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Do subordinate species punch
above their weight? Evidence
from above- and below-ground
Introduction
Variation in the relative abundance of species is a ubiquitous feature
of ecological communities. Understanding the link between the
relative abundance of a species and its contribution to ecosystem
function is key to predicting ecosystem stability over time or during
perturbations. According to the ‘mass ratio hypothesis’ (Grime,
1998), proportional inputs to primary production act as immediate
controls on ecosystem function and sustainability. While dominant
species are considered more important in ecosystems because of the
large amount of biomass they produce, an increasing number of
recent studies have shown that subordinate species may have a
larger influence on ecosystem functioning than their relative
abundance suggests. In particular, subordinate species can have
significant impacts on soil microbial communities (Peltzer et al.,
2009; Holdaway et al., 2011; Mariotte et al., 2013d). Growing
recognition of how belowground processes affect biodiversity,
ecosystem functioning and services (De Vries et al., 2013; Grigulis
et al., 2013; Van der Putten et al., 2013) likely explains the recent
interest in less abundant species. Nevertheless, studies of subordinate species remain scarce, largely because of the influence of the
‘mass ratio hypothesis’, which likely overestimates the role of
dominant species, as well as a lack of adequate understanding of the
distinguishing features of subordinate species. In addition to
differences in relative abundance, other characteristics may differ
between dominant and subordinate species including functional
groups, traits, resource acquisition strategies, and spatial growth.
While these differences remain poorly understood, their implications could be far reaching if subordinate species are capable of
buffering ecosystem functions against perturbations, and under
climate change.
This paper aims to reconcile theories about subordinate species
in order to provide a framework for future studies of biodiversity
effects on ecosystem functioning. I synthesize the current state of
knowledge about subordinate species and give a clear definition for
these species, I provide evidence of their functional role in
ecosystems, and I show how the importance of this group may
increase with global climate change; a topic which has not been
addressed in the literature. I address each of these issues by
including an above- and below-ground perspective, which is often
missing from studies of functional diversity. While evidence is
drawn mainly from experiments in grassland communities, the
basic principles can be applied more widely.
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Reconciling theories of subordinate species
Many studies have classified species in plant communities to
demonstrate the importance of functional groups (Wardle et al.,
2003; MacLaren & Turkington, 2010), functional traits (Lavorel
et al., 2011), relative abundance (Whittaker, 1965; Grime, 1998),
or keystone species (Lyons & Schwartz, 2001; Boeken & Shachak,
2006). These different components of biodiversity can have
different effects on ecosystem function (Hooper et al., 2005) but
are not necessarily independent. In his attempt to define the
functional role of species, Whittaker (1965) recognized that the
simplest way to classify components of biodiversity is to order
species according to their relative abundance or productivity. The
categorization of dominant, subordinate and transient species
(DST classification), suggested by Whittaker (1965), was incorporated into the ‘mass ratio hypothesis’ (Grime, 1998). Grime
suggested that dominant species would directly affect ecosystem
properties due to the large amount of biomass produced, while
subordinate species would only act as a filter, influencing
regeneration by dominants following major perturbations in
grasslands (Grime, 1998; Walker et al., 1999; Boeken & Shachak,
2006) or increasing diversity of climbing plants in forests (Garbin
et al., 2012, 2014). Grime’s classification was similar to the coresatellite species hypothesis (CSS classification; Hanksi, 1991).
These classifications were compared by Gibson et al. (1999), who
showed no difference between dominant and core species, between
intermediates and subordinates and between satellites and transient
species. Similarly, dominant species have also been referred as
competitors (Grime, 1973), foundation or matrix species (Gibson
et al., 2012) and subordinates as fugitive (Platt & Weis, 1985),
interstitial (Keddy et al., 1994), minor (Walker et al., 1999),
redundant (Rastetter & Shaver, 1996) or low abundant species.
Dominant and subordinate species intrinsically exist, as demonstrated by Olff & Bakker (1998), through a statistical test on field
data. Indeed, when considering a habitat as a homogeneous area in
term of vegetation type, and divided into a grid with small-scale
plots, subordinate species are defined as species found in most of the
plots but which never attain dominance. This means that
subordinates are interspersed within the community and can occur
at high frequency in plant communities but yield low relative cover
compared with dominant species. The selection of both speciesgroups requires using replicated plots in homogenous vegetation, in
order to include the maximum species diversity of the studied
community. By including frequency of occurrence and relative
cover, both easily measurable in the field, a generalization can be
attempted to distinguish dominant and subordinate species in
various ecosystems, summarized by a frequency–abundance curve
in Fig. 1. Dominant and subordinate species are both frequent in
plant communities and should occur in most of the plots by
contrast to transients, which generally fail to regenerate and persist
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Fig. 1 Frequency–abundance curve used for the selection of competitive
hierarchical groups in herbaceous vegetation. Dominant (1, gray area) and
subordinate (2, dark gray area) species are always present in the community
and are distinguished from transient species (3), which do not persist in the
vegetation, by a frequency > 50%. The distinction between species groups is
then based upon cumulative relative abundance (%) and has been set at an
arbitrary value of 12 to 100% for dominant, 2 to 12% for subordinate (i.e.
10% total abundance) and under 2% for transient species. (Modified, with
permission, from Mariotte et al., 2013a).
in the vegetation. The distinction between dominant and subordinate species is then based upon cumulative relative abundance
(i.e. mean relative species abundance in a site, ranked in ascending
order and cumulated for each species). As suggested by Grime
(1998), subordinate species would represent 10% of the plant
community. Based on experiment carried out in grasslands (Grime,
1998; Mariotte et al., 2012, 2013a,b,c,d) and shrublands
(Kichenin et al., 2013), I suggest that species with a cumulative
relative abundance below 2% should be considered as transients,
comprised between 2% and 12% as subordinates (i.e. 10%) and
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> 12% as dominants (Fig. 1). This species selection has been set at
arbitrary values and principally tested in grasslands. Nevertheless,
this gives a first attempt to generalize the DST classification and
provides basis for further research in a broad range of ecosystems.
While relative abundance has been the main factor differentiating species-groups, more recent studies suggest that dominant
and subordinate may also diverge in several other characteristics.
For example, dominant and subordinate species vary in their
morphology and functional traits (Grime, 1998; Peltzer et al.,
2009; Doherty et al., 2011; Mariotte et al., 2013d); dominant
species are generally taller with large leaves (i.e. high canopy height,
specific leaf area (SLA), leaf area, leaf N) allowing better light
capture, while subordinate species are smaller in stature with small
leaves (i.e. opposite traits; Table 1). Traits of dominant species
reflect a strategy for rapid acquisition of resources, while those of
subordinate species are associated with resource conservation
(Grime et al., 1997; Diaz et al., 2004; Mariotte et al., 2013d).
Above-ground, the differences between the species-groups result in
a trade-off between biomass production of dominants and nutrient
retention of subordinates (Lavorel et al., 2011). Below-ground,
traits of dominant species such as high litter quality promote
bacterial-dominated communities with fast microbial activities
while those of subordinates (i.e. low litter quality) favor fungaldominated communities with slower activities (De Vries et al.,
2012a; Grigulis et al., 2013). Trait differences between dominant
and subordinate species arise principally from grasslands but there
are also few examples for forest ecosystems. For example, dominant
woody species in forest communities are associated with two aboveground plant traits, high height and high shade tolerance (Koide,
2001), while subordinate woody species had relatively higher root
nutrient content (nitrogen (N) and phosphorus (P)), thicker root
diameter and more root hairs than dominants (Holdaway et al.,
2011). Similarly, the dominance of climbing species in forest has
been associated to shade-tolerance with high photosynthetic rate
and low dark respiration (Gianoli et al., 2012) reflecting a strategy
of maximizing exploitation of resource availability. The classification of dominant and subordinate is then intimately related to the
plant economics spectrum research discussed earlier, except that
studies on plant functional traits focus principally on dominant
Table 1 Characteristics of subordinate and dominant species in grassland ecosystems
Previous denomination
Competitive abilities
Relative biomass proportion
Deterministic processes
Plant traits
Resource strategy
Above-ground trade-off
Below-ground trade-off
Spatial growth
Subordinate
Dominant
Fugitive, intermediaries, interstitial, minor, rare, redundant or
low abundant species
Low
Low but numerous individuals
Niche differentiation
High functional dissimilarity
Low stature, SLA, leaf area, leaf N, High root N, P
Conservation
Nutrient retention
Low-quality litter
Fungal-dominated communities
Slow microbial activity
Aggregated
Competitor, foundation, matrix or core species
High
High but few in number
Habitat filtering
High functional similarity
High canopy height, SLA, leaf N, Low root N, P
Acquisition
Biomass production
High-quality litter
Bacterial-dominated communities
Rapid microbial activity
Random
SLA, specific leaf area.
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species (e.g. species making up 80% of cumulated biomass; Garnier
et al., 2007; Lavorel et al., 2011) by analogy to the ‘mass ratio
hypothesis’. Moreover, while measuring plant functional traits
(leaves and roots) is constraining, destructive or somehow expensive, determining dominant and subordinate species based on
frequency and relative cover in the field (see earlier), would be a
simplified and more rapid method to estimate functional diversity
and resource capture strategy of all species in the plant community.
Differences in resource capture strategies between dominant and
subordinate species are also associated with spatial niche differentiation and complementarity for resource use (Von Felten et al.,
2009). Moreover, due to fast growth and rapid acquisition of
resources, dominant species can displace subordinates from
occupied patches but subordinates cannot displace dominants
(Tilman, 1994; Amarasekare, 2003). Using a multidimensional
trait-based approach, Maire et al. (2012) showed that within
competitive plant communities, dominant species are mainly
affected by habitat filtering (i.e. ecological filters selecting species
with suitable traits for a given habitat), while subordinate species are
stabilized by niche differentiation. These findings suggest that
co-dominant species should be functionally similar and occupy the
same ecological niches while subordinate species should be
functionally dissimilar and occupy multiple niches dependent on
specific abilities for soil nutrient preemption (Werger et al., 2002;
Dassler et al., 2008) or different phenology (Catorci et al., 2012).
This implies also that systems with multiple niches would promote
communities composed essentially of subordinate species, while
systems with low niche availability would promote dominance of
few dominant species. When habitat filtering is weak relative to
niche differentiation, subordinate species, favored by size-asymmetry (Hodge et al., 1996; Latenzi et al., 2012), usually grow in
patches between or under the canopy of randomly growing
dominants (Liancourt et al., 2009; Lamosova et al., 2010). This
aggregated pattern seems to reduce exclusion of these less
competitive species, at short-term (Wassmuth et al., 2009;
Lamosova et al., 2010) and long-term (Porensky et al., 2012),
promoting subordinate’s persistence in plant community. Intraspecific aggregation also prevents dominant species from moving
into patches colonized by subordinate species, or at least slow down
subordinate’s displacement by better competitors (Racz & Karsai,
2006).
By connecting recent studies and theories with existing literature
on the DST classification, two patterns emerge. First, differences in
morphology, functional traits and resource acquisition strategies
that are correlated with relative abundance are likely to produce sets
of characteristics that are predictably associated with dominant and
subordinate species, and these characteristics may be generalizable
across a broad range of ecosystem types. However, it should be
noted that, because plant traits, competitive abilities and niche
differentiation are influenced by environmental factors (Koide,
2001; Wellstein et al., 2013), a species can be simultaneously
subordinate in a site and dominant in another depending on
specific conditions. Second, recent evidence supports a much
stronger functional role for subordinate species than Grime (1998)
originally envisioned, suggesting that relative abundance alone
cannot be used to predict ecosystem function for all species groups.
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Functional role of subordinate species: a new
framework
While communities are generally dominated by few dominant
species, the range and number of subordinate species is highly
variable and considerably influences plant diversity (i.e. species
richness). The number of subordinate species strongly varies with
disturbance (e.g. resources, burning, drought), and follows a
humped-back model with a higher proportion of subordinates at
intermediate levels of disturbance (Fig. 2; Grime, 1973; Pierce
et al., 2007; Mariotte et al., 2013a). Other factors may then modify
the amplitude of this curve, such as selective grazing (De Deyn
et al., 2003; Van der Putten, 2005; McCain et al., 2010), trampling
(Kohler et al., 2006; Mariotte et al., 2012) or mycorrhizas (see
mutualism–parasitism continuum; Van der Heijden et al., 1998;
Urcelay & Diaz, 2003; Mariotte et al., 2013b), depending on their
relative influence on dominant and subordinate species. By
conditioning the persistence of subordinate species, disturbance
factors restrict the range of situations in which these species can be
functionally important relative to dominants (e.g. species-rich
communities with intermediate levels of resources).
Based on specific plant traits, subordinate plant species may have
larger impacts on ecosystem functioning than expected, especially
below-ground. Indeed, fungal-dominated communities favored by
subordinate species are known to reduce N leaching (De Vries et al.,
2011) and to maintain productivity over the long-term. Using a
3-yr removal experiment, Mariotte et al. (2013d) demonstrated
that subordinate species were associated with distinct bacterial and
arbuscular mycorrhizal fungal communities, and improved plant
productivity through positive plant–soil feedbacks (see also Mikola
et al., 2002; Van der Putten, 2005). Similarly, Peltzer et al. (2009)
highlighted the disproportionate influence of nonnative subordinate species on soil biota compared with dominant species. As
illustrated by Grime (1998), the ‘mass ratio hypothesis’ is restricted
in application to the role of plants, and the impacts of other trophic
elements (bacteria, pathogens, symbionts) on ecosystem processes
are less predictably dependent on their abundance (see also Urcelay
et al., 2009). Therefore, the influence of subordinates on belowground communities may be disproportionate to their relative
abundance, and the effect on ecosystem function may be large even
when the proportion of the total microbial biomass involved is low.
The specific impacts of subordinate species on soil microbial
Fig. 2 Relationships between species diversity and disturbance as
highlighted by Grime (1987). The humped-back model includes the relative
proportion of the three components of plant biodiversity: dominant (1),
subordinate (2) and transient (3) species along the disturbance gradient (e.g.
resources including water, nutrients, light, etc.), according to Grime (1973,
1987) and Mariotte et al. (2013a).
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communities have important implications for soil processes and
nutrient cycling (Grigulis et al., 2013) and recent research from
De Deyn et al. (2009, 2011) in grasslands showed that a single
subordinate species (Trifolium pratense) improved soil C and N
storage, whereas a second subordinate (Achillea millefolium) promoted nutrient sequestration in plant tissue. Together, these findings
slightly modify the ‘mass ratio hypothesis’ (Grime, 1998) by showing
that, not only dominant species, but also low-biomass subordinates,
may greatly influence ecosystem processes and functioning.
The functional importance of subordinate species has been
mainly investigated through the lens of compensatory dynamics
and ecosystem stability (Adler & Bradford, 2002; Suding et al.,
2006). If interspecific competition maintains dominance and
functional redundancy is high, as expected in species-rich plant
communities, better resistant subordinate species should be able to
compensate for any loss of dominant species by release from
competition (Adler & Bradford, 2002). The increasing interest in
climate change has given a new importance to this process through
the insurance hypothesis (Yachi & Loreau, 1999). Recent findings
suggest a significant role of subordinate species in the resistance of
plant communities to climate change. Results of a mesocosm
experiment (Kardol et al., 2010) and a field experiment in
mountain grassland (Mariotte et al., 2013c) showed that subordinate species increased their biomass production during drought
and enhanced community stability. Both studies suggested that
dominant species responded most strongly to the direct impacts of
drought, whereas subordinate species were more resistant to
drought, and responded to reduced competition with the dominant
species. Interestingly, the fungal-based soil food webs associated
with subordinate species have also been shown to be more resistant
to drought than the bacterial-based food webs found with
dominant species (De Vries et al., 2012b). This finding suggests
that plant–soil feedbacks and litter promote more resistant fungal
communities (e.g. mycorrhiza), which then improve the resistance
of subordinates against perturbations. The resistance of subordinate species to climate change is not limited to drought; similar
responses have also been observed under warming in sub-arctic
dwarf shrub community (Richardson et al., 2002), and under
elevated carbon dioxide (CO2) (Navas et al., 1997; St€ocklin &
K€orner, 1999; Maestre et al., 2005). In both cases, subordinate
species improved biomass production and N uptake, suggesting
that subordinates can increase their biomass relative to dominant
species when resources (e.g. water, CO2) increase in initially low
resource systems, or when resources decrease in initially high
resource systems (Fig. 3). Therefore, while subordinate species are
expected to have greater effects on ecosystem functioning at
intermediate resource levels where they are most abundant, these
species may become more important at low and high resource levels
under climatic perturbations (Fig. 3) and may compensate for the
loss of less resistant species to improve stability. However, findings
on subordinate species are still scarce and while the abundance of
subordinate species seems to be related to resources, less is known
about the functional importance of subordinates in relation to soil
microbial communities along the resource gradient. This is also not
entirely clear if the higher resistance of plant communities to
climate change is related to higher abundance of subordinates or
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Forum 19
Fig. 3 Conceptual model representing the dominance–rank curve (dominant
(D) vs subordinate (S)) in function of available resource (e.g. water, CO2, etc.)
and changes induced by a shift (increase or decrease) in resources. The dotted
box summarizes cases where subordinate species are expected to be
functionally important (i.e. subordinate insurance hypothesis) either due to
an increase in abundance or biomass, depending on the initial resource state
and the direction of resource shifts. Gray boxes highlight cases forecasted
under climate change, such as an increase in a resource that is typically scarce
in a particular ecosystem (e.g. an increase in spring rainfall in Mediterranean
areas) or a reduction in a resource that is typically abundant (e.g. a decrease in
summer precipitation in temperate ecosystems).
only to the presence of one or few subordinate species. Determining
the mechanisms of resistance and resilience to climate change is an
important contemporary theme of research at broad scale and the
relative abundance of subordinate species in plant communities
might explain, at least partially, why some communities are more
resistant than others. Future experiments utilizing the new
framework presented here (Fig. 3) could easily test the functional
role of subordinate species under present and projected climate in a
large range of ecosystems and environmental conditions to draw
more general patterns for the functional role of these species.
Future directions
The recognition of ecosystem-level effects of subordinate species is
recent, probably because their effects were missed in experiments
with randomly assembled communities (Bardgett & Wardle,
2010), which generally neglect the relative abundance of species
and functional traits in the community. By synthesizing existing
knowledge on this species-group, this paper addresses these issues
and highlights the ‘subordinate insurance hypothesis’, suggesting
that subordinate species may assist dominant species or compensate
for their loss on ecosystem functions. Without refuting the ‘mass
ratio hypothesis’, this synthesis shows that subordinate species also
matter in ecosystems and emphasizes the importance of
below-ground processes, which remain poorly understood. For
example, the specific root-associated microbial communities and
below-ground traits of subordinates have not been well studied.
Another aspect to be considered is the functional effect of a single
subordinate (i.e. species identity) vs the effects of several subordinate species (i.e. species-group). By using the new framework
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presented here, future research should assess these mechanisms to
understand whether and to what extent subordinate species may
buffer or stabilize ecosystem functions under climate change. This
shall definitely include (1) whether higher community resistance is
related to higher number of subordinates at intermediate resource
level or whether one single or few subordinate species at high and
low resource levels may also compensate for the loss of dominant
species, (2) whether the role of subordinate species is similar under
different environmental conditions and (3) whether traits of
subordinate species change under climate perturbations to fulfill
the same functions than dominant species. The classification of
dominant, subordinate and transient species is well adapted to a
range of ecosystems (e.g. forests, grasslands, wetlands, etc.) and
given the key role of subordinate species where they have been
studied, future challenges include determining their importance at
a broader scale and for multiple ecosystem functions, in order to
better understand patterns of functional diversity.
Acknowledgements
The author is grateful to Katharine Suding, Paul Kardol, Emily
Farrer, Erica Spotswood, Lauren Hallett and Alexandre Buttler for
their assistance in the writing of this paper and to the Swiss National
Science Foundation, which supported the research (no. 31003A
114139 and PBELP3 146538).
Pierre Mariotte
Department of Environmental Science, Policy and Management,
University of California Berkeley, Berkeley, CA 94720, USA
(tel +1 5107171526; email [email protected])
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Key words: climate change, competitive hierarchical groups, ecosystem
functioning, fungal-based food webs, plant–soil feedbacks, subordinate and
dominant species, subordinate insurance hypothesis.
New Phytologist (2014) 203: 16–21
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