection phases, populations that
would have otherwise been reproductively isolated. Interspecific hybridizations performed during crop development often involve the cultivated crop as female
parents (cytoplasmic donor) and the wild species as
male and may take many generations of recurrent or
congruity backcrossing (Haghighi & Ascher, 1988) to
eliminate undesirable traits and select plants that do
not exhibit hybrid breakdown (Anderson et al., 1996;
Haghighi & Ascher, 1988; Hogenboom, 1975). Among
the hybrid populations produced in a breeding program, only the superior hybrids are selected. Selection for superior genotypes among a hybrid population may take longer in the wild, depending on levels
of natural selection, but is relatively rapid and intense
during domestication where non-adaptive phenotypes
are ruthlessly rogued out (Allard, 1960). Many of the
traits these hybrids possess may confer an advantage
in the wild over their parental lineages. For example,
there can be strong selection to produce early flowering crops that allocate more resources to reproduction than to vegetative growth, a pattern that is consistent with Harper’s prediction of colonizing plants
(Harper, 1977). Even the stabilization of hybridization, which can contribute to invasiveness (Ellstrand
& Schierenbeck, 2000), is accomplished much more
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rapidly in breeding programs than in natural conditions through induced polyploidization or vegetative
propagation. Once these superior genotypes are identified in a breeding program, propagated, and widely
distributed, there are fewer barriers left to overcome
before evolving into invasiveness.
During the selection and improvement phase, extensive knowledge about the specific breeding populations is gained and can be incorporated into global
information systems (GIS) and climate matching programs to assess risk of invasion (see Bass in this issue).
As breeding progresses and progeny are generated for
evaluation, plant breeders will conduct various types of
evaluative trials to test and select individual genotypes
(vegetative breeding), populations (seed breeding) or
parents (for continued inbreeding of seed products).
Each trial may be conducted multiple times on every
new generation of populations upon which selection is
advanced. Initial trials are conducted at a single location, but as potential products are advanced, these trials
will be conducted in an increasing range of locations
to screen for stability across environments. To make
sense of the information obtained, climate matching
programs can be used to infer the likelihood a particular crop could establish self-sustaining populations in
a new environment. In this special issue of Euphytica,
Bass et al., describe the potential benefits of using GIS
as a method to determine habitat suitability at a finer
scale than the level attainable with climate matching
programs.
These programs could also be used to determine
locations for field trials especially designed to evaluate
invasive potential of new crops and the impact on, and
effect of, other trophic levels. Evaluations to determine
invasiveness within the new environment can be helpful in cases where invasiveness was not reported in the
location of origin as was the case of several ornamental crops including Acacia spp. (native to Australia;
invasive in S. Africa; Musil, 1993), Rhamnus cathartica (native to Europe; invasive in Minnesota, USA and
elsewhere; Archibold et al., 1997), Cortaderia jubata
(pampas grass; native to the tropical Americas, invasive in California, USA; Lambrinos, 2000), Lythrum
salicaria (purple loosestrife; native to Eurasia, invasive
across N. America; Thompson et al., 1987), and Dipsacus fullonum (teasel; native to Eurasia, widespread
invasive in the USA; Solecki, 1989). Field evaluations
of the advanced lines of a breeding program can provide
valuable information about higher order trophic level
interactions. For example, the likelihood of establishment of Asparagus in non-shaded habitats seems higher
than observed when accounting only for this species
tolerance to light levels (Bass et al., this issue) when
in fact, it just occurs under tree canopies. Communitylevel studies confirm that seed dispersal patterns are
driven by birds, which perch on trees while they deposit the seeds.
Competition experiments will be crucial at this
phase. Since initial trials should have eliminated genotypes with obvious morphological traits that are likely
to confer invasiveness in nearly all settings, the goal
of risk assessments at this phase should be to identify
the likelihood that a match between a species characteristic and a new environment will result in invasiveness. For example, Heger and Trepl (2003) observed
that Impatiens parviflora is invasive in some European
hardwood forests because its shallow roots exploit soil
not occupied by indigenous forest species. Impatiens
is less likely to be invasive in forests with extensive
understory development. Neither an assessment of the
species or ecosystem, alone, would be adequate to have
predicted the invasive potential of Impatiens parviflora.
Since there is little control of the ultimate distribution of crop introductions (other than import bans
of specific species by a country), it is important that
these trials be conducted across a range of indigenous soils and with indigenous plants as potential competitors. Klironomos (2002) showed that some invasive plants accumulate soil pathogens more slowly
than their neighbors, resulting in relatively high growth
rates. In their study, pathogens were most likely to be
a determinant of invasiveness at high plant densities.
Morrison and Molofsky (1999) compared the performance of three genotypes of the forage grass, Phalaris
arundinacea in sparse and dense vegetation and identified clones that are less competitive in sparse vegetation
than dense vegetation, and vise versa. Relative competitive ability in a community will frequently reflect
species’ capacities to acquire limiting nutrients, either
directly or indirectly. Callaway and Aschehoug (2000)
observed some species are invasive because their neighbors cannot tolerate root exudates that affect competition for resources.
Understanding which resources are likely to be limiting in particular communities (i.e., light, nitrogen, or
phosphorus) is a crucial first step in designing effective
trials. Also important is identifying the logical mixture
of neighbors. In some ecosystems, more species in a
community likely reduces species’ invasibility (Hector
et al., 2001, Kennedy et al., 2002), whereas in others diversity has no effect on invasive species establishment
and spread (Hector et al., 2001). Even for herbaceous
213
species, competition trials represent a significant commitment of time and space. They should be conducted
over more than 1 year to ensure seasonal changes in
plant growth and reproduction are accounted for; adequate numbers of treatments and replicates can result
in large experiments. For woody plants, the task becomes more complicated because plants usually take
longer to reach maturity (although valuable insights
will often be gained before maturity) and experimental units are necessarily larger. Grafting is commonly
used to truncate the juvenility period and cause flowering, which may further complicate invasive screening
due to the confounding factor of rootstocks (Hartmann
et al., 1997). Nonetheless, given the lack of information about the genotypes under consideration, there is
little way to make predictions without some direct observations of the interactions between genotypes and
the environment.
Research needed to improve pre- and post-release
predictions of invasive potential
Many taskforces and committees have been formed
worldwide to rank research priorities for invasive
species on national, regional, provincial, state, or local levels. For example, the Committee for Noxious
and Invasive Plant Management in the state of Alaska,
U.S.A., ranked ‘prevention’ as the top priority and most
inexpensive, cost-effective means of eliminating invasive species (Conn et al., 2003; National Invasive
Species Council, 2001). However, research priorities
have been traditionally directed towards the control of
existing problem species via chemical, bio-control, or
other techniques (Conn et al., 2003). While research
needs in the breeding and development of noninvasive, domesticated crops vary depending on location,
prevailing governmental policies, breeding objectives,
market incentives, and consumer acceptance, there are
several gaps in scientific information that are of universal interest.
The benefits of a breeding method involving early
trial and selection against invasiveness should be assessed and compared directly to the current practice
of evaluating cultivars at the final stage of domestication immediately prior to release. It will also be necessary to quantify the costs associated with implementing
multiple trial and evaluation steps along the crop development process. The two approaches for predicting
invasive potential reviewed in this paper – evaluating
species traits alone, and evaluating competitive out-
come between new introductions and potential neighbors in varying environments – have the possibility
to detect potential invaders in some, but not all situations. These approaches do not adequately account
for stochastic events (e.g., climatic events), landscapescale processes and the importance of low frequency
colonizations. Empirical assessments of these factors
are not feasible prior to introduction, yet they are potentially crucial aspects of a comprehensive risk assessment.
Further research on modeling strategies are needed
to augment experimental approaches available for assessing invasive potential. Peters (2004) identified three
types of models that have been used to evaluate invasive
potential: non-spatial, spatially implicit and spatially
explicit. Models need to present key processes and
driving variables that explain population and ecosystem dynamics while avoiding extraneous parameters
that contribute more to overall error than explanatory
power. Population growth and mortality as a function
of species traits and environmental characteristics can
be represented with non-spatial models (see Perry &
Galatowitsch, this issue). Spatially implicit models incorporate geographic location as a parameter, but not
spatial process parameters and landscape context (e.g.,
propagule supply and dispersal constraints). Many
studies on invasive potential have employed a spatially implicit approach by using regression to model
climatic preferences than predicting a species’ potential distribution with a Geographic Information System (see Bass et al., this issue). Spatially explicit models determine invasion dynamics based on both spatial location and spatial processes. Modeling invasive
spread with very low rates of dispersal (Kolar & Lodge,
2001), with variable propagule pressure, with periodic
or rare climate changes, or in discontinuous versus continuous suitable habitat requires use of spatially explicit models. Developing modeling approaches that
can be readily adapted for many new introductions,
that do not have high error versus explanatory power,
and that rely on generally available data is a critical
research need for risk assessment of introduced plants.
Spatial models have been successful at predicting the
spread of disease but these models have underestimated
rates of spread by an order of magnitude (c.f. Peters,
2004).
Despite intentional avoidance of invasive traits during breeding programs we anticipate that domestication and introduction will continue to be a source of
invasive species for several reasons: (1) our ability
to predict invasiveness relying on traits is imperfect
214
(e.g., Kolar & Lodge, 2001), (2) the number of new
introductions into some regions of the world is likely
increasing as global trade increases, (3) implementing our proposed invasiveness screening procedures
will not be immediate due to cost and significant research/development needs, and (4) we cannot control
the genetic and environmental changes that can lead
to invasiveness post-introduction. Therefore, strategies
including adoption of mandatory professional codes
of conduct are needed so that released plants that become invasive do not spread more rapidly because they
continue to be promoted commercially (Peters et al.,
in this issue). Research needs at the post-release stage
include study of the feasibility and effectiveness of potential incentives to increase the adoption and implementation of mandatory codes of conducts. Barbier and
Knowler (in this issue) demonstrate that the issue of
invasive species introduction is quite amenable to economic analyses and that one possible solution could
involve the implementation of an “introducer’s pay”
tax. Other potential research questions that need to be
addressed from a risk assessment and economic standpoint are what time period is necessary to determine
whether a species is invasive, and how long breederproducer and distributor companies will forgo revenue
in order to assess the invasive risk of a new crop. Methods to inform consumers about the threat of ornamental
crops with invasive potential should be developed and
studies should aim to determine their impact on crop
marketability.
Conclusions
The problem of invasive species of ornamental origin is
a complicated one. On one hand, there are the interests
of a market sector to obtain economic gain from the
introduction of species and strong demand among consumers for distinguishable products that involve greater
invasive risk. On the other hand, there is an increasing
awareness of the devastating, irreversible effects of invasives on native and natural communities and greater
demand for the direct involvement of plant breeders in
the development of ‘environmentally safe’ crops. The
prevailing factor limiting our ability to come up with
an easy solution is the degree of uncertainty associated
with predicting invasiveness, and even though prevention has been noted as the most important component in
resolving the issue, it is a difficult element to execute.
Currently, the methods to assess invasive risk of new
crops involve an often subjective evaluation during the
product development process or immediately prior to
release into the market and studies focus on cultivar
comparisons for traits associated with invasive potential. As we have demonstrated, analysis of the process
of crop development reveals important junctures that
lend themselves to evaluating invasive potential prior
to crop release. Assessing the risks of invasiveness at
these multiple junctures is likely to be more reliable
and cost-effective because it focuses research on the
highest risk species/cultivars with economic promise
being selected or rogued earlier and less risky species
receiving follow-up evaluations prior to release. Empirical assessments are likely to be the major thrust of
invasive potential screening. However, models offer the
potential to make predictions over longer time frames
and across greater geographic areas than is observable
prior to release.
With or without preventative measures, the spread
of invasive crops is, to certain degree, inevitable. Postrelease strategies are essential to prevent the distribution of known invasive crops via commercial venues.
Future research needs involve social, economical, ecological and breeding aspects because the development
and distribution of ornamental crops is part science,
art and industry. Incentives should be developed for
adoption and enforcement of regulatory mechanisms
and mandatory (rather than voluntary) professional
codes of conduct. Plant breeders and everyone involved in the distribution of ornamental crops should
become aware of the potential risks associated with
the products they produce and sell. Consumers should
demand greater participation from their local retailers in minimizing the risks associated with invasive
species.
Plant breeders will continue making decisions in
the midst of uncertainty and there will always be gaps in
our ability to prepare for the unexpected. However, we
are better prepared to respond to the challenges posed
by invasive species if alternative scenarios are studied
thoroughly prior to facing the outcomes. We propose
that strategic modifications to the crop development
process, adoption of post-release regulatory codes, and
continued research on invasives are some of the mechanisms to proactively minimize invasive risk of new
crops and products.
Acknowledgements
This paper was supported by the Minnesota Agricultural Experiment Station.
215
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