Download Ecosystem resistance to invasion and the role of

Journal ofMediterranean Ecology 2: 233-245,2001
O 2001 Backhzrys Publishers, Leiden
Ecosystem resistance to invasion and the role of propagule supply: A California
perspective
Carla D'Antonio, Jonathan Levine & Meredith Thomsen
Dept. of Integrative Biology, University of California, Berkeley, CA 94 720-3140, US.A.
Keywords: alien species, competition, disturbance, exotic invaders, non-indigenous plants.
Abstract
The concept of ecological resistance includes both abiotic and biotic features of a recipient environment that influence the success of propagules of a species that has not previously occurred on a site. Despite broad interest in this topic by ecologists and
land managers, we lack an understanding of what factors contribute to ecological resistance and how processes influencing resistance interact with the supply of propagules to determine invasion success. Here we present a simple conceptual framework for
examining how variation in propagule supply should interact with ecosystem resistance to influence the rate at which exotic
invaders enter a habitat. We suggest that when resistance is low, it takes very few propagules for an invader to become established
and that rates of invasion will be fast regardless of propagule supply. As resistance increases, however, it takes proportionally
more propagules for the invader to establish. When resistance is high invasion will occur only when propagule pressure is high
or when invaders themselves can alter resistance as they get a toehold in the community. When resistance is controlled largely
by biotic factors we believe that it can be overcome by high rates of propagule supply even if initially appears to be strong,
because over space and time biological sources of resistance are likely to be variable allowing windows when a site has moved
to a region of the propagule supply axis where many fewer propagules are required for invasion to occur. By contrast, strong abiotic resistance is less likely to be overwhelmed by high propagule pressure and if determined largely by soil factors, is likely to
be relatively constant over space and time. We also suggest, that some invaders of harsh environments are successful because of
their own ability to modify abiotic conditions thus decreasing the number of propagules needed to promote further invasion. We
review examples of resistance in California plant communities and where possible show how resistance interacts with propagule
supply. Overall, we found very few studies that measure or consider the role of propagule supply and how it interacts with resistance factors and we believe that such studies are badly needed if we are to advance our understanding of controls over biological invasion.
Introduction
In his seminal book, The ecology of invasions by
animals and plants, Elton (1958) called attention
to the devastating impacts that biological invasions
have on native species. However, he also pointed
out that most introduced species actually fail to
establish self-replacing populations. To explain
this establishment failure, he introduced the concept of "ecological resistance," the natural
processes or ecosystem properties that negatively
influence invasion success. In the time since
Elton's landmark book, interest in the success and
impact of non-indigenous species has skyrocketed,
yet our understanding of ecological resistance
remains fragmentary. A better understanding of
resistance is important for predicting communities
that will be most susceptible to future invasions
and for advising managers on how to enhance ecological resistance. Maximizing ecological resistance may be a means by which to constrain the
spread and subsequent damage done by unwanted
invaders.
Interest in ecological resistance has spurred
efforts to understand which communities are most
invaded and impacted by non-indigenous species.
Recent surveys indicate that several Mediterranean
ecosystems including those in California contain
some of the highest numbers of non-indigenous
species on the planet (Macdonald et al., 1988;
Mooney et al., 1986; Kruger et al., 1989; Usher et
al., 1988). Possible explanations include: ecological resistance may be weak in some Mediterranean
communities because of regular disruption by natural or anthropogenic disturbances. Alternatively,
resistance may be substantial but may be overwhelmed by a large supply of exotic species to
these regions because of high human activity. This
high propagule pressure might also be explained by
the fact that since Mediterranean systems are distributed worldwide, and since many of their
invaders come from other Mediterranean habitats
(Mooney et al., 1986; Fox, 1990; Rejmanek et al.,
1991), there is simply a large pool of species well
adapted to similar climatic conditions and that pool
is being very actively moved. Without knowing
more about the flow of propagules among regions,
it is impossible to evaluate the importance of ecological resistance in any given area.
The basic theme of this manuscript is that variation among communities in their susceptibility to
invasion can be attributed to biotic and abiotic factors, and to the supply of invader propagules
(Lonsdale, 1999). Here we examine our knowledge of how these factors affect the success of
non-indigenous plant species in California's
Mediterranean ecosystems focusing largely on
plant invasions since plants are the focus of our
individual research. Our major goal is to review
empirical evidence about resistance in California
and develop a conceptual framework linking resistance and propagule supply that generates predictive, testable hypotheses regarding community
susceptibility to invasion.
Our decomposition of the controls over invasion
into propagule supply, abiotic factors and biotic
factors is not without precedence in community
ecology. Plant ecologists, for example, have debated whether populations are limited by the arrival of
seed or the availability of suitable or "safe" sites
(Harper, 1977; Crawley, 1990; Turnbull et al.,
2000). Meanwhile, marine ecologists have grappled with competition-predation (Menge &
Sutherland, 1976) versus "supply-side" explanations for community patterns (Gaines &
Roughgarden, 1985; Roughgarden et al., 1988).
Because of the parallels between these issues and
invasibility (sensu Rejmanek, 1989), we feel that
approaching the invasion of Mediterranean systems
from a general community perspective is fruitful.
General framework
Elton's original use of the term "ecological resistance" included both abiotic features of the environment and biotic features of the community
occupying a site. Beginning with Elton, community susceptibility to invasion has largely been treated as a yeslno issue: communities are either deterministically resistant or susceptible to the invasion
of a particular species (Fig. 1). Realistically, however, communities vary continuously in their susceptibility to invasion, making invasion success a
A Deterministic Perspective
lnvasion Resistant
Invasion Suscept~ble
B Probabilistic Perspective
Resistant
Susceptible
-Increasing
- - - Disturbance
------
+
Fig. I . Alternative perspectives on community invasibility or
conversely on community resistance to invasion. The deterministic perspective views communities as either invasion
resistant or invasion susceptible. The probabilistic perspectives places communities along a continuum where the probability of successful establishment varies from low to high.
In this case propagule supply rates can dictate whether or not
invasion will occur. A single site may vary in its location on
the continuum over time given variation in weather, disturbance, management activities, etc.
probabilistic process (Fig. 1). A single community
can vary in its location on a resistance continuum
depending climate, disturbance, herbivory and natural succession (Davis et al., 2000). 'Natural' and
anthropogenic disturbance will tend to push a
community towards the susceptible end of the continuum (Hobbs, 1989; Hobbs & Huenneke, 1992;
D'Antonio et al., 1999), while managers desire to
push or keep communities nearer the resistant end.
Where a community lies on this continuum dictates the number of arriving propagules that it
takes to establish a population. Viewed in this way,
propagule supply rates play an important role in
determining the ultimate success of invaders.
Where environmental resistance (biotic or abiotic)
is strong, propagule supply must be great for invasion to occur. By contrast, where resistance is
weak or temporally variable, propagule supply
need not be as great to overcome resistance. Since
the invaders' reproductive biology is an important
determinant of propagule pressure, we might see a
wider range of invader reproductive traits in less
resistant habitats. Alternatively, less resistant habitats may rapidly switch to being more resistant if a
competitively superior invader arrives early.
In California, invasive non-indigenous species
are well known to be abundant near the coast, in
counties with large urban areas, and near roads, disturbance corridors and structures (Mooney et al.,
1986; Knops et al., 1995; Zink et al., 1995; Randall
et al., 1998).Thus, human disturbance and propagule pressure are likely major contributors to the
invasion of California ecosystems. Nonetheless,
there is intense human contact with some California
systems that are not very invaded suggesting that
California ecosystems vary in the strength of mechanisms that influence invasion resistance.
Abiotic factors affecting invasion success in
California ecosystems
The important role of abiotic factors in limiting the
entry of exotic species into new areas has been
strongly emphasized by several researchers (e.g.
Simberloff, 1986, 1989; Baker, 1986; Ehler, 1998;
Alpert et al., 2000). Indeed, it is assumed that climate matching (a coarse scale abiotic factor) is a
precondition of successful invasion (Baker, 1986).
Potential abiotic constraints on invasion include
harsh or toxic soil conditions, prolonged summer
drought, repeated scouring or submergence by
water, and severe climatic conditions such as those
in deserts or high montane habitats.
In California, an example of abiotic resistance
appears to be the limited success of European annual species on serpentine-derived soils while they
thrive on adjacent unaltered soils (McNaughton,
1968; Mooney et al., 1986; Harrison, 1999a,b).
Harrison (1999a) surveyed a wide range of serpentine outcroppings in northern California and found
that the cover of exotic species was positively related to the Ca* content of the soil. Low Ca++patches of serpentine soil had very few exotics despite
being surrounded by a sea of European annual
species on unaltered soils. Interestingly, small
patches of serpentine showed a much stronger positive correlation between soil Ca++and number of
exotic species than large patches of serpentine,
potentially because they are more susceptible to
propagule swamping. On a small serpentine outcropping in central California, Huenneke et al.
(1990), found that harsh conditions on serpentine
could be alleviated somewhat by fertilization which
then allowed for invasion by exotic grasses.
Most evidence for the role of abiotic resistance
in limiting invasions into California's
Mediterranean ecosystems is based on species
lists. For example, of all of the major eco-regions
in California, the California deserts (Mojave,
Colorado/Sonoran, and montane deserts) contain
the lowest number of exotic species per km2
(mean=27). This cannot strictly be due to distance
from the coastal sources of propagules, because
regions such as the Sierra Nevada foothills are at
least as far from areas of introduction (Los
Angeles or San Francisco) as many parts of the
Mojave desert (24 species/km2) but they contain
significantly more exotics per km2 (mean for
Sierra Foothills=85, Randall et al., 1998).
Lonsdale (1999) examined species lists from
around the world and also concluded that deserts
contain distinctly fewer exotic species than most
other habitats (except islands) and Alpert et al.
(2000) looked at evidence from a range of spatial
scales and concluded that water stressed environments have reduced levels of invasion. Those
species that have established in California deserts
often alter the abiotic environment during invasion
(Kemp & Brooks, 1998) and therefore modify abiotic resistance. For example, exotic annual grasses
such as Bromus spp. create litter that decays slowly. This litter traps moisture, enhancing conditions
for seed germination of the invaders (Evans &
Young, 1970; Young & Evans, 1985) thus partially
ameliorating abiotic stress.
The number of exotics per km2 declines with
elevation in the Sierra Nevada (Mooney et al.,
1986; Randall et al., 1998) suggesting that severe
winter conditions may limit the invasion of upper
montane environments. However, the relative roles
of propagule pressure versus abiotic factors in driving patterns of invasion across elevational or climatic gradients has yet to be examined. Also unexplored is the potential role of abiotic disturbance
such as flooding or fire in reducing the invasion of
exotic plants many of which are not adapted to
such disturbances. Burns & Sauer (1993) suggest
that chaparral fires have been important sources of
abiotic mortality for introduced conifers in coastal
mountain plantations. Other factors may also
account for the lack of spread of these plantation
trees (see below).
With the exception of studies on Serpentine soils
(e.g. Huenneke et al., 1990; Hobbs & Mooney,
1991), little experimental work has examined the
role of abiotic factors in limiting invasions in
California. While manipulation of abiotic features
is a difficult management action, better understanding the role of abiotic features in influencing invasion success could aid our understanding of where
restoration and exotic species control is most likely
to be effective. Likewise, identifying those invaders
capable of reducing abiotic resistance as they
invade may help to prioritize species for control.
Biotic factors affecting invasion success in
California ecosystems
Elton (1958) and others (e.g. Simberloff, 1986, 89;
Lawton & Brown, 1986; Ehrlich, 1989) have
focused largely on competition and predatiodparasitism in their consideration of biotic mechanisms
of resistance. Nonetheless biotic resistance can
result from any of the following: (I) Competition
including, [a] preemption or priority effects
whereby established native species keep out potential invaders and [b] competition among seedlings
or regenerating individuals of native and exotic
species after disturbance. In this latter case, it is
the relative ability of native versus exotic species
to colonize or regenerate that influences invasion.
This dichotomy has not typically been included in
discussions of resistance mechanisms. (2)
Predation or parasitism by native or previously
established organisms may prevent invader
propagules from establishing and reproducing. (3)
Attack by indigenous pathogens. (There is no published information on this topic for California
plants so we will not discuss it further). (4)
Limited availability of required mutualists. In the
latter case, resistance may arise from a depauperate mutualist biota or competition from native
species that limits the availability of mutualists
(e.g pollinators or dispersers) for the invaders.
Experimental tests for biotic resistance mechanisms are few. Perhaps this is because in their
purest form they would involve introducing potential invaders into native-dominated habitats where
they are currently rare or absent while manipulating the biological environment. Nevertheless, several experimental studies have examined mechanisms influencing invasion by exotics that are
already established in California and these provide
useful insights into the role of community structure in affecting invasions.
Competition
Peart (1989) introduced seeds of non-native species
into patches where existing grassland species had
been killed by insecticide but the soil was undisturbed. Virtually no establishment occurred if the
resident species weren't killed. D'Antonio (1993)
introduced seeds and seedlings of Carpobrotus
edulis near to and away from shrubs to test for
facilitative or interference effects of shrubs in a
dune and coastal scrub habitat. Weak competitive
effects were present in some years, while in other
years shrubs had no effects or were facilitative.
Evidence for the role of competition at broader
scales comes largely from anecdotal observations
and descriptions of communities where invaders
are generally lacking (Baker, 1986). Several investigators have observed that mixed conifer forests,
hardwood forests and dense chaparral are depauperate in introduced species in California (Baker,
1986; Mooney et al., 1986; Randall et al., 1998). It
is assumed that competitive suppression by light
limitation is the cause although the role of herbivores or pathogens has not been examined.
Most often, the role of competition in limiting
invasion by exotics is inferred from studies of disturbance or species removals or from negative correlations between vegetation stature and presence
of exotics (Mooney et al., 1986; Rejmanek, 1989).
D'Antonio (1993) and Peart (1989) introduced
propagules of non-native perennial species into
manually disturbed and undisturbed coastal grassland in California and found that seedlings germinated but survived poorly in undisturbed plots presumably because of competition from grassland
species. By contrast, on artificial and natural
rodent disturbances the invaders survived quite
well. Likewise, Schiffman (1994) found that disturbances associated with kangaroo rats promoted
a community of annual exotics in an interior grassland that otherwise had a reasonable component of
native annual species.
Most invasiorddisturbance studies do not document the mechanism through which disturbance
promoted invasion but alteration of the competitive
environment with resident species is likely to be
important. Disturbance can facilitate invasion by
other mechanisms such as direct stimulation of the
seed bank. While these studies suggest that preemption type competition can suppress invasion, they
likewise point to the important role that native
sources of soil disturbance play in promoting inva-
sion. In many California grasslands, rodents and
other vertebrates are a constant source of soil disturbance (Schiffman, 1999) turning over up to 25% of
the soil per year (Hobbs & Mooney, 1991,
S c h i h a n , 1999). Thus, these environments may
lack strong biotic mechanisms of resistance because
they are and have been disturbed by animals for centuries (Schiffman, 1999). Furthermore, many of the
native species in these communities apparently lack
the regenerative ability of introduced species.
Perhaps when resistance comes down solely to
regenerative ability, communities are always susceptible to invaders with superior regenerative powers.
In contrast, disturbance does not favor exotic
invaders in communities in which many of the
native species are better at regeneration. For example, Kotanen (1995) found that disturbance by
feral pigs, which reduced native perennial grass
cover in a northern California meadow, favored
both native and exotic annual species, all of which
had a dense seedbank. Eventually native perennial
species from the surrounding area recolonized the
disturbances. Interestingly, disturbances in some
of these same meadows are now being invaded by
Holcus lanatus, a persistent perennial grass from
northern Europe that also has very rapid colonization and growth capabilities.
Apparently, the invasion of better colonizing
and highly persistent exotic species has not yet
happened in California chaparral - a vegetation
type with numerous native species capable of rapid
regeneration after fire. Though annual exotic
species often colonize after fire, they do not persist: chaparral has remained dominated by native
perennial species (Mooney et al., 1986) because
after fire these species readily reestablish from
seed or by resprouting. We cannot however,
assume this situation will persist indefinitely. The
South Africa fynbos is replete with native perenni-
al species capable of rapid regeneration after fire,
but has been invaded by Australian shrub species
that have more prolific post-fire regeneration.
Thus far in California the only sites where chaparral vegetation has been replaced by exotic species
are those where fire frequencies have been greatly
increased (Zedler et al., 1983; Haidinger &
Keeley, 1993). Also in a restricted form of maritime chaparral exotic perennials have been able to
invade and persist after fire because of fast growth
rates compared to the natives (Zedler & Sheid,
1988; D'Antonio et al., 1993) but this is an exceptional circumstance where a very open form of
chaparral occurs on sandy soils.
Several authors have noted that some apparently undisturbed communities are readily invaded
(Rejmanek, 1989; D'Antonio et al., 1999). These
studies should not be treated as cases of communities with no resistance. Rather, resistance may be
strong but persistent propagule pressure could
have gradually led to invasion. Conversely, they
may be situations where invaders have altered
resistance mechanisms as they invade. Careful
experimental work would be required to distinguish the various possibilities.
Herbivory
D'Antonio (1993; D'Antonio et al., 1993) found
that native animals could strongly limit the success
of the South African succulent, Carpobrotus
edulis, in coastal dune, grassland and scrub habitats in central California. Vila & D'Antonio (1998)
made similar findings for invading Carpobrotus
taxa in northern California coastal sites.
D'Antonio (1993) found that one of best habitats
for growth of C. edulis in the absence of herbivores was a coastal scrub site with dense shrubby
vegetation. Despite the high shrub cover, competi-
Table 1. Sources or mortality and number of propagules required for invasion of three California coastal habitats by the South
African succulent, Carpobrotus edulis. Sites and invasion experiments are described fully in D'Antonio, 1993. Mortality data are
percent of seedlings outplanted to field sites that died from particular causes. Number of seeds needed for establishment are based
on germination rates of seed in microhabitat where survival occurs, typical abundance of that microhabitat across transect
through each site, and survival rates estimated on natural and outplanted seedlings in each habitat.
Sources of Mortality
Habitat
Competition
Backdune
Grassland
Coastal Scrub
0
53
0
Abiotic
Herbivory
Number of seeds required
tion had only a weak effect on seedling survival
and growth. Still seedling establishment rates were
near zero because of intense herbivory. Propagule
supply was estimated to have to be very high in
order for establishment of the invader to occur
(Table 1). The herbivores abundant in this study
were brush rabbits, (Sylvilagus bachmanii), a
species shown to have a strong influence on understory structure at the ecotone between shrublands
and grasslands in California (Bartholomew, 1970;
Halligan, 1974). Other shrubland-associated animals such as seed-eating birds have been found to
reduce seed densities of Scotch Broom in coastal
California (Bossard, 1991) and mammalian herbivores in the same system reduced growth and
reproduction of the same invader (Bossard &
Rejmanek, 1993). Cushman (unpublished data)
has experimentally demonstrated that vertebrate
herbivores reduce the abundance of both exotic
annual grasses and an aggressive South Africa
grass in coastal dunes in northern California.
high; hence mycorrhizal inoculum may also be
diverse. Yet Horton et al. (1999) and others have
shown that native conifers can be limited in their
invasion of shrublands by the availability of appropriate mycorrhizal inoculum. Burns & Sauer
(1992) reviewed the history of conifer introductions into the San Gabriel Mountains in southern
California and found that none of the 40+ introduced species planted there have spread beyond
their original plantations. They claim that this is
due to competition from the dense surrounding
vegetation, harsh abiotic conditions and/or the relatively greater ability of native species to recover
from fire. But this failure may also result from the
lack of compatible mycorrhizal inoculum away
from planted stands. It is unlikely that invasion is
limited solely by low propagule pressure since for
many of the species thousands of individuals were
planted in the original stands.
Mutualists
Numerous recent studies have focused on the relationship between biological diversity and the invasibility of Mediterranean systems. Diversity may
increase community resistance through any of the
mechanisms listed above, though the most commonly cited mechanism is competition.
Specifically, higher plant species richness is
hypothesized to better preempt available resources
and thereby reduce the likelihood of invasion - an
argument based on species packing and LotkaVolterra type models (see Levine & D'Antonio,
1999). Though several experimental studies have
found that diversity can enhance resistance to invasion in some California ecosystems on a plant
neighborhood scale (Levine, 2000; Dukes, 2001;
Lyons et al., in review), these effects are not strong
enough to drive community-level patterns (Levine,
2000). Indeed the most diverse California ecosystems often contain the most invaders or are most
easily invaded (Peart & Foin, 1985; Knops et al.,
1995; Robinson et al., 1995). A similar result has
been found in a global analysis of invasive species
(Lonsdale, 1999). It seems that factors co-varying
with diversity and not diversity itself are responsible
for driving these community-wide patterns (Levine
& D'Antonio, 1999). Levine (2000) found that patterns of invasion in a riparian community in northern California are much more strongly related to
patterns of propagule dispersal than to local scale
resistance associated with high species diversity.
Recently, Richardson et al. (2000) and Simberloff
& Von Holle (1999) have pointed out that mutualistic interactions involving introduced and native
species are common and the ease with which they
are acquired by invaders will enhance invasion
rates. There is however, some limited evidence that
availability of mutualist partners such as pollinators may slow invasion for some outcrossing plant
species in California (Parker, 1997; Parker &
Haubensak, in press). Parker and Haubensak (in
press) found that for both French and scotch broom
in some coastal California settings pollinator availability could greatly limit seed set. This in turn can
affect population growth rates (Parker, 1997). It
was not clear, however, whether pollinator limitation resulted from competition between the brooms
and simultaneously flowering native species or an
asynchrony between pollinator activity and flowering time. Although both broom species are abundant in several regions of the state, these pollination studies suggest that seed production in some
habitats could be much greater than current levels.
While invasion by introduced plantation
conifers into the surrounding vegetation can be
limited by the availability of ectomycorrhizal
mutualists in South Africa (see Richardson et al.,
2000), this possibility has not been examined in
California. Native conifer and ericoid diversity are
Species diversity
Summary of evidencefor resistance
Perhaps the most striking aspect of this review is
the paucity of experimental studies of mechanisms
responsible for resistance in California environments. In particular there are no studies that simultaneously manipulate propagule supply rates and
sources of resistance, or that measure rates of seed
arrival and per capita seed success in different
environments. We found that native vertebrate
activity can be very important in both promoting
and limiting plant invasions and its importance to
invasions is under appreciated. While competition
has been demonstrated to be significant at the
local scale in invasions, it may be less important at
the community scale because of the widespread
occurrence of soil disturbance in many California
environments.
Evidence for the importance of propagule
supply
Although the number of arriving propagules is an
obvious factor influencing the rate of invasion of a
system, few studies have explored the importance
of propagule supply to invasion into California
ecosystems, particularly by plants. The already
discussed studies of Harrison showing that small
serpentine patches are more invaded than large
ones and of Levine, showing that downstream
assemblages along the Eel River are more invaded
than those upstream, provide some of the best evidence for the role of propagule supply in
California. We could find no study that directly
measured the supply of propagules to an entire
ecosystem or across several sites and attributed
patterns of invasion to variation in supply rates.
Evidence from other systems for the importance
of propagule supply comes largely from the purposeful introductions of birds and biological control agents. This work has demonstrated that the
number of introduced propagules is the greatest
predictor of invasion success (Newsome & Noble,
1986; Crawley, 1989; Hopper & Roush, 1993;
Veltman et al., 1996; Duncan, 1997; Green, 1997).
Nevertheless, the application of these studies to
natural communities and those in California is
questionable for several reasons. These introductions are typically into highly altered ecosystems
such as agricultural fields or urban parks.
Furthermore, because of the very nature of bio-
control introductions, suitable prey items are typically abundant. Thus, it is no surprise that ecological resistance is weak. Still, a few studies of purposeful introductions do suggest that native consumers can deter the establishment of potential
invaders so resistance is not always nil in these settings (Goeden & Louda, 1976; Crawley, 1990;
Mack, 1996; Ehler, 1998). Given that a number of
factors influence patterns of invasion, only some
of which relate to ecological resistance, controlled
experimental studies of the mechanisms underlying the success or failure of biological invasions
are badly needed.
Conceptual model for approaching resistance
While we have evidence for the importance of abiotic and biotic resistance, the links between these
factors and propagule supply remains unclear. In
the following discussion we present a simple conceptual framework for examining how variation in
propagule supply should interact with ecosystem
resistance to influence the rate at which exotic
invaders enter a habitat. We separate abiotic and
biotic resistance because we believe that they
interact slightly differently with propagule pressure.
By reducing invader performance, abiotic resistance may slow the invasion process or when
extreme, may completely restrict invasion (Fig.
2a). For abiotic forms of resistance, there are likely to be thresholds of conditions above which the
probability of establishment and persistence for a
given invader is essentially zero (see discussion of
serpentine soils below). In this case no level of
propagule supply will result in invasion (Fig. 2a).
However, abiotic resistance may vary over time
providing windows of establishment. For example,
in a serpentine grassland, Hobbs and Mooney
(1991) found that during wet years gopher disturbance could promote the invasion of serpentine
grassland by non-native grasses. Presumably this
was because the harsh abiotic conditions were
lessened by increased water availability. In contrast, during average years, gopher disturbance did
not promote invasion onto serpentine.
Biotic resistance mechanisms may be strong in
any year or place but are more likely to be variable
over time and space since natural variation in herbivore populations, disturbance regimes and plant
vigor are common. As with abiotic resistance,
By contrast, when biotic resistance is strong,
increasing propagule pressure should have a strong
- - . High Propagule Supply
effect on invader establishment (Fig. 2b). High
..-..... Medium Propagule Supply
propagule supply should increase the likelihood of
plants finding refuges from herbivory or competiLow Propagule Supply
tion so unlike abiotic resistance, under high biotic
resistance, increasing propagule supply has a large
effect on the likelihood of invasion.
Once an invader is established in a site and
begins to reproduce there, seed production from
within the habitat eventually overwhelms the
influx of propagules from outside and greatly
exceeds seed supply prior to initial colonization.
With respect to the model, the invader population
can rapidly climb the propagule supply curves
(Fig. 2) and the invasion process should accelerate.
The speed at which this happens will be a function
of the reproductive biology, dispersal and dormanlncreasing Abiotic Resistance
cy characteristics of the invaders. For example,
invader seeds that require scarification or passage
through an animal gut have a low chance of ger- - . High Propagule Supply
minating if they fall passively beneath the parent
......... Medium Propagule Supply
plant (D'Antonio, 1990). For these species, influx
Low Propagule Supply
from outside the habitat may continue to be important for many years after initial invasion. This is
also true for invaders that take many years to
become reproductive, during which time control
can be enacted. By contrast, passively dispersed
species, particularly those with short juvenile periods, may only need to disperse outside the adult
\
canopy to establish. Such populations may quickly
-.-----.......-..._...accelerate propagule supply.
-----
Adding impact to the model
lncreasing Biotic Resistance
Fig. 2. Interaction of propagule supply (different lines within a graph) and ecological resistance to invasion (x axis).
Abiotic resistance may involve thresholds above which no
level of propagule supply can ove~whelmresistance (without
evolution of new genotypes). We suggest that biotic resistance factors are less likely to lead to this sort of threshold
response and that high propagule supply can overwhelm
even relatively high biotic resistance.
when biotic resistance is weak, the probability of
invasion occurring is not strongly influenced by
propagule supply - even a small number of propagules can result in successful invasion (Fig. 2b).
In discussions of community invasibility or lists
enumerating exotic species within a given region,
all established non-native species are treated as
equals. In California, fewer than 10% of the 1000+
invasive non-native species are listed by the
California Exotic Pest Plant Council (CalEPPC) as
damaging to wildland ecosystems in California
(Randall et al., 1998; D'Antonio & Haubensak,
1998). In other words, many of the invasive nonnative species in California coexist with residents
on a small scale and appear to have little effect on
their biomass. By contrast, those species on the
CalEPPC list reduce native species populations
either through some form of interference or by
altering ecosystem processes (including disturbance regime). High impact invaders should be
those species that either preempt resources freed up
by disturbance and persist and/or slowly overgrow
native species causing death or preventing the further recruitment of native species, or ones that
erode resident community resistance once they are
established. The former species rely on a disturbance trigger or death event to promote their dominance and overwhelm the survival and/or regenerative capacity of the native species. The latter group
may erode resistance by promoting a change in disturbance regime (e.g. increased fire frequency
D' Antonio & Vitousek, 1992; Mack & D' Antonio,
1998), which then causes rapid community change.
Alternatively, invaders may alter conditions for germination andlor growth of natives, causing slower,
but still significant community change. Examples
include the erosion of resident species' priority by
direct competition, or the accumulation of litter that
negatively affects native species germination or
survival (e.g. Facelli et al., 1988). As we display
graphically in our model, if resistance is eroded, the
number of propagules required for further invasion
is reduced (Fig. 3). In this way, erosion of resistance
by invaders can create positive feedbacks between
the invader and its own persistence or spread. The
existence of such feedbacks has been hypothesized
but rarely demonstrated. Feedbacks can be complex
and involve groups of invaders rather than individual species. For example, N fixing shrubs can
increase soil nitrogen (Vitousek et al., 1987; Stock
et al., 1995; Maron & Jeffries, 1999) while reducing native herbaceous cover through shading. After
their death or removal, the original abiotic conditions have been altered and the new conditions
(high soil N) contribute to success of other fastgrowing invaders that can rapidly put N into biomass and seed production. Previous research on
species impacts has not directly linked invasibility
with generation of impact and erosion of resistance.
Research Needs
Our review suggests that research is badly needed
in the following three areas: 1) Relating mechanisms of resistance at small spatial or temporal
scales to larger scale patterns. 2). Examining the
link between variation in propagule pressure and
resistance. 3). Clarifying the relationship between
invasibility and species impacts.
--.
High Propagule Supply
......... Medium Propagule Supply
Low Propagule Supply
lncreasing Abiotic Resistance
--.
High Propagule Supply
.-...... Medium Propagule Supply
Low Propagule Supply
-----...........__.
t
-
lncreasing Biotic Resistance
Fig. 3. Ecological resistance may be influenced by invaders as
they enter the system. For example, the build up of litter in
association with grass invaders in xeric environments may
increase surface soil moisture thereby increasing the likelihood of either germination or seedling survival of the invader.
1). Issues of scale. In a riparian plant community in
northern California, the second author showed
experimentally local scale resistance occurs but
does not drive community-wide patterns (Levine,
2000). To what extent is this result a function of the
specific mechanism (in this case competition)
responsible for resistance? Competition is inherent-
ly a local process subject to spatial variability in disturbance, propagule arrival and abiotic factors and
thus it may poorly control the resistance of an entire
habitat. By contrast, mobile generalist herbivores
have effects that might be more evenly distributed
across a habitat and thus herbivory by generalist
species may more strongly control community level
invasion patterns. The extent to whlch local scale
abiotic stress affects invasibility of entire habitats
will depend on microsite variation within a habitat
and temporal variation in resource availability that
might override locally induced microsite heterogeneity. Further exploration of these scale issues is
essential to establishing the relevance of the current
literature (which focuses on small scale studies of
resistance) to invasion patterns in entire ecosystems.
2. Propagule supply. We know almost nothing
about actual seed rain into most sites and since it
is very hard to measure, we need to develop and
refine the proxies that we use for it. In addition,
models linking seed supply and resistance could
generate testable insights into controls over habitat
invasion by particular types of invaders. Empirical
studies manipulating propagule pressure or simply
measuring the per capita probability of success
under different scenarios of resistance (including
manipulation of spatial and temporal variation
would be insightful.
3. Invasibility and impact. Invasibility studies and
discussions based on species lists all too often do
not separate high from low impact species. Since
less than 20% of invaders appear to have an impact
on wildland populations or ecosystems (Simberloff,
1981; D'Antonio & Haubensak, 1998), it is important to examine mechanisms controlling invasion
for high impact species. We have suggested some
hypotheses relating impact to resistance and
propagule pressure and these await further experimentation on a range of species. In particular, the
extent to which high versus low impact species
influence the interaction of resistance and propagule supply needs to be rigorously examined.
Management implications and conclusions
A greater understandng of resistance mechanisms
and propagule pressure could be used in many different management contexts. Resistance mechanisms extend the period of time during which an
invader and native species coexist, which widens
the temporal window available for control and
potentially reduces the extent of site alteration associated with invasion. Likewise, managers must
ensure that their own practices do not disrupt resistance that is already working in a site. Alpert et al.
(2000) suggest ways in whlch managers might
manipulate abiotic features of the environment to
increase stress (more or less similar to 'abiotic resistance' in our terminology) and reduce invasibility.
The identification of abiotic features that influence resistance can help set priorities for restoration. For example, native perennial dominated
grasslands that are not on serpentine soils still
exist in California (e.g. Keeley, 1993; Stromberg
& Griffin, 1996). A greater understanding of abiotic conditions that correlate with cover and diversity of native grassland species in non-serpentine
sites would aid in the identification of sites with
high potential for restoration.
Furthermore, since disturbance can either
increase or decrease the strength of community
resistance depending on the relative responses of
native and exotic species, the management of disturbance regimes can have profound impacts on
community resistance. Management practices that
introduce new disturbances to a system might erode
community resistance. Where human caused habitat
disturbance is unavoidable, disturbance should be
timed or handled in ways that decrease an invader's
ability to benefit from them. Techniques that
increase the competitiveness of natives in new disturbances, including boosting native propagule
pressure, should be more hlly explored.
The interaction of resistance mechanisms with
propagule supply is critical to better predicting
invasions. Little empirical data is available on the
ways in which invasion rates respond to an
increase in propagule number. Research is needed
on patterns of seed rain away from population tenters of invasive plants into potential habitats.
Estimates of spread rates will allow managers to
allocate resources to areas that are immediately
threatened, and away from sites which are likely to
remain uninvaded for a longer time. More generally, a better understanding of the mechanisms controlling the spread and success of invasions is an
important research goal for protecting native biological diversity in California habitats.
Acknowledgements
This manuscript benefited from discussions with
E. Berlow and T. Dudley. Comments on an earlier
draft were provided by D. Richardson, l? Alpert
and M. Rejmanek. Financial support was provided
by a National Science Foundation grant (DEB 9910008) to C.D. and a dissertation improvement
grant to J.L.
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