Journal of Ecology 2010, 98, 1269–1275
doi: 10.1111/j.1365-2745.2010.01709.x
FORUM
Strong facilitation in mild environments: the stress
gradient hypothesis revisited
Milena Holmgren1* and Marten Scheffer2
1
Resource Ecology Group, Wageningen University, P.O. Box 47, 6700 AA, Wageningen, The Netherlands; and
Aquatic Ecology and Water Quality Management Group, Wageningen University, P.O. Box 8080, 6700 DD
Wageningen, The Netherlands
2
Summary
1. The idea that the role of facilitative interactions increases as environmental conditions become
more stressful has become a ruling paradigm in ecology. Here, we review three reasons why positive
interactions may actually be more prominent than generally thought under moderately stressful
rather than under extreme conditions.
2. First, there is evidence that in some communities the net effect of amelioration of shortage of a
limiting resource, such as water under the canopy of nurse plants, may be beneficial under moderate
conditions whereas it can be overruled by increased competition for the same resource in very harsh
environments.
3. Secondly, we show that even in situations where the relative role of facilitation increases monotonically with stress, the absolute effect should as a rule be largest at intermediately stressful conditions. This is because under the harshest conditions, facilitative amelioration of conditions is
insufficient to allow growth altogether. Therefore, while facilitation will expand the range of conditions where an organism may occur, the largest absolute effects on biomass will always occur under
less stressful conditions.
4. A third reason why facilitation may be more important under moderate conditions than previously thought is that in any ecosystem, the suite of organisms is adapted to local conditions. This
implies that even under conditions that appear benign, facilitation may play an unexpectedly large
role as organisms are simply more sensitive than those found under harsher overall conditions.
5. Synthesis. We argue that while facilitation will extend the range of conditions where an organism
can occur, it should also boost performance of the species well into the more moderate range of conditions. Broadening our search image for facilitative effects towards milder environments will reveal
wider than expected prevalence of positive interactions and their effects on stability and diversity in
nature.
Key-words: abiotic amelioration, community, competition, grazing, herbivore, nurse plant,
plant–plant interactions, positive interaction, predator, stress
Introduction
The recognition of the ubiquitous role played by facilitation in
the organization of ecological communities has major implications for theoretical frameworks in ecology (Bruno,
Stachowicz & Bertness 2003). In an influential article, Bertness
& Callaway (1994) predicted the role of facilitative interactions
to increase with the harshness of abiotic or biotic challenges to
species. Many studies have confirmed this stress gradient
hypothesis (SGH; Callaway 2007). While most work has
*Correspondence author. E-mail: milena.holmgren@wur.nl
focused on plant communities (Callaway 2007), results from
animal communities tend to be in line with the SGH as well.
For instance, in sessile marine animal communities facilitation
is more prevalent under harsher conditions (Bertness et al.
1999; Stachowicz 2001; Kawai & Tokeshi 2007), and in terrestrial herbivore assemblages small grazers depend on larger
ones on sites dominated by nutritionally low quality forage,
where larger grazers are essential to promote high quality
regrowth (Arsenault & Owen-Smith 2002).
The reasons to expect facilitation under more extreme conditions are intuitively straightforward. Facilitative amelioration of a given stressor is obviously more important if that
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1270 M. Holmgren & M. Scheffer
stressor is more severe. Together with the fact that facilitating
species always have negative impacts as well, this explains why
the role of facilitation will tend to diminish as conditions
become more benign, and competition will become prevalent
(Holmgren, Scheffer & Huston 1997).
The empirical research inspired by the SGH conceptual
model has led to rather diverse outcomes depending on the
interacting species (Callaway 2007), their ontogenic stage
(Miriti 2006; Nuñez et al. 2009), the indicators used to evaluate
plant performance (Gómez-Aparicio et al. 2005), the type of
stress factor (Kawai & Tokeshi 2007) and the magnitude of
the stress imposed (Kitzberger, Steinaker & Veblen 2000;
Tielbörger & Kadmon 2000; Callaway et al. 2002; Maestre &
Cortina 2004; Holzapfel et al. 2006). This has stimulated
considerable debate in plant ecology (Maestre, Valladares &
Reynolds 2005, 2006; Lortie & Callaway 2006) and has motivated refinements to the original SGH model. Based on the
classical work of Grime (1979), Michalet et al. (2006) reasoned
that the facilitation effects would depend on the life history of
the interacting species (stress tolerance vs. competitive ability
of benefactor and beneficiary) and that contrary to what is
expected by the SGH model, facilitative interactions would
probably be insufficient to expand the niche of stress-intolerant
competitive species under the most stressful conditions, resulting in a decline in species diversity towards the most stressful
end of an environmental gradient. Later on, Maestre et al.
(2009) expanded these ideas with predictions that fall largely
into two categories: (i) facilitation is predicted to increase with
stressfulness of conditions when the abiotic stress gradient is
not driven by resource limitation (e.g. temperature) or when
the beneficiary (facilitated) species is stress tolerant; and (ii) a
hump-shaped model with negative interactions overruling
facilitation at both ends of the stress gradient is predicted especially when the stress gradient is driven by a resource, such as
water or when both benefactor and beneficiary species have
similar life histories.
These refinements to the SGH model are thought provoking. However, as acknowledged by Maestre et al. (2009),
detailed predictions are difficult without a mechanistic understanding of the nature of the stress, the effects of the benefactor
species on the stress and the ecophysiological tolerances of the
interacting species to the stress. In this article, we use a simple
model based on the response of plants to water and light and
the effects of plants on the availability of these two resources,
to argue that the effects of facilitation may often be more
important under relatively benign conditions than in the most
stressful situations. Although this point has been made earlier
for particular dry plant communities, where the positive effect
of nurse plant canopies on microsite microclimate conditions
can be overruled by negative effects of competition for soil
water (Maestre et al. 2009), we will demonstrate that this can
be generalized. We will first show that irrespective of whether
the relative effect of facilitation declines at the extreme end of
the range of conditions or not, the absolute effect of facilitation
on performance will be largest under moderately stressful conditions. Subsequently, we will argue that if we compare across
regions at larger scales, facilitation will tend to be important
in regions where conditions may seem benign at first glance,
simply because organisms adapted to such environments are
more sensitive to stress. Our conceptual model is based on two
key resources widely studied by plant ecologists, but as we will
discuss later, the basic results can be expanded to understand
the role of other stressors.
Absolute and relative facilitation effects along
stress gradients
A GRAPHICAL MODEL
We will illustrate what may happen to the absolute and relative
effects of facilitation along a stress gradient, using a graphical
model of the effects of nurse plants (benefactor) on water and
light for small plants, such as seedlings growing in their vicinity
(beneficiaries). While numerous forms of facilitation are widespread across the plant and animal kingdoms, a particularly
large number of studies address this type of facilitation in plant
communities (Callaway 2007). It has often been shown that in
dry environments, shading by nurse plants may promote
growth and survival of plants in the understorey through positive effects on water conditions (Holmgren, Scheffer & Huston
1997). In contrast, light limitation may negatively impact the
beneficiaries if the canopy of the benefactor becomes denser
(Forseth, Wait & Casper 2001; Valladares & Pearcy 2002), and
in some dry environments competition for soil moisture may
counteract the positive effects of reduced transpiration rates
often found under the canopy (Valladares et al. 2008).
Following earlier work (Holmgren, Scheffer & Huston
1997; Holmgren 2000), we assume that growth of a plant
increases with the availability of water and light (Fig. 1a). We
also assume that along gradients from under the canopy of a
nurse plant to the open, light will increase, but microsite moisture availability will simultaneously decrease. Microsite moisture is used here as the combined effect of microclimatic
conditions and soil water availability on plant water relations.
In the model (Fig. 1a), four hypothetical gradients from the
canopy to the open are represented by dashed lines (I–IV).
Each line represents the gradient in a different climatic situation, from mesic (I) to xeric (IV). The relationship between microsite light and microsite moisture along the gradients is
reflected in the projections of the four curves on the bottom
plane. In our first situation (Fig. 1a), we assume that the relative change in microsite moisture along the gradient from the
open to the canopy is smallest in the most mesic areas (e.g. a
very rainy temperate climate) and strongest in the driest areas.
It can be seen from this representation that in dry areas
(curve III), the positive effect of improved moisture may overrule the negative effects of shade over part of the gradient from
the open to the canopy. As a result, maximum growth (gopt
open dots) may appear under a certain optimal level of canopy
protection. Since microsite moisture nevertheless decreases
with overall drought in an area, the expected gains from facilitative canopy shade eventually decline to zero as we go to xeric
environments (curve IV; also, protective canopies will become
increasingly sparse in more xeric environments, limiting the
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Strong facilitation in mild environments 1271
(a)
(a)
(b)
(c)
(b)
(d)
Fig. 1. Graphical model to illustrate how the growth of seedlings
may change along gradients from the canopy to the open (curves I–
IV in both a and b). The surface (a) represents growth as a function of
light and moisture conditions, assuming a physiological trade-off
between drought tolerance and shade tolerance (Holmgren, Scheffer
& Huston 1997). From the canopy to the open, light increases, but
depending on overall climatic conditions, microsite moisture available to the seedlings decreases. Curves I–IV in both (a) and (b) represent the growth response of seedlings to such correlated changes in
light and moisture in four different kinds of environment, from mesic
(I) to xeric (IV). The effect of increasingly dry conditions can be seen
from the difference between growth in the open (g0) and growth under
an optimal facilitative canopy (gopt) in (b).
shading gradient that will be found). The expected effect of
regional climate on the growth of seedlings along a gradient
from dense canopy to the open can be compared more easily
by plotting the growth curves (I through IV) in two dimensions
(Fig. 1b).
To see how this affects overall facilitative effects, we consider the difference between growth in the open (g0) and
growth under an optimal facilitative canopy (gopt) (Fig. 2a).
This representation reveals that the largest gain in absolute
growth should be expected under intermediate climatic conditions (Fig. 2b). There are, however, different ways to quantify
the net effect of one species on another. It is common to use a
relative indicator of interaction strength. A problem if we want
to apply such measures to facilitation under harsh conditions
is that growth in the absence of facilitation goes to zero. As a
result, the classical Relative Competition Index (Wilson &
Fig. 2. Magnitude of the maximum facilitative effect going from a
mesic to a xeric climate inferred from the model presented in Fig. 1.
The absolute difference between growth in the open and growth at
the optimal level of shade is predicted to be highest under intermediately dry climate conditions (a and b). The relative effect of the canopy measured as the Relative Competition Index (RCI) goes to
infinity as growth in the open goes to zero (c). Relative measures of
interaction strength avoiding this effect, such as the Relative Neighbour Index (RNE) tend asymptotically to 1 (the maximum) (d)
despite the fact that absolute facilitative effects become negligible
(see (b)).
Keddy (1986), which puts biomass in the absence of the interaction effect in the denominator, tends to infinity (Fig. 2c).
Therefore, other indicators have been proposed more recently,
such as the Relative Neighbour Index (Markham & Chanway
1996) and the Relative Interaction Intensity index (Armas, Ordiales & Pugnaire 2004). These tend to a maximum effect of 1
rather than going to infinity (Fig. 2d). Clearly, to make generalizations across environments and species groups we need to
quantify the magnitude of interactions between species in a
way that allows comparisons. This is an advantage of such relative measures. However, it might be argued that this way of
quantifying the role of facilitation overstates the effect of facilitation in harsh environments, as for all practical purposes,
measurable facilitation effects will disappear there.
CASES WHERE COMPETITION INCREASES UNDER
EXTREME CONDITIONS
Microsite moisture conditions in the understorey result from
several mechanisms. Although plant canopies often have
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1272 M. Holmgren & M. Scheffer
cooler and moister air that ameliorates transpiration rates
and plant water stress, soil water conditions are more variable. Soil water availability in the understorey results from
mechanisms that can act in opposite directions with a net
result that is not easily predictable. Lower evaporative
demands, improved soil water infiltration and active hydraulic lift all have positive effects on soil water availability in the
understorey. However, canopy interception can reduce the
amount of water reaching the soil and root competition for
water can make understoreys drier than open patches. These
negative effects on soil water availability can potentially
override the positive ones and as a consequence make conditions drier in shade. So, while the effect of nurse plants on
microclimatic conditions is often positive for plants in the
understorey, competition for soil moisture may work in the
opposite direction. As a result, the net effect of nurse plants
on water conditions may be neutral or actually become
negative under very dry conditions (Aguiar & Sala 1994;
Kitzberger, Steinaker & Veblen 2000; Tielbörger & Kadmon
2000; Maestre & Cortina 2004; Valladares et al. 2008). In
our graphical model, this situation may be represented by
assuming that in xeric systems microsite moisture does not
increase along the light gradient from the open to the canopy
(Fig. 3a). As a result, the facilitative effect disappears in the
driest systems, and not only the absolute effect, but also the
relative effect of facilitation is highest under moderate conditions (Fig. 4). Some empirical studies have found this humpshaped pattern. For example, Maestre & Cortina (2004)
compared the net effect of the tussock grass Stipa tenacissima
on the shrub Pistacia lentiscus at 10 experimental sites across
a gradient of accumulated rainfall in semi-arid Mediterranean steppes. They found that competitive interactions dominated at both extremes of the gradient, whereas facilitation
was found under intermediate conditions. In conclusion, our
analysis supports the assertion that facilitation may be most
important at intermediate stress levels (Michalet et al. 2006;
Maestre et al. 2009). However, it also shows that with
respect to relative facilitative effects on growth, this humpshaped pattern is probably limited to particular cases where
competition increases under extreme conditions. In contrast,
(a)
(a)
(b)
(c)
(b)
(d)
Fig. 3. As Fig. 1, but assuming that under the driest condition, the
net increase of microsite moisture along the gradient from the open to
the canopy is lost because of increased competition for soil moisture
(see text for further explanation).
Fig. 4. As Fig. 2, but assuming (as in Fig. 3) that under the driest
condition, the net increase of microsite moisture along the gradient
from the open to the canopy is lost because of increased competition
for soil moisture. The dashed vertical line indicates the point in the climatic gradient where the canopy has no net positive effect anymore
(gop = g0), and therefore marks the border of the range of conditions
for which facilitation is found.
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Strong facilitation in mild environments 1273
we predict that absolute effects of facilitation will always be
highest in moderately stressful rather than extreme environments.
BEYOND ABIOTIC STRESS AMELIORATION AND
RESOURCE ACQUISITION
Facilitative interactions in plant communities are not only
owing to amelioration of harsh abiotic conditions or improvement of resource acquisition, but also commonly arise from
protection against herbivores (also called ‘associational
defence’) (Atsatt & O’Dowd 1976). Switches from competitive
to facilitative interactions at increasing grazing pressure have
been clearly demonstrated in Mediterranean ecosystems
(Baraza, Zamora & Hodar 2006), heather vegetation (Brooker
et al. 2006), Alps woodlands (Smit et al. 2007) and the Patagonian steppe (Graff, Aguiar & Chaneton 2007). It is easy to
imagine that in most plant communities a net positive effect of
facilitation by herbivore protection cannot be expected at very
high herbivore density simply because herbivores would eat
anything available, including less palatable protective nurse
plants. In contrast, at very low herbivore density not much is
to be gained, and competition for resources among neighbouring plants will probably override the small protective effects
against potential herbivore damage. Indeed, several studies
illustrate that such protection against grazing tends to have the
most effect at intermediate herbivore pressure (Brooker et al.
2006; Smit et al. 2007).
In summary, while our graphical model (Figs 1–4) highlights one particular example, various studies illustrate that
facilitative interactions may ameliorate stressful conditions
only within a certain range. At low levels of stress, positive
effects may typically be overruled by competitive impacts,
whereas at high stress levels organisms will typically be unable
to produce sufficient amelioration to facilitate the survival and
growth of others. We therefore predict the maximum absolute
effect of facilitation (in terms of biomass gain) to be found
under relatively moderate conditions rather than under the
most stressful conditions. This implies that, while facilitation
can expand the range of conditions where organisms may
occur (as stressed in earlier work), performance may be
boosted most strongly under more moderate conditions.
Facilitation under seemingly benign conditions
The general focus on the role of positive interactions under
harsh conditions also carries some risk of introducing myopia when it comes to our search image for facilitation. For
instance, isolated studies have demonstrated that facilitation
through shading is essential for seedlings, even in relatively
moist regions, such as former rain forest land of central
Amazonia (Vieira, Uhl & Nepstad 1994; Ganade & Brown
2002) and New Caledonia (Rigg et al. 2002), temperate
deciduous forests (Simard & Vyse 2006) or riparian forests
(Shararn et al. 2009). At first sight, this may seem surprising
as most of the literature is on the effect of nurse plants in
stressful (dry or alpine) ecosystems of the world. However,
Fig. 5. Schematic representation of the role of facilitative amelioration of water stress in plant communities. In wetter climate zones,
microsite conditions tend to be wetter, but species (represented by
Gaussian niche curves) are also adapted to wetter conditions than
those found in dry climates. As a result, the range of conditions under
which species experience water stress that may be ameliorated by a
canopy (grey zone) changes with climate. In mesic ecosystems, species
that depend on canopy protection (grey Gaussians) occur under
much wetter microsite conditions than in xeric ecosystems.
the suite of organisms present in a given ecosystem is of
course adapted to the local conditions (Fig. 5). Therefore,
apparently minor deviations from the optimal conditions
can impose a large stress. Even in tropical and temperate
forests where light availability by treefall gaps plays a key
role in the maintenance of species diversity, seedlings of the
shade-tolerant species that characterize these forests may be
unable to grow in larger gaps (Hoffmann 2000; Ganade &
Brown 2002). Tropical rain forest species tend to have large
leaf area ratio and specific leaf area which increase their vulnerability to higher temperature and water deficit found at
higher irradiance. Recent analysis of restoration attempts
across ecosystems shows that indeed facilitative interactions
play a key role in explaining the success of plant regeneration in tropical and temperate ecosystems (Gómez-Aparicio
2009). While few studies have addressed such situations, one
may imagine that in a general sense similar patterns might
occur in a wide range of ecosystems (Fig. 5). In a broader
context, this also applies for facilitation along grazing pressure gradients where the most sensitive species to grazing are
expected to benefit more from associational defence provided
by neighbours and to respond more strongly to increasing
levels of grazing pressure. Recent field experimental results
point in this direction (Vandenberghe et al. 2009).
Synthesis
While the role of facilitative interactions has been recognized
as a key-structuring force in plant communities early on
(Clements 1916), most of our theoretical thinking has long
been dominated by competition. Bertness & Callaway (1994)
catalysed a change by providing the SGH that has inspired
much empirical research in plant communities (Callaway 2007;
Brooker et al. 2008). This clear and simple conceptual model
helped to attract attention to positive interactions in a literature dominated by thinking about competition and predation.
Simple theoretical models in ecology have historically played a
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1274 M. Holmgren & M. Scheffer
key-catalysing role in advancing our understanding and stimulating research. However, as with any scientific theory, such
models can invoke myopia (Chamberlin 1897; Carpenter et al.
2008). The eye-opening SGH has led to a focus on extreme
environments in the search for facilitation effects. Some
authors have already pointed out that in particular cases
competition may overwhelm facilitative effects when conditions become very harsh (Michalet et al. 2006; Maestre et al.
2009). However, we argue that it may be the rule rather than
the exception to find large facilitation effects under moderate
rather than extreme conditions. One reason is that, as growth
tends to zero under the most extreme conditions, the absolute
positive effects on growth and survival will typically be largest
at intermediate conditions (Fig. 2). A quite independent reason why facilitation is more important than one might expect
under the moderate conditions in moister ecosystems is the relatively lower drought tolerance of the plants species adapted to
these environments. In seemingly benign environments organisms will tend to be more sensitive to stress, and may depend
on facilitation more than we would expect at first sight
(Fig. 5). As facilitation has fundamental implications for the
stability and functioning of communities (Butterfield 2009), it
is important to recognize that the role of facilitation is not limited to extreme environments. A too-narrow focus on extreme
environments would bias our view of the overall role of facilitation in ecological communities.
Acknowledgements
Thanks to Mark Bertness and Frank van Langevelde for inspiring discussions,
to Fernando Maestre, Rene van der Wal and Rob Brooker for constructive criticism and to the British Ecological Society for the invitation to present these
ideas during the British Ecological Society Symposium: Facilitation in Plant
Communities (20–22 April 2009). M. H. thanks the Dutch NWO Meervoud
Programme (836.05.021).
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Received 8 May 2009; Accepted 5 July 2010
Handling Editor: Rob Brooker
Ó 2010 The Authors. Journal compilation Ó 2010 British Ecological Society, Journal of Ecology, 98, 1269–1275
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