Introduction
Context dependence, where relationships differ in different situations,
is widespread in ecology and invasion ecology (Catford et al.2022; Pyšek et al. 2020). For example, invasion can have a
positive, negative, neutral or unimodal relationship with disturbance
(Moles et al. 2012). Such variation can make it difficult to
generalise across studies, systems and species, can prompt questions
about the validity of hypotheses, and can hamper invasive species
management. Like other subfields of ecology (Rillig et al. 2019),
most studies in invasion ecology consider only one or two factors
(Jeschke et al. 2020; Moles et al. 2012; Zhang et
al. 2022), and most invasion hypotheses only consider one or two
processes (Latombe et al. 2021). However, multiple factors can
limit species’ growth, survival and reproduction in heterogenous
environments (Farrior et al. 2013; Harpole et al. 2016;
Harpole & Tilman 2007; Tilman 1982), and unless the primary limiting
factor in a given situation is alleviated, a response to increases in
other factors will be slight or not occur (Cade et al. 1999;
Tilman 1990). For example, in a resource-limited system, increasing
species’ seed dose (or propagule pressure) will not result in increased
invasion if resource availability, rather than seed availability, is the
main factor constraining species’ abundance (Fig. 1) (Kaiser et
al. 1994). The concept of limiting factors (or environmental
constraints (Tilman 1990) or Sprengel-Liebig’s Law of the Minimum (van
der Ploeg et al. 1999)) is central to thinking in community and
restoration ecology (Farrior et al. 2013; Greet et al.2022; Seabloom 2011; Tilman 1982) (but see Danger et al. 2008),
as well as agronomy (van der Ploeg et al. 1999), but invasion
ecology typically concentrates on drivers or correlates of invasion
rather than on the factors that limit it (Catford et al. 2009;
Taylor et al. 2016). In this paper, we argue that a greater focus
on ecological mechanisms rather than ecological phenomena in invasion
ecology, and a greater focus on limiting factors specifically, will help
us better explain and anticipate context dependence and enable more
accurate predictions of invasion and its impact on native diversity.
Because species coexistence relies on species being able to invade
communities from which they are absent (Chesson 2000), increased
mechanistic understanding of invasion is central to community ecology
too.
Invasion by plant species requires seeds, resources, suitable abiotic
conditions and biotic interactions, and sufficient time and space for
populations to establish and grow; any of these factors could limit
invasion when in short supply (Catford et al. 2009; Pearsonet al. 2018). However, their relative scarcity – and thus
importance – may vary from situation to situation depending on the
species-site mixes in question. Variation in species’ life histories
means that what may limit one species may not limit another (Catfordet al. 2019; Tilman 1990). If a study considers and manipulates
multiple factors in parallel, effectively alleviating multiple limiting
factors, then the effect of these factors should become visible (Fig.
1). However, if invasion is co-limited by two essential factors but only
one limiting factor is alleviated, then otherwise positive or negative
relationships may appear neutral. Because of this, studies that
investigate multiple factors and hypotheses in combination may be more
likely to find evidence for underlying mechanisms than studies that
manipulate one factor at a time. Considering factors that are likely to
limit invasion in a given situation can help us to understand and
predict context dependence. A species-site matrix provides a structure
for considering the hierarchy and interplay of limiting factors and for
making such predictions (Fig. 1).
Imagine we have two groups of species, “fast invaders” characterised
by resource acquisitive traits, fast growth rates, high seed production
and poor competitive ability, and “slow invaders” with conservative
traits, slow growth rates, low seed production and high competitive
ability (Craven et al. 2018; Reich 2014). These species might
invade early, mid and late successional sites (Fig. 1a). Succession
theory tells us that early succession should primarily be seed-limited
and late succession resource-limited (Catford et al. 2012a;
Huston & Smith 1987). However, the extent of limitation should differ
between the two groups of species reflecting their life histories (and
associated tradeoffs, Tilman 1990), and these differences may be most
pronounced in mid-succession where seed- and resource-limitation are
less extreme. We might thus expect that fast invaders will be
resource-limited in mid succession, whereas slower-growing and less
resource-demanding slow invaders will – in the initial years of
invasion – primarily be limited by their intrinsic growth rates and
seed availability. Once we have a species-site matrix portraying the
hierarchy of limiting factors, we can then imagine how seed addition or
disturbance might modulate these conditions, revealing underlying
relationships (Fig. 1b). Where seed-limited, invader abundance should
primarily be determined by seed dose, whereas species’ competitive
ability for limiting resources and disturbance (or other actions that
increase resource availability) should largely determine the extent of
invasion when resources are limiting. Alleviating primary limiting
factors can allow effects of other, sequentially limiting factors to be
observed, thus revealing the interplay of limiting factors.
By considering factors that are likely to limit resident plant diversity
and how invasion may affect those limiting factors, we can also use the
concept of limiting factors to predict the conditions under which
invasion may reduce resident diversity (cf community diversity made up
of both residents and invaders). For example, in the very early stages
of succession, resident diversity would likely be limited by resident
seed availability and to a lesser extent by resident population growth
rates. Resident diversity in mid succession will likely be limited by a
combination of resources, seeds and growth rates, moving to
resource-limitation in late succession (Fig. 1). In the first few years
of invasion, especially when invasion is small-scale, invading plants
are unlikely to alter the seed availability or population growth rates
of resident plants, so invaders will primarily affect resident diversity
through resource competition. By consuming resources, like space, soil
nitrogen or water, plant invaders can increase the extent of resource
limitation, and thus potentially reduce the occupancy and abundance of
resident species. The diversity impacts of invasion will depend on
context though, such that invasion may have little impact on resident
species when invaders are poor competitors or when factors other than
resources primarily constrain resident diversity (i.e. plant invaders
will only reduce diversity if they effectively lower the capacity of
Liebig’s barrel; Fig. 1a).
In this study, we use a seed addition experiment in Minnesotan
grasslands to test whether the concept of limiting factors can help
predict and explain the cover abundance of two groups of invading
species and their impact on resident diversity in communities that vary
in successional stage. Our three-year experiment involves four
treatments in a partially factorial design: i) successional stage of
recipient community; ii) disturbance; iii) invader type; and iv) invader
seed dose. Invader type and community successional stage provide a
matrix of conditions where we expected the relative importance of seed-,
resource- and growth rate-limitation on invader abundance and resident
diversity to vary (Fig. 1). Invader seed dose, disturbance (which
elevates resource availability) and invader type (fast vs slow invaders)
enable us to effectively modulate invader seed-, resource- and invader
growth rate-limitation respectively and to test our predictions.
Variation in invader type and abundance in the invaded communities
enabled us to test how invasion can reduce resident diversity via its
effect on resource availability.
Through simultaneous invasion of up to 14 grassland species (10/14
native but all species formerly absent from the experimental sites), we
also examine the importance of interactions among invaders, specifically
whether resource acquisitive “fast” invaders constrain the abundance
of more conservative and competitive “slow” invaders via niche
pre-emption, or whether slow invaders constrain fast invaders via
resource competition for soil N and soil water (Catford et al.2012a). We use measures of resource availability (light at ground level,
soil moisture, soil nitrate) and, where relevant, resident species
richness to help understand the trends observed. We use “invasion” to
describe the colonisation and establishment of previously absent
(“invading”) plant species in this paper, using the term invasion in a
broad mechanistic sense (Chesson 2000; Tilman 2004). The processes that
we examine and discuss may thus relate to native species added for
restoration, range-shifting and range-expanding species, as well as
human-mediated alien species invasion and community ecology research
(Seabloom et al. 2003). To avoid confusion, we use the term
“factor” to refer to limiting factors only, and “treatment” to refer
to the four factors manipulated in the experiment.